Bird Coloration: Function and Evolution 9780674273818

Citation preview

bird coloration

Bird Coloration volume 2

Function and Evolution

edited by

Geoffrey E. Hill and Kevin J. McGraw

harvard universit y press Cambridge, Massachusetts London, England • 2006

Copyright © 2006 by the President and Fellows of Harvard College All rights reserved Printed in the United States of America Library of Congress Cataloging-in-Publication Data Bird coloration / edited by Geoffrey E. Hill and Kevin J. McGraw. p. cm. Includes bibliographical references (p. ) and indexes. ISBN 0-674-01893-1 (volume 1) ISBN 0-674-02176-2 (volume 2) 1. Birds—Color. I. Hill, Geoffrey E. (Geoffrey Edward) II. McGraw, Kevin J. QL673.B555 2006 598.147′2—dc22 2005046126

Contents

Preface

vii

I. Function 1. Natural Selection and Coloration: Protection, Concealment, Advertisement, or Deception? gary r. bortolotti 2. Intraspecific Variation in Coloration james dale 3. Color Displays as Intrasexual Signals of Aggression and Dominance juan carlos senar

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4. Female Mate Choice for Ornamental Coloration geoffrey e. hill

137

5. Function and Evolution of Color in Young Birds rebecca m. kilner

201

6. Benefits to Females of Assessing Color Displays simon c. griffith and sarah r. pryke

233

7. Female Coloration: Review of Functional and Nonfunctional Hypotheses trond amundsen and henrik pärn

280

Contents

vi

II. Evolution 8. Colorful Phenotypes of Colorless Genotypes: Toward a New Evolutionary Synthesis of Color Displays alexander v. badyaev

349

9. Ecological Explanations for Interspecific Variability in Coloration ian p. f. owens

380

10. Adding Color to the Past: Ancestral-State Reconstruction of Coloration kevin e. omland and christopher m. hofmann

417

Acknowledgments

457

Contributors

461

Species Index

465

Subject Index

473

Color illustrations follow p. 454

Preface

Why birds have striking coloration is far from a trivial question. Darwin considered the ornaments of animals, including the brilliant colors of birds, to be among the traits that presented the greatest challenge to his idea of evolution by natural selection. It was, in large part, plumage coloration that inspired Darwin to devise sexual selection as a corollary hypothesis to natural selection that could account for traits that seemed to be ornamental rather than utilitarian. Despite the focus on bird coloration by evolutionary biologists in the late nineteenth century, however, it was not until late in the twentieth century that female choice for more colorful males was experimentally demonstrated in birds, that coloration was shown to predict resource-holding potential, and that comparative studies were conducted showing that color displays are correlated with estimates of the intensity of sexual selection. Since the early 1980s, our understanding of the function and evolution of avian colors has advanced rapidly. Despite the abundance of studies that have been published on the function and evolution of bird coloration in the past few decades, the most recent comprehensive review of animal coloration with a focus on function is Adaptive Coloration in Animals written by Hugh Cott in 1940. Two reviews of the function of plumage coloration were published in 1989 and 1995, but these reviews made no attempt to be comprehensive, and they have already fallen out of date (Butcher and Rohwer 1989; Savalli 1995). Andersson’s (1994) landmark book on sexual selection included an extensive review of the function and evolution of ornamental coloration, but because of the breadth of coverage of the book— all ornaments and armaments in all animals—the review of color displays is dispersed, incomplete, and not readily accessible.

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Preface

At the close of the twentieth century, there was a clear need for a comprehensive review of animal coloration, and in the summer of 2001, we began discussing plans for a grand, comprehensive synthesis of information on animal coloration, including production, measurement, perception, function, and evolution. We briefly considered covering all animals but quickly retreated to vertebrates. Birds and fish were the focus of most of the color literature related to signal content and sexual selection, and so vertebrates seemed like a natural focus for our book. We began to work on chapters in early 2002, and it was not long before we realized that we had taken on a daunting task. After a year of work on this project, it became clear that the topic was too large. The two of us simply could not complete a synthetic review of all vertebrate coloration. We decided to retreat to the topic that we knew best—bird coloration. Still, comprehensively reviewing the vast literature on the production, measurement, perception, function, and evolution of avian coloration proved too much for two authors. There are simply too many studies now published. We decided that, to create this grand overview of bird coloration, we would have to enlist the help of other color experts. In late 2003, we sent out invitations to colleagues asking if they would be willing to write chapters in their areas of expertise. We stuck with the original outline of our book—contributors were asked to write synthetic reviews of assigned topics. In this way, we structured the book to be comprehensive, with minimal overlap among chapters. The massive workload was now spread among 20 experienced scientists, so the time frame for the project could be greatly accelerated. We could not be more pleased with the results. We intend for this book to mark a new era in the scientific study of avian coloration. When Cott wrote his review in 1940, the focus was almost entirely on how natural selection shaped the colors of animals. There was no mention of sexual selection in Cott’s monograph, and discussions of the signal functions of coloration were limited to crypsis, aposematism, and species identity. At the start of the twenty-first century, research on animal coloration is now squarely focused on how color displays serve as signals to conspecifics. Sexual selection is the dominant theme throughout nearly every chapter of this volume. Studies have moved from purely descriptive to more experimental. Researchers no longer accept the demonstration of a function of a trait like a color display to mean that the trait evolved for that function. New comparative methods allow evolutionary hypotheses to be tested directly. One important new theme in the avian coloration literature, and a theme that we have encouraged in the chapters of this book, is that color displays pro-

Preface

duced by different mechanisms are functionally distinct. Carotenoid, melanin, and structural coloration differ in sensitivity to environmental challenges; they differ in their responses to hormones; they differ in the degree to which variation in expression is under genetic control; and they differ in their signaling effectiveness in different light environments. Mechanistic control of color displays was a theme of Volume 1 and provides a critical foundation for the studies presented in this volume. There is growing evidence that color displays that result from different mechanisms can serve very different signal functions and can be directed at different receivers (e.g., males versus females). For these reasons, in drawing generalities about the function and evolution of ornamental color displays, it is important not to lump together coloration that result from these fundamentally different mechanisms. We have divided this second volume of Bird Coloration into two sections. The chapters in the first section of the book collectively ask questions about the current utility of colors. In this section, authors look at the function of coloration in a variety of contexts—from mate choice, to social signaling, to individual recognition, and parent-offspring signaling. This is perhaps the area of research in which the greatest amount of recent work related to bird coloration has been conducted and it is the larger section of the book. In the second section, the chapters take an explicitly evolutionary approach to understanding why birds have color displays. They review the various selective pressures that have led to the evolution of colors and patterns in the plumage and bare-parts of birds. These evolutionary studies necessarily build from studies of the mechanisms of production, controls of expression, and function, and it is fitting that the entire two-volume effort ends with a summary of these comparative studies. Through 150 years of research on the function and evolution of avian coloration, biologists have constructed a broad foundation for understanding how these traits function and by what means and under what circumstances they have evolved. The topic is so immense and so complex, however, that despite the achievements in the field, we have really only scratched the surface. We hope that this second volume and this entire two-volume project serve as both a starting point and a source of inspiration for future studies of avian coloration. We hope that the next century and a half of work on bird coloration is as fruitful and exciting as the previous period has been.

References Andersson, M. 1994. Sexual Selection. Princeton, NJ: Princeton University Press.

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Preface Butcher, G. S., and S. Rohwer. 1989. The evolution of conspicuous and distinctive colouration for communication in birds. Curr Ornithol 6: 51–108. Cott, H. B. 1940. Adaptive Coloration in Animals. London: Methuen. Savalli, U. M. 1995. The evolution of bird coloration and plumage elaboration: A review of hypotheses. Curr Ornithol 12: 141–190.

I Function

1 Natural Selection and Coloration: Protection, Concealment, Advertisement, or Deception? gary r. bortolot ti

Old Questions and New Opportunities In an era when so much exciting research is revealing the complexities and pervasiveness of sexual selection in maintaining the bright colors of birds (Chapters 3 and 4), a discussion of how natural selection has shaped avian coloration seems almost anachronistic. Isn’t it obvious that a ptarmigan blends her brown summer plumage with her surroundings at the nest, and her white feathers against winter’s snow, to hide from predators (Plate 19, Volume 1)? Perhaps. Most modern biologists would consider the bright conspicuous ornamentation of birds to be the product of sexual selection, whereas all other colors and patterns are, by default, the work of natural selection. Not only is this dichotomy incorrect, but it typically reduces the adaptive nature of coloration to a simplistic catch-all of “survival.” The latter is naïve at best, and ignores numerous exciting opportunities that exist for understanding the evolution and ecology, not to mention physiology and psychology, of birds. I hope to show here that the plausible naturally selected functions of color are as rich and complex as those we now know to be involved in sexual selection. The study of natural selection and animal coloration has been an attractive topic for many years. It has been a blend of good old-fashioned observational

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gary r. bortolot ti natural history, evolutionary theory, and psychology that have been thoroughly and successfully integrated—so well integrated perhaps that the very distinction between proximate and ultimate explanations is somewhat blurred. The use of such terms as “camouflage” is a good example of this blurring of mechanism and function. However, the degree to which hypotheses concerning the adaptive nature of coloration have been rigorously formulated and tested is highly variable. One only has to look at Savalli’s (1995) comprehensive review of the evolution of avian coloration to see the nature of science in this field. Of 16 hypotheses related to natural selection (for simplicity here, excluding all aspects of signaling), the supporting evidence was listed as anecdotal for five (31%) and experimental for only six (37%). Compare this to zero anecdotal and eight (73%) experimental for 11 hypotheses involving intraspecific signaling. In part, this disparity may arise because many studies of the potential role of natural selection in maintaining avian colors and patterns are older and so perhaps did not have the rigor, or the modern analytical tools, of current investigations of the sexually selected nature of color. However, the more mechanistic, psychological, and ethological approach to understanding coloration and the perception of color patterns has always had a firm foundation in experimental science. Mottram (1915), for example, manipulated candlelight (literally, the number of and distance to candles) to determine the conspicuousness of patterns in nature. At least historically, the study of how natural selection may have operated on coloration has relied heavily on anecdotal and comparative evidence. Intimate familiarity with the behavior and ecology of their subjects has been the great strength of many ornithologists. However, the intuitive logic and “obvious” nature of much of coloration’s function have surely been some of the biggest impediments to the advancement in understanding of what selective pressures have acted on birds. Is it really necessary to question whether an Arctic bird is white to be cryptic against snow? The short answer is yes! (See, e.g., Montgomerie et al. 2001; Honkavaara et al. 2002; Tickell 2003.) There are rich opportunities for a fresh look at some of the classical concepts that have been developed (but surprising rarely tested) over the decades to understand the adaptive nature of bird coloration. Two factors in particular provide this opportunity. First, today’s biologist has a far better appreciation of the sensory world of birds; for example, the relatively recent finding that avian vision extends into the ultraviolet (UV) range has revealed exciting aspects of foraging behavior and signaling (Chapter 1, Volume 1). Second, better phylogenetic trees based on molecular data and the appropriate statistical tools for revealing evolutionary independent events allow for more meaning-

Natural Selection and Coloration

ful comparative studies (Harvey and Pagel 1991; Chapters 9 and 10). With these tools, we can move away from “just-so” adaptive stories of single species or limited groups of species that have plagued progress toward a more meaningful understanding of color and natural selection. As with any study of the ecology and behavior of animals, a major challenge is to be aware of the sensory world of one’s subjects. In studies of natural selection and color, not only visual perception but other sensory experiences (e.g., gustatory) are potentially important. Unlike a study of sexually selected traits, where the signaler and the receiver are at least the same species, studies of natural selection are faced with the daunting task of appreciating the sensory world of a community. A further challenge is to consider an even broader perspective on the receiver animal, what Guilford and Dawkins (1991) refer to as the “psychological landscape”: everything about the brain of the receiver that might affect its response to a signal. Although a considerable amount of study has gone into the concepts of signal design in communication systems, less effort has been directed toward understanding other functions of color. Guilford and Dawkins (1991) discuss design in promoting efficacy of signals, including detectability, discriminabilty, and memorability. What has not been done to any extent is a comparable approach to understanding the efficacy of color patterns in crypsis. In other words, how does natural selection operate on the design of animals so that information is not conveyed? My approach in this chapter is to examine how natural selection has operated from two fundamentally different perspectives. The first, paradoxically, is that coloration could be the result of selection acting on nonoptical attributes of coloration. In other words, color as it is perceived by other animals, even conspecifics, is not relevant. Instead, coloration of skin and feathers may have important functions dealing with the bearer’s physiology, environmental protection, or as an aid to the animal’s own vision. Alternatively, natural selection may act on the relationship between the bearer of the colors and other animals. In most cases discussed here, these interactions will be between predator and prey species. I do not deal with questions of how color may facilitate individual, kin, or species recognition (Chapter 2), nor how it may function in parent-offspring relationships (Chapter 5).

Historical Perspective Like much of modern biology, the roots of our understanding of the adaptive coloration of animals can be found in the works of Charles Darwin and Alfred Russel Wallace because prior to the writing of these biologists, little function

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was ascribed to color. Cronin (1991) has detailed the special role in the history of evolutionary biology that the subject of coloration, particularly avian, has played. Perhaps it was the intuitive appeal of such ideas as crypsis or warning signals, but arguments for the adaptive nature of coloration seem to have been important for the widespread acceptance of natural selection as a viable theory (Cronin 1991). In addition, she recounts a tale of prolonged conflict between Darwin and Wallace over the function of coloration. The two great thinkers held opposite perspectives, a dichotomy that in fact typifies some views on the subject today. Darwin (1871) focused on how males evolved bright colors to be successful in reproduction (i.e., sexual selection). Wallace (1889), however, believed color to be a natural attribute of the chemicals of life (e.g., blood is bright red), and so females evolved dull colors to be cryptic on the nest (i.e., natural selection). So tenacious was his commitment to natural selection that Wallace even described himself as being more “Darwinian than Darwin” (see the complete argument in Cronin 1991). Some of the later figures who were influential in the study of both proximate and ultimate factors for the evolution of coloration were A. H. Thayer (1896), G. H. Thayer (1909), J. S. Huxley (1938) and H. B. Cott (1940). In their works, the adaptive nature of coloration was almost entirely one involving the relationship between predators and prey. First, the Thayers (1896, 1909), and then especially Cott (1940), stressed putting the animal into the perspective of its environment. Cott’s (1940) book is exciting and informative to this day. Thayer (1909), for example, so believed that all coloration could be viewed as concealment that he forced examples, including beautiful, but contrived, color plates (Plate 1; for an interesting critique, see Gould 1991). Although perhaps Thayer is judged unfairly by modern standards, such ideas as flamingos being pink so they can be cryptic in sunsets, or the display train of a peacock resembling a fruit tree, are not very defensible.

Is Color Always Necessary or Adaptive? Some color variation in birds may be selectively neutral, as has been proposed for many plumage polymorphisms (Buckley 1987a; Price and Boag 1987). A few examples are known for which color forms are merely the nonadaptive consequence of pleiotropic effects of genes (Buckley 1987b; Cooke and Buckley 1987). White has been termed the “default” color in birds (Tickell 2003). The rationale is that white is a structural color of feathers, and if there is no selective

Natural Selection and Coloration

advantage to being colored, natural selection should cease to maintain pigmentation. Tickell (2003) noted that birds appear to have a subtle economy in the use of pigment. Perhaps because of thermal or synthetic costs of pigmentation, the portions of feathers underlying colored feathers that are overlapping (i.e., the parts that are not exposed) are often white. After an exhaustive review of the possible functions of white plumage, Tickell (2003) concluded that there were few examples of adaptive scenarios for white coloration that convincingly falsified the hypothesis that feathers were white by default. However, Beauchamp and Heeb (2001) examined a wide range of species and found that the evolutionary transition from solitary to social foraging was associated with an increase in the proportion of white plumage as a recruitment signal to attract distant foragers. Studies of avian coloration often focus on hue, saturation, or brightness, but spots, stripes, bars, and patches can be just as important. In one of the most insightful studies of plumage patterns, Price and Pavelka (1996) showed the importantance of considering the roles of both selection and development in investigating how color patterns can be lost or gained during the course of evolution. Using reaction-diffusion models, they showed that many patterns are predictable given the tapered shape of avian embryos, and how such ontogenetic considerations explain why more color patterns appear on the heads of birds. Few studies of bird colors and patterns have so carefully considered the role of developmental constraints (Chapter 8).

Is What You See What You Get? Selection for Nonoptical Properties of Coloration Some of the functions proposed for the pigments in feathers do not involve their optical properties. Because many colors may be multipurpose, especially in such social animals as birds, single-function analyses are fraught with confounding factors. This problem is especially relevant for research on nonoptical properties of pigments, as most comparative studies of nonoptical pigment function predate analyses of phylogenetically independent events and were conducted on a limited number of species. The perspective has also been somewhat narrow, as there has been a disproportionate amount of attention given to contrasting black and white. Even then, we are often left unsatisfied that there are no unambiguous naturally selected functions even for the extremes (e.g., Tickell 2003). In his investigation of the abrasion-resistance hypothesis

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oceanic

desert

Percentage of species

40

30

20

10

0 0–9

10–19 20–29 30–39 40–49 50–59 60–69 70–79 80–89 90–100

Percentage of white on body surface Figure 1.1. Percentage white on the body surface of desert birds and those oceanic birds that neither dive nor dig burrows. Adapted from Burtt (1981).

for the melanization of feathers (see below), Burtt (1981) showed that desert birds are typically dark, whereas pelagic birds have a considerable amount of white on their bodies (Figure 1.1). However, interpreting that finding is complicated, as there are other important considerations, such as thermoregulation and social foraging (see below), that are especially relevant to those species. Experimental studies are surprisingly uncommon, and many of the tenets of how color serves to protect birds, for example, remain untested (for exceptions, see Burtt 1979, 1986). Protective Effects of Color One of the few functions of color that does not involve signaling and is well supported is the value of melanin in protection from abrasion. The idea that

Natural Selection and Coloration

melanin increases the strength and resistance to wear of feather keratin has long been suspected from observational evidence (reviewed in Burtt 1986). Many predominantly white birds (e.g., geese, gulls, pelicans, cranes) have black wing tips (Plate 2). Inspection of individual birds with atypically white feathers and extreme feather wear has also supported the abrasion-resistance hypothesis (Barrowclough and Sibley 1980; Parker 1985; Lee and Grant 1986). Burtt’s (1986) extensive experimentation demonstrated that melanic feathers are more resistant to abrasion that nonmelanic feathers, whereas carotenoid pigments offer no protection. Experimental studies of mechanical properties of keratin with respect to color have been quite recent, and so far have focused on just a few taxa. Bonser and Witter (1993), examining the bills of European Starlings (Sturnus vulgaris; Plate 23, Volume 1), and Bonser (1995), studying feathers of Willow Ptarmigan (Lagopus lagopus race scoticus), found melanin to increase hardness. Recently, however, Butler and Johnson (2004) pointed out that although strength and hardness have been treated as synonyms in the behavioral literature, this need not be the case. Butler and Johnson (2004) tested the tensile strength of black and white barbs on a single remige of an Osprey (Pandion haliaetus). Their comprehensive sampling along the feather revealed that, when morphology and position of barbs were considered, there was no difference between melanized and unmelanized keratin. Careful sampling design is needed for future studies to separate the effects of position from melanin on feather wear. Melanin-based coloration is nonrandom with respect to position on the body. Most birds have a darker dorsal than ventral surface. Although this is often attributed to “countershading” to enhance crypsis (see below), it is plausible that the surface most exposed to the sun is pigmented to protect against the damaging effects of UV radiation. The only concerted test of this hypothesis has been Burtt’s (1979) analysis of the plumage, bill, and leg color of wood-warblers (Parulidae). Warblers whose upper mandible is dark spend more time in sunny locations than those whose bill is light; however, such behavior is not related to plumage or leg color. I know of no study that has analyzed in depth the variation or function of skin color over the body (other than ornaments, e.g., Bortolotti et al. 1996). Especially when one considers altricial species that are exposed to the sun, there are species with pale skin (e.g., pelicans, Pelecanidae) and others with dark skin (e.g., cormorants, Phalacrocoracidae). Having watched cormorant chicks panting in the intense heat of a Patagonian desert, I had to wonder whether there was an advantage to their jet-black skin, for there seemed to be an obvious disadvantage in overheating.

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gary r. bortolot ti However, such speculation leads to adaptive, just-so stories. Designing experimental tests of such function will be a challenge. Carotenoid pigments in feathers offer some protection from UV radiation, but not as much as melanins (Burtt 1979). However, a more plausible connection between carotenoids and UV protection is in areas of exposed skin. Many species of birds (e.g., birds of prey, pheasants and partridges, pelicans, cormorants, storks, ibis, hornbills, cranes) have large areas on the face or head that are conspicuously devoid of feathers (Plate 30, Volume 1). In some cases, the skin is brightly colored with carotenoid pigments (hemoglobin from blood also gives red color to bare parts; Chapters 5 and 8, Volume 1). Although such color may often be a social signal (e.g., Bortolotti et al. 1996; Negro et al. 1998), it is plausible that an added, or perhaps original, benefit of the pigment was UV protection. It is well known that exposure to UV light causes photooxidative reactions that are damaging to cells and cause pathologies in humans (Stahl and Sies 2002). Carotenoids are used as pigments in human skin and offer UV protection (Alaluf et al. 2002; Stahl and Sies 2002), but comparable studies in birds have not been done. Carotenoids may also play an interesting role in the protection of feathers from bacterial degradation. Recently it has been discovered that featherdegrading bacteria are commonly found on birds, but little is known of their ecological or evolutionary significance (Burtt and Ichida 1999; Shawkey and Hill 2004). Grande et al. (2004) investigated how the colors of feathers may influence susceptibility to degradation. Using in vitro techniques, they showed that Bacillus licheniformis effectively broke down feathers, but the degree of damage was contingent upon color. The first samples to show damage were melanized, followed by unpigmented (white) and carotenoid-pigmented feathers, and finally green feathers of a parakeet (whose color is derived from a yellow psittacofulvin pigment [Chapter 8, Volume 1] and blue structural color [Chapter 7, Volume 1]). At the end of the experiment, melanic and white feathers were more degraded than those of the parakeet or those with carotenoid-based color (Figure 1.2). These results are contrary to those of Goldstein et al. (2004), who tested the bacterial degradation rates of black versus white chicken feathers and found the former to be better protected. The difference between the findings of Grande et al. and Goldstein et al. could be related to the strain of bacterium used in the lab (J. J. Negro, pers. comm.). What is not known is how bacteria may influence living birds under natural conditions. However, Burtt and Ichida (2004) have started us on this path by investigating bacterial degradation and avian coloration in a well-known eco-

Natural Selection and Coloration

11

a

b C

Greater Flamingo

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Roseate Spoonbill

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C

Scarlet Ibis

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Eurasian Golden Oriole

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Little Egret

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Blue-crowned Conure

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Time to degradation (d)

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Feather degradation category

Figure 1.2. Mean (solid black squares) ± standard error (SE; boxes) and ± 1.96 SE (whiskers) for (a) number of days postinoculation that feathers with carotenoid (C), melanin (M), psittacofulvin + structural green color (P), or unpigmented (U) began to show clear signs of bacterial degradation, and (b) final state of feathers at the end of the experiment. Degradation categories: 1 = intact, 2 = partially damaged, 3 = clearly deteriorated, 4 = fibers, and 5 = dust. Adapted from Grande et al. (2004).

logical context—across a gradient of humidity. Gloger’s rule states that birds inhabiting relatively humid areas will be more darkly colored that those in arid areas. Burtt and Ichida (2004) found that dark Song Sparrows (Melospiza melodia morphna) of the Pacific Northwest have a significantly more active strain, and perhaps a somewhat higher incidence, of Bacillus licheniformis on their plumage than the pale Song Sparrows (M. m. fallax) of the arid southwest. Thermoregulation Dark colors absorb more radiant energy than do light colors, but this property alone does not allow one to make predictions about how bird coloration should vary with climate. The properties of feathers are such that dark colors prevent radiation from passing through to the skin, and instead keep it near the surface where it may be lost. In contrast, light-colored plumage allows more radiant energy to pass through the feathers where it may warm the animal (Wolf and Walsberg 2000). Most attempts to relate climate to color have found little satisfying evidence for a relationship (Bretagnolle 1993; Tickell

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2003). Such a result may not be surprising, given that wind and degree of ptiloerection have been shown to be more significant factors for thermoregulation than color (Walsberg 1982; Tickell 2003). Burtt (1981) suggested that the trend for darker birds to be found in humid environments (Gloger’s Rule) may be due to dark colors enhancing the drying out of feathers. Burtt (1986) found some support for a thermoregulatory function of color by comparing warblers (Parulidae) with dark versus light legs. One largely ignored association between color and thermoregulation has been the ability of colorful, vascularized tissue to dissipate heat. Recently, Negro et al. (in press) described rapid changes in dermal coloration in large birds, for example, the wattles of Wild Turkeys (Meleagris gallopavo; Plate 32, Volume 1), the face of Crested Caracaras (Polyborus plancus), and the skin on the head of the Hooded Vulture (Necrosyrtes monachus). Color changes are possible from variation in peripheral blood flow (i.e., visibility of hemoglobin). Although some of these colors may now serve a signaling function, it is likely that the specialized blood transport to bare facial skin evolved for thermoregulation (Negro et al., in press). Selection to Enhance Vision The heads of birds are particularly enriched with color patterns (Burtt 1986; Price and Pavelka 1996), and some patterns may function to enhance vision. Many species have dark feathers in patches, rings, or lines near their eyes. One intuitively appealing explanation for the presence of these markings is that they may reduce glare. American athletes apply “eye black” under their eyes for this purpose (Ficken and Wilmot 1968). This may be one of the least tested hypotheses for coloration. Falcons are often touted as examples of high-speed birds whose moustache, or malar stripe, acts to reduce glare (e.g., Wheeler 2003). The degree of melanization of the feathers in the eye-stripe in Falco is variable among species, but the antiglare hypothesis fails to explain why. Presence and intensity of stripes are not associated with hunting style (e.g., compare Accipiter-like attackers such as the Aplomado Falcon [F. femoralis] and the Mauritius Kestrel [F. punctatus], and harrier-like searchers such as the Red-footed Falcon [F. vespertinus] and Lesser Kestrel [F. naumanni]; Cade 1982). Why should such desert falcons as the Saker (F. cherrug) and Prairie Falcon (F. mexicanus) that inhabit brightly lit environments have faint stripes, compared to the nearly all-black heads of forest dwellers like the Orangebreasted Falcon (F. deiroleucus) and Bat Falcon (F. rufigularis)?

Natural Selection and Coloration

Figure 1.3. On the heads of birds, various markings may function as sight-lines, to reduce glare, or for concealment. Clockwise from upper left: Blue Tit (Parus caeruleus), Red-legged Partridge (Alectoris rufa), Whimbrel (Numenius phaeopus), Great Kiskadee (Pitangus sulphuratus), Loggerhead Shrike (Lanius ludovicianus), and Golden-cheeked Warbler (Dendroica chrysoparia). See also Box 1.1.

Burtt (1986) proposed that the upper mandible of warblers may be dark to minimize reflection. He also experimented by painting the dark upper mandible of Willow Flycatchers (Empidonax traillii) with white nail polish; manipulated birds increased foraging time in the shade (Burtt 1984). For many birds, a straight, uninterrupted dark line passes through or beside the eye and leads to the bill (Figure 1.3; Plates 28 and 29). Ficken and Wilmot (1968) and Ficken et al. (1971) proposed that such marks serve as sighting lines, which aid in tracking and capturing fast-moving prey. Some evidence for passerines (although not using modern statistical techniques) supported that claim (Ficken and Wilmot 1968; Ficken et al. 1971). How a bird might actually focus using sight-lines has been questioned (Burtt 1986). Zahavi and Zahavi (1997) suggested that birds with binocular vision were more likely to have eye-lines (but for the handicap of revealing the direction of gaze), whereas species with monocular vision had rings. It is difficult to test the sight-line hypothesis experimentally, and equally plausible and more testable hypotheses, such as concealment (see Box 1.1) have also been proposed (Cott 1940; Gavish and Gavish 1981). Eye-lines may function to hide the eye because, for most species of bird, the iris is dark. Why birds have dark eyes, and even the pigments responsible for

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Box 1.1. Concealment of the Eye In his seminal work on the function of adaptive coloration in animals, Cott (1940:82) refers to eyes as “that most difficult of all organs to conceal” because of their great inherent conspicuousness. One has only to think how the eyes in portrait paintings seem to follow you around the room to understand his point. Eyes may evoke both attraction and aversion, and several authors have addressed the psychological impacts of eyelike shapes (Cott 1940; Hinde 1954; Curio 1975; Gavish and Gavish 1981). Scaife (1976a,b), using a stuffed Eurasian Kestrel (Falco tinnunculus), showed that chicks of domestic fowl had a strong aversion to the model only when conspicuous eyes were visible. Detailed investigations have also shown how important eyes are in eliciting avian mobbing responses (Hinde 1954; Curio 1975) or in influencing aspects of mobbing attacks (Altmann 1956; Deppe et al. 2003). If eyes are so stimulating, the question then becomes one of how a bird conceals its eyes to reduce its visibility (i.e., vulnerability).

a b c Figure B1.1. Examples of the location of eyes in relation to color patterns in birds: (a) interior eye (Yellow-rumped Warbler [Dendroica coronata]), (b and c) borderline eyes (Sandwich Tern [Sterna sandvicensis] and Great Tit [Parus major]). Adapted from Gavish and Gavish (1981).

a

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d

e

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Percentage detectability

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e

f

g

a b c d

0 –X

0

X

Distance to border Figure B1.2. Results of an experiment to determine the detectability by humans of “eyes” relative to a border between light and dark. Detectability of eyes is plotted against the distance to the border. Note how the poorest detection was for “eyes” protruding just below the border. Adapted from Gavish and Gavish (1981).

Even a cursory glance at a field guide reveals that birds have an array of stripes and patches that run through or near the eye. As well stated by Burtt (1986:96), “the face may be the most intricately patterned, most brightly colored, and least understood area of birds.” One function of black near the eye may be to reduce glare (see text), although there are no data to support this idea. More plausibly for many species is a concealing function for markings proximal to the eye. Gavish and Gavish (1981) found that eyes were more often located at the border of contrasting colors than well inside the dark area (Figure B1.1). Eyes often protrude out of the borderline. This observation led Gavish and Gavish (1981) to test the hypothesis, using humans as subjects, that borderline eyes are more concealed. The detectability of simulated borderline eyes were substantially lower than that of interior eyes, and the most concealed pattern was a protruding eye (six times less detectable than an interior eye; Figure B1.2). Although it would seem that concealment of the eye may be useful in avoiding the attention of predators, Gavish and Gavish (1981) interpreted these results primarily as allowing birds to stay at short distances from one another without eliciting an avoidance response.

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gary r. bortolot ti eye color, is relatively poorly understood (e.g., see Oliphant et al. 1992; Bortolotti et al. 2003; Chapter 8, Volume 1). It has been hypothesized that iris color influences visual clarity (M. Worthy, as cited by Savalli 1995). Light irides may allow more light to reach the retina, especially at the edges, which may reduce the sharpness of images relative to dark irides. Whether associations exist, as might be predicted, between the behavior or habitat of birds and their iris color is not known (Burtt 1981; Savalli 1995).

To Be Seen or Not to Be Seen? That Is the Question Unlike the preceding discussion, here I explain how natural selection may act on color as it is perceived by other animals. I focus mainly on the dynamics of predators and their prey. Cott (1940), in his remarkable book on adaptive coloration in animals, realized that virtually any attribute that could protect a bird from predation could similarly be used by a predator to its advantage— a duality that is not often recognized. He believed there were three main classes of function according to the visual results produced. Color was a question of concealment, advertisement, and disguise. Major questions then become: Who is the intended receiver and what is their visual perception and psychology (Guilford and Dawkins 1991)? The investigation of colors purported to function in concealment is more complex than are investigations of colors purported to function in sexual selection, because in the latter, one knows the target receiver. In an antipredator scenario, there could be a community of predators with a variety of taxa. Studies have not been designed to measure potential trade-offs and conflicts between conspicuousness as perceived by mammalian versus avian predators, for example. Another consideration that is rarely quantified in studies of coloration is the behavior of the bearer of the color. Coordination between the bird and its environment is crucial. Although seemingly obvious, many studies fail to report or consider the role of choice of habitat, background, or specific behaviors that reduce or enhance visibility. The American Bittern (Botaurus lentiginosus), for example, evades detection in a marsh using cryptic plumage coupled with behavior. The throat and breast are streaked in a fashion to blend with emergent vegetation, but the crypsis only works when an alarmed bird holds its bill straight up in reed-like fashion. A bittern will even sway its body back and forth to the appropriate rhythm of the reeds in the wind (Bent 1963). It has been suggested that Red-winged Blackbirds (Agelaius phoeniceus; Plate 11; Andersson 1994), Chaffinches (Fringilla coelebs; Marler 1956), and ground jays

Natural Selection and Coloration

(Podoces spp.; Londei 2004) facultatively conceal colored patches to make themselves less conspicuous in the presence of a bird of prey or when otherwise vulnerable. This kind of behavioral modification has received little attention, but should be considered to properly evaluate the predation risk, and hence costs, of bright colors. Comparative studies also show the importance of adding a behavioral context to color (wing patches flush prey [ Jablónski 1996] and plumage polymorphisms and activity pattern [Galeotti et al. 2003], as discussed below). Concealment Given the long history of interest in natural selection and color, one might expect that concealment would have been tested thoroughly, but such is not the case for either an ultimate or proximate perspective (see Dale and Slagsvold 1996 as an exception). When comparative studies have looked for broad generalizations, they have often failed to find or have had difficulty identifying mechanisms (e.g., Bretagnolle 1993; Tickell 2003). Rather than examining interspecific variation, which is complicated by different life histories, some authors have looked at plumage polymorphisms. Preston (1980) suggested that the perch-site preference he observed for different morphs of Red-tailed Hawks (Buteo jamaicensis) facilitated concealment from prey. However, for diurnal birds of prey and owls collectively, Fowlie and Kruger (2003) did not find ecological variables to be associated with the frequency of polymorphisms. The first comprehensive analysis of frequency and potential causes of color polymorphism in all Aves has only recently been completed (Galeotti et al. 2003). Polymorphism is apparently uncommon, as it is found in only 3.5% of all species; however, it is found in 61% of all orders. Galeotti et al. (2003) found that polymorphisms were most common in species that inhabited semiopen habitats and particularly if they were active in both the daytime and the nighttime. They interpreted these findings as the consequence of varying light levels on crypsis. Much like the idea that white is the default color, crypsis is often used as a default explanation. Or, ironically, some of the better evidence for the value of cryptic plumage comes from studies designed to examine sexual selection. The simplest observations come from studies of single species that report higher mortality of birds with brighter plumage (e.g., Pied Flycatchers [Ficedula hypoleuca; Plate 27, Volume 1], Slagsvold et al. 1995; Rock Ptarmigan [Lagopus mutus; Plate 19, Volume 1], Montgomerie et al. 2001). Studies that

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gary r. bortolot ti have examined the potential costs of sexual dimorphism using comparative analyses that included many species have found variable results (Promislow et al. 1992, 1994; Owens and Bennett 1994). The problem with such tests is that males and females differ in so many ways besides color that undoubtedly affect survival (e.g., behavior, cost of reproduction, physiology). Because the conspicuousness of a bird depends on the spectra of ambient light in the context of the environmental background, a community-level comparative study is likely to be most productive. In an uncommonly comprehensive analysis of a rainforest bird community, Gomez and Théry (2004) considered spectrometry, modern comparative analyses, height within the forest, color components, and sex, while contrasting predictions of natural and sexual selection. For crypsis to be maximized, they predicted that plumage should be brighter (lighter) for canopy than for ground birds and that birds should be green in the canopy and brown in the understory. Both predictions were supported by the data (Figure 1.4; see Chapter 4, Volume 1; Plate 28). Crypsis as a means of avoiding predation is only half the story. Predators also require concealment. Thayer (1909) presented contrived scenarios, complete with photographs, to convince the reader that all manner of colors and patterns in raptors were advantageous in hiding them from their prey. Although coloration in this group of birds has not been dealt with in recent years, a considerable amount of literature exists on seabirds (e.g., Simmons 1972; Bretagnolle 1993; Tickell 2003). Regardless of phylogeny, most seabirds show large areas of even coloration of black, brown, or white on their bodies, consistent with the simplicity of their light environment (relative to, e.g., forests). It has long been suspected that white underparts of seabirds and other waterbirds render them inconspicuous to aquatic prey against the bright sky (e.g., Thayer 1909; Simmons 1972), with experimental support from Phillips (1962: cut-outs of birds shown to fish), Mock (1980: models of plumage morphs of herons), and Götmark (1987: gulls dyed black). However, a recent and thorough review suggests there are too many inconsistencies between plumage and the diet or mode of foraging to support this hypothesis (Tickell 2003). Even if an advantage of cryptic plumage is demonstrated, many questions remain regarding mechanisms: how is concealment actually achieved? Here I discuss how visibility may be reduced in a number of ways, regardless of function. Unfortunately, these concepts have been more often tested on other taxa than birds (e.g., Cott 1940; Hailman 1977). In most cases, I present a simplified version of the optical principle, for there are often many subtle variants. There is no better or more complete reference than Cott (1940).

Natural Selection and Coloration female

19 male

Hue (degrees)

100

50

Brightness (µmol•m–2•s–1)

0

1

0

canopy

ground

Foraging height in tropical rainforest

Figure 1.4. Variation in mean (± standard error) hue and brightness among 40 bird species that forage at different heights in mature primary rainforests. Hue scale is an angle expressed in degrees based on Munsell colors, increasing from red (12°) to yellow (51°) to green (170°). Brightness scale is expressed relative to an incident light of 10 µmol m–2 s–1. Adapted from Gomez and Théry (2004).

Color Resemblance In “general color resemblance,” birds are colored to match their surroundings, be it pale brown to match the sand of a desert (Plate 2), or green to match the foliage of a tree. In “variable color resemblance” (Cott 1940), color changes according to life-history stage (concealing downy young), season (e.g., turning white in winter), or from moment to moment (generally not applicable to birds).

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Countershading (Obliterative Shading) An animal being lit from above has its upper surface more illuminated than its lower parts. This kind of shading gives a three-dimensional object a sense of depth and makes it easier for an observer to detect. Perhaps it is not surprising that an artist, A. H. Thayer (1896), was the first to propose that most animal taxa are countershaded (i.e., more heavily pigmented on the upper than on lower surfaces) to counteract the natural effects of shade and light and become less conspicuous. The pattern is so widespread that it is the exceptions that catch our attention (e.g., Bobolinks [Dolichonyx oryzivorus]). Newton (2003) proposed that melanistic birds were more common on islands because reduced predation risk allowed some species to abandon countershading. Disruptive Coloration Although Cott (1940) believed that countershading was protective, he pointed out that, as many animals are very active, they are constantly in contact with backgrounds that vary in color, pattern, and lighting. A uniformly colored animal would be conspicuous against variable surroundings; therefore the most important form of concealment involved the disruption of form (Cott 1940). Animal studies inspired a considerable amount of research on this and related forms of concealment for military application during World Wars I and II (see Cott 1940; Gould 1991; Tickell 2003). Cott’s book, which was published during World War II, is punctuated with reference to war. Cott (1940:48) writes, “When the surface of a fish, or of a factory, is covered with irregular patches of contrasted colors and tones, these patches tend to catch the eye of the observer and to draw his attention away from the shape which bears them.” The breast bands of small shorebirds are plausible examples (Hailman 1977; Plate 2). In general, white marks on dark animals that live in dark environments and black marks on light animals in bright environments are said to be the most effective disruption (Cott 1940). Coincident Disruptive Coloration In this case, coloration serves to join separate parts of the body, usually the limbs, body, and head of many nonavian taxa (Cott 1940). Where this applies most to birds may be in eye-lines that serve to conceal the eye, and such eye lines are very common in birds (Cott 1940; Gavish and Gavish 1981; Box 1.1).

Natural Selection and Coloration

Concealment of Shadow A shadow can be more revealing than the animal that cast it. Disruptive patterns may mimic shadows (Cott 1940), but most examples of concealment of shadow in birds are related to behaviors, such as crouching and lateral body compression (Cott 1940; Hailman 1977). Advertisement In sharp contrast to the previous discussion, natural selection may operate to increase conspicuousness of both predators and their prey. Some of the ideas on protective coloration, such as flash marks, date back to Wallace (1889; see Cronin 1991:124). Unprofitable Prey Conspicuous colors may be protective to prey because they signal their “unprofitability” (e.g., difficult to capture, aggressive, distasteful, poisonous) to predators (Baker and Parker 1979). Overall the evidence regarding mortality or predation risk of brightly colored birds is mixed. As discussed earlier, much of what is known about predation and crypsis suggests that bright colors are not advantageous (e.g., Slagsvold et al. 1995; Montgomerie et al. 2001). Comparative studies of ducks (Promislow et al. 1994) and passerines (Promislow et al. 1992) suggest that the brightly colored sex has a higher mortality. No such difference was found in a study using a broader avian phylogeny (Owens and Bennett 1994). Rytkönen et al. (1998) studied prey selection by the Sparrowhawk (Accipiter nisus) and found that bright species had a higher predation risk (Plate 4); however, color did not seem to matter in Baker and Bibby’s (1987) study of Merlins (Falco columbarius). By far the most extensive testing of the unprofitable prey hypothesis has been by Götmark, primarily through the presentation of stuffed birds that varied in conspicuousness, with automatic photographs taken of attacks by avian predators (primarily Accipiter spp.). Even then, results were variable (Götmark 1993, 1997; Götmark and Unger 1994). Götmark (1993) presented male and female models 1.5 m apart; dull female Pied Flycatchers, but bright male Chaffinches were more frequently attacked by Sparrowhawks (Figure 1.5). These results are at odds with Slagsvold et al. (1995), who found that brightly colored male Pied Flycatchers disappeared (believed to be killed by

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Number of attacks

16 12 8 4 0

female

male

Pied Flycatchers

female

male

Chaffinches

Figure 1.5. Number of attacks by accipiters directed to stuffed female versus male Pied Flycatchers (n = 18 trials; p = 0.008) and Chaffinches (n = 21 trials; p = 0.026). Models of males and females of each species were presented at the same time, giving the hawks an immediate choice of prey. Adapted from Götmark (1993).

Sparrowhawks) more frequently than did dull, female-colored males (see Slagsvold et al. 1995 for several explanations for these differences). Even when results support the unprofitable prey hypothesis, it is not known by what mechanism protective coloration may operate. Götmark (1994a) examined the question of the level of predation risk when a conspicuous, novel plumage trait appeared in evolution. It is possible that a new trait has a higher risk because raptors seem to be effective in selecting unusual forms (apparently at least in birds that flock; see Götmark 1994a). Alternatively, some predation risk may be frequency dependent (i.e., apostatic), and so novel traits or rare morphs are protected. Götmark (1994a) tested the effect of novel coloration on predation by painting red wing patches on stuffed European Blackbirds (Turdus merula) and recording attacks by hawks, as he had in earlier work. The conspicuous, novel color appeared to offer protection. These findings led Götmark (1994a) to reflect on his previous results that had shown differential predation on the sexes but that had been inconsistent with respect to plumage brightness (Götmark 1993; Figure 1.5). He concluded that the frequency of morphs, which varied depending on specifics of the situation, may explain overall predation risk. Could bright plumages serve as a warning that the species is noxious or dangerous? Although well understood in other taxa than birds, generally such aposematic signals involve the use of a few colors of bold pattern (Cott 1940).

Natural Selection and Coloration

The striking white wing patch of kleptoparasitic skuas (Catharacta spp.) may signal their victims to give up food (Spear and Ainley 1993). The idea that warning colors could signal a bird being distasteful or poisonous has been around for a long time, but without widespread support or attention. Cott (1947) and Cott and Benson (1970) presented considerable evidence for aposematism in plumage relating to the palatability of birds as determined by hornets, cats, and a panel of human testers. Cott’s data on birds from southern Africa were reanalyzed by Götmark (1994b). He found that, for nonpasserines and female passerines, conspicuousness and edibility were negatively correlated. However, for male passerines, there was no such relationship, perhaps because their plumage was the result of sexual selection (Götmark 1994b). More credence has been given to Cott’s findings since the discovery of poisonous birds in New Guinea. Dumbacher et al. (1992) documented this phenomenon in three species of Pitohui, one of which may be aposematic (Plate 3). There is reasonable evidence that distasteful or poisonous birds may be more common than previously believed (Diamond 1992). Perception Advertisement It has been proposed that conspicuous markings on birds may act as warnings to nearby conspecifics or as signals to predators that they have been detected (Baker and Parker 1979). The latter hypothesis is usually referred to as “pursuit deterrence.” Although the idea has been better developed and tested for mammals (Caro 1995; Zahavi and Zahavi 1997), the behavior was first reported in a bird: tail flicking to expose white undertail coverts by Eastern Swamphens (Porphyrio porphyrio; Woodland et al. 1980; but see Craig 1982). This idea could be considered a variant of the unprofitable prey hypothesis, as prey that have detected a predator should be more difficult to catch (Baker and Parker 1979). The flash marks of shorebirds (white stripes or patches on the wings, rump, lower back, and tail that are conspicuous when a bird flies) have been proposed as “take-off signals” to conspecifics to enhance escape from predators, as they are more commonly found in flocking species; Figure 1.6). However, this association may be confounded by the marks being more common in species inhabiting open areas (Beauchamp and Heeb 2001). Allurement to Prey Allurement to prey likely has limited application to birds. Cott (1940) recounts an unusual observation of bees being fatally attracted to the red crest

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Figure 1.6. Flash marks and other plumage traits that may function to signal take-off in flocking birds (e.g., shorebirds), to flush prey (e.g., some passerines), or to disrupt schools of fish to make them easier to catch (e.g., penguins). Markings that are white on an otherwise cryptic bird and that flash at take-off may also startle or confuse a predator. Clockwise from upper left: Northern Mockingbird (Mimus polyglottos), Willet (Catoptrophorus semipalmatus), Black Turnstone (Arenaria melanocephala), Humboldt Penguin (Spheniscus humboldti), and American Avocet (Recurvirostra americana).

of an Eastern Kingbird (Tyrannus tyrannus). It seems more plausible that the trait evolved for some other reason and then proved serendipitous for that bird. Other cases of potentially alluring color are more relevant as deception (see below). Allurement to Conspecifics There is some support for the hypothesis that white plumage is a passive recruitment signal to attract distant conspecifics so that feeding flocks could be formed (Beauchamp and Heeb 2001). Potential benefits could be increased food intake rate or increased predator vigilance (Simmons 1972). Cohesion and Coordination of the Flock Brooke (1998) tested several hypotheses for the function of flash marks on shorebirds (Figure 1.6). One of the more plausible explanations was that these markings may help coordinate flight within flocks to reduce predation or to increase aerodynamic efficiency. Furthermore, related to the latter, Brooke (1998) noted that geese that were long-distance migrants (Anser and Branta) all have bold, white rumps.

Natural Selection and Coloration

Startle, Flash, Confusion Color may be used to enhance behaviors that serve to startle or confuse predators or prey (Plate 5). Although it seems intuitive that the sudden appearance of a white flash mark on a cryptic bird (Figure 1.6) could startle a predator, the actual psychological effect on observers, in this context, has not been studied. What is known is that patterns that are rounded in shape are more striking and easily seen and recognized (Scaife 1976a,b). In addition, Forsman and Merilaita (1999) suggest that species possessing warning coloration should be subjected to selection for large and symmetrical pattern elements. The eyelike shapes on the wings of the Sunbittern (Eurypyga helias), especially as they are used to display to predators (del Hoyo et al. 1996), seem to be a good example. Baker and Parker (1979:69–70) even proposed that the ocelli of peacocks may “serve to confuse predators at a time when the birds are otherwise preoccupied.” Such an explanation underestimates the abilities of predators (Zahavi and Zahavi 1997). However, recently there have been results showing the effectiveness of contrasting color patches in eluding predators. Palleroni et al. (2005) studied coloration of feral Rock Pigeons (Columba livia) in relation to predation by Peregrine Falcons (Falco peregrinus). Using both experimental and extensive observational data, they showed that the white rump patch of the wild phenotype significantly reduced the success rate of attacks by falcons. Palleroni et al. (1995) believed that the white patch may disguise the pigeon’s evasive roll, a dodge that is initiated by the cryptic gray wings. Although traditionally the function of conspicuous markings has largely been seen as protective, recent studies expose the potential for conspicuous patterns to be aids in foraging. Wilson et al. (1987) observed that piscivorous penguins (Spheniscus spp.) and dolphins had highly conspicuous black-andwhite markings on their flanks, compared to typically countershaded species (Pygoscelis spp.) that fed on invertebrates (Figure 1.6). Their experiments with models supported their hypothesis that conspicuous markings disrupted the schooling behavior of fish in a way that facilitated their capture. It has long been suspected that the presence of contrasting patches on the wings and tail of many passerines serve to flush insect prey (see Jablónski 1996; Figure 1.6). Recent studies of redstarts (Myioborus spp.) have provided the first good experimental evidence for color patterns being used to startle potential prey ( Jablónski 1999; Mumme 2002). Recently it has been appreciated that several small predatory birds have a contrasting pattern of two spots on the back of the head that resemble eyes

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Figure 1.7. Many pygmy-owls have two distinct eyelike spots on the nape (right), giving the impression of a face on the back of the head. There are several potential functions for this “false face,” including protection from predators or mobbing birds.

(Negro et al. 2004; J. J. Negro, G. R. Bortolotti, and J. H. Sarasola, unpubl. data). Such ocelli or eyespots, and even well-developed false faces, have been well known in pygmy-owls (Glaucidium spp.) and American Kestrels (Falco sparverius) for some time (Clay 1953; Deppe et al. 2003; Figure 1.7). They may serve to startle or confuse an attacker, be it predator, mobber, or conspecific, or as described below, they may deflect blows or be alluring to prey. Disguise Cott (1940) presented an impressive array of ideas and evidence for how deception may be used to mislead an observer as to an animal’s whereabouts, attitude, or identity. Many of these hypotheses have been better tested with, or are more applicable to, other taxa. Resemblance to Particular Objects Although this is a form of concealment, it is clearly more specialized than general color matching, in that a model object is required. An excellent (perhaps rare) example is the “broken branch” appearance of frogmouths (Podargidae) in the presence of a predator (del Hoyo et al. 1999). Note that the bird must not only use its cryptic plumage, but also adopt a particular body posture and reduce its eyes to slits (Plate 2).

Natural Selection and Coloration

Deflective Marks Conspicuously colored patches may direct an attack from more to less vulnerable parts of the body. The eyespots of owls and falcons (Deppe et al. 2003; J. J. Negro, G. R. Bortolotti, and J. H. Sarasola, unpubl. data) and the single, cryptic occipital spot of the Accipitridae (Hafner and Hafner 1977) could function to direct strikes away from the face and toward the back of the head. Small birds will attack the eyes of owls (Altmann 1956). In the first experimental test of the function of these spots, Deppe et al. (2003) presented wooden models of Northern Pygmy-owls (Glaucidium gnoma) to a community of passerines. They found that attacks were redirected toward the front, not the rear, of the model with eyespots. Conspicuous patterns on wings and tails could also potentially deflect attacks (Baker and Parker 1979; Savalli 1995), but at least for shorebirds, they are not generally placed on the least vulnerable areas (Brooke 1998). The idea has also been extended to characters that deflect the attack of enemies from more to less vulnerable members of the species (Cott 1940; Baker and Parker 1979). For example, bright patterns could be supplemental to such behavior as injury feigning and so help parents to lead predators from the nest (Baker and Parker 1979). Less plausible is the possibility that sexual dichromatism of some species, or delayed molt of male ptarmigan, evolved for this reason (Baker and Parker 1979; Montgomerie et al. 2001). Directive Marks Rather than being protective, as are deflective colors, directive markings may have an “aggressive” function to obtain prey or intimidate enemies. Cott (1940) writes that the vertebrate eye is an instrument of intimidation. Brightly colored irides, fairly common in birds but rare in other homeotherms (Oliphant et al. 1992), are supposedly typical in “predaceous and well protected forms” (Cott 1940:389). Although this generality needs to be properly analyzed, one only has to look into the piercing yellow and orange eyes of Bubo owls to see how effective intimidation may be (Plate 14, Volume 1)! Alluring Colors The bird literature has few plausible examples of alluring colors. The false face of small owls, many falcons, and some other raptors may induce mobbing in passerines as an aid in killing or censusing prey ( J. J. Negro, G. R. Bortolotti,

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and J. H. Sarasola, unpubl. data). It is well known that such simple stimuli as eyespots will elicit a mobbing response in passerines (Hinde 1954). Mimicry As discussed above, there is good evidence for the existence of distasteful and noxious birds. Early research dates back to a limited experiment by Swynnerton using a cat (see Cott 1940:413). He suggested that, of four species that were similar in appearance, two palatable species were mimetic of two that were distasteful (drongos [Dicrurus spp.]). Diamond (1992) proposed that there may be examples in New Guinea of both Batesian mimicry, in which nonpoisonous species copy poisonous ones, as well as Müllerian mimicry, in which a groups of species share common warning signals. Although the palatability or dangerousness of only a few species has been confirmed, these birds travel in large mixed-species flocks. As most are predominantly brown and black, it may be difficult for predators to discriminate among them. Dumbacher and Fleischer’s (2001) phylogenetic analysis suggests that one clade of the Variable Pitohui (Pitohui kirhocephalus), which, as a species, is extraordinarily diverse in plumage color, and the Hooded Pitohui (P. dichrous) are Müllerian mimics (Plate 3). Independent of the issue of palatability, tropical birds are implicated in another potential form of mimicry of which little is known. This so-called “social mimicry” (Moynihan 1968; Diamond 1982) involves the tendency for members of mixed-species flocks to resemble one another. The similarity is sometimes quite striking; for example, see Diamond’s (1982) analysis of friarbirds (Philemon spp.) and orioles (Oriolus spp.). Potential explanations include reduction in interspecific aggression, maintenance of interspecific territories, increased flock cohesion, and protection from predators by either accompanying a pugnacious species, or by reducing the chance of a predator selecting a rare phenotype (Diamond 1982; Savalli 1995). It is also possible that the species are similar because of character convergence rather than mimicry (Burtt and Gatz 1982). Another potential example of Batesian mimicry is the similarity between the striking wing patches of kleptoparasitic skuas (Stercorarius spp. and Catharacta spp.) and two Pterodroma spp. petrels (Spear and Ainley 1993). Skuas do not parasitize conspecifics, and so the petrels appear to benefit by being victims less often compared to nonmimetic procellarids. Alternatively, the petrels may mimic skuas so that they can intimidate other birds and thus increase their own success as parasites (Spear and Ainley 1993).

Natural Selection and Coloration

Predatory birds have been implicated in cases of “aggressive mimicry”; that is, where the model (unlike Batesian mimicry) is not dangerous. Zonetailed Hawks (Buteo albonotatus) are said to be similar in appearance and behavior to a harmless scavenger, the Turkey Vulture (Cathartes aura), so that they may get closer to prey (Willis 1963). The insectivorous Rufous-thighed Kite (Harpagus diodon) may use its resemblance to a bird-eating raptor, the Bicolored Hawk (Accipiter bicolor), to scare off birds that may disturb its prey (Willis 1976). The eyespots and false faces of predatory birds, mostly falcons, may mimic owls (Clay 1953; J. J. Negro, G. R. Bortolotti, and J. H. Sarasola, unpubl. data). Passerines habitually and vigorously mob owls, so stimulating a close approach, or manipulating the direction of the attacking mobber, may facilitate prey capture (Deppe et al. 2003). Raptors could also be encouraging mobbing to census prey in an area. Similarly, the Common Hawk-cuckoo (Cuculus varius) and other cuckoos are believed to mimic Accipiter hawks in morphology and plumage to induce mobbing so that they can locate potential hosts (del Hoyo et al. 1997).

Summary Surprisingly, hypotheses concerning the survival advantages of avian coloration have seldom been rigorously formulated and tested. The function of color in birds may not involve how the bird is perceived by other animals. Instead, color may provide protection from abrasion or damage from UV radiation or bacteria degradation. Although plumage coloration should influence thermoregulatory costs, most studies have failed to find convincing associations between color and climate. The heads of birds are particularly rich with patterns, and dark lines and patches are suspected to aid an individual’s vision by reducing glare or providing a sight-line. By far the most studied of potential naturally selected functions for coloration involves interactions between predators and prey. The same protective benefits that color may offer a bird that is subject to predation may also be used by the predatory birds that seek to capture it. The visibility of a bird can be described according to one of three classes of function: concealment, advertisement, and deception. Concealment may be enhanced by a variety of optical mechanisms, such as background matching, countershading, and disruptive coloration. Alternatively, birds may choose to be conspicuous to advertise their unprofitability as prey, or to warn, confuse, and startle predators. Deception may be used to mislead an observer to the bird’s identity, attitude, or whereabouts. It is perhaps not surprising that

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prey species may avoid predators in this fashion, but predatory birds may use deceptive coloration to attract and confuse prey species to make them more vulnerable.

References Alaluf, S., U. Heinrich, W. Stahl, H. Tronnier, and S. Wiseman. 2002. Dietary carotenoids contribute to normal human skin color and UV photosensitivity. J Nutr 132: 399–403. Altmann, S. A. 1956. Avian mobbing behavior and predator recognition. Condor 58: 241–253. Andersson, M. 1994. Sexual Selection. Princeton, NJ: Princeton University Press. Baker, R. R., and C. J. Bibby. 1987. Merlin Falco columbarius predation and theories of the evolution of bird coloration. Ibis 129: 259–263. Baker, R. R., and G. A. Parker. 1979. The evolution of bird coloration. Phil Trans R Soc London B 287: 63–130. Barrowclough, G. F., and F. C Sibley. 1980. Feather pigmentation and abrasion: Test of a hypothesis. Auk 97: 881–883. Beauchamp, G., and P. Heeb. 2001. Social foraging and the evolution of white plumage. Evol Ecol Res 3: 703–720. Bent, A. C. 1963. Life Histories of North American Marsh Birds. New York: Dover Publications. Bonser, R. H. C. 1995. Melanin and the abrasion resistance of feathers. Condor 97: 590–591. Bonser, R. H. C., and M. S. Witter. 1993. Indentation hardness of the bill keratin of the European Starling, Sturnus vulgaris. Condor 95: 736–738. Bortolotti, G. R., J. J. Negro, J. L., Tella, T. Marchant, and D. M. Bird. 1996. Sexual dichromatism in birds independent of diet, parasites and androgens. Proc R Soc London B 263: 1171–1176. Bortolotti, G. R., J. E. Smits, and D. M. Bird. 2003. Iris colour of American Kestrels varies with age, sex, and exposure to PCBs. Physiol Biochem Zool 76: 99–104. Bretagnolle, V. 1993. Adaptive significance of seabird coloration: The case of procellariiforms. Am Nat 142: 141–173. Brooke, M. D. 1998. Ecological factors influencing the occurrence of “flash marks” in wading birds. Funct Ecol 12: 339–346. Buckley, P. A. 1987a. Epilogue and prologue: Past and future research in avian genetics. In F. Cooke, and P. A. Buckley, ed., Avian Genetics, 453–475. New York: Academic Press. Buckley, P. A. 1987b. Mendelian genetics. In F. Cooke and P. A. Buckley, ed., Avian Genetics, 1–44. New York: Academic Press.

Natural Selection and Coloration Burtt, E. H., Jr. 1979. Tips on wings and other things. In E. H. Burtt, Jr., ed., The Behavioral Significance of Color, 76–110. New York: Garland STPM Press. Burtt, E. H., Jr. 1981. The adaptiveness of animal colors. Bioscience 31: 723–729. Burtt, E. H., Jr. 1984. Colour of the upper mandible: An adaptation to reduce reflectance. Anim Behav 32: 652–658. Burtt, E. H., Jr. 1986. An analysis of physical, physiological, and optical aspects of avian coloration with emphasis on wood-warblers. Ornithol Monogr 38: 1–126. Burtt, E. H., Jr., and A. J. Gatz, Jr. 1982. Color convergence: Is it only mimetic? Am Nat 119: 738–740. Burtt, E. H., Jr., and J. M. Ichida. 1999. Occurrence of feather-degrading bacilli in the plumage of birds. Auk 116: 364–372. Burtt, E. H., Jr., and J. M. Ichida. 2004. Gloger’s Rule, feather-degrading bacteria, and color variation among Song Sparrows. Condor 106: 681–686. Butler, M., and A. S. Johnson. 2004. Are melanized feather barbs stronger? J Exp Biol 207: 285–293. Cade, T. J. 1982. The Falcons of the World. Ithaca, NY: Cornell University Press. Caro, T. M. 1995. Pursuit-deterrence revisited. Trends Ecol Evol 10: 500–503. Clay, W. M. 1953. Protective coloration in the American Sparrow Hawk. Wilson Bull 65: 129–135. Cooke, F., and P. A. Buckley. 1987. Avian Genetics. New York: Academic Press. Cott, H. B. 1940. Adaptive Coloration in Animals. London: Methuen & Co. Cott, H. B. 1947. The edibility of birds: Illustrated by five years’ experiments and observations (1941–1946) on the food preferences of the hornet, cat and man; and considered with special reference to theories of adaptive coloration. Proc Zool Soc London 116: 371–524. Cott, H. B., and C. W. Benson. 1970. The palatability of birds, mainly based on observations of a tasting panel in Zambia. Ostrich Suppl 8: 375–384. Craig, J. L. 1982. On the evidence for a “pursuit deterrent” function of alarm signals of Swamphens. Am Nat 119: 753–755. Cronin, H. 1991. The Ant and the Peacock. Cambridge: Cambridge University Press. Curio, E. 1975. The functional organization of anti-predator behaviour in the Pied Flycatcher: A study of avian visual perception. Anim Behav 23: 1–115. Dale, S., and T. Slagsvold. 1996. Plumage coloration and conspicuousness in birds: Experiments with the Pied Flycatcher. Auk 113: 849–857. Darwin, C. 1871. The Descent of Man and Selection in Relation to Sex. London: John Murray. del Hoyo, J., A. Elliott, and J. Sargatal. 1996. Handbook of the Birds of the World. Volume 3. Barcelona: Lynx Edicions. del Hoyo, J., A. Elliott, and J. Sargatal. 1997. Handbook of the Birds of the World. Volume 4. Barcelona: Lynx Edicions.

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gary r. bortolot ti del Hoyo, J., A. Elliott, and J. Sargatal. 1999. Handbook of the Birds of the World. Volume 5. Barcelona: Lynx Edicions. Deppe, C., D. Holt, J. Tewksbury, L. Broberg, J. Petersen, and K. Wood. 2003. Effect of Northern Pygmy-owl (Glaucidium gnoma) eyespots on avian mobbing. Auk 120: 765–771. Diamond, J. M. 1982. Mimicry of friarbirds by orioles. Auk 99: 187–196. Diamond, J. M. 1992. Rubbish birds are poisonous. Nature 360: 19–20. Dumbacher, J. P, and R. C. Fleischer. 2001. Phylogenetic evidence for color pattern convergence in toxic piohuis: Müllerian mimicry in birds? Proc R Soc London B 268: 1971–1976. Dumbacher, J. P., B. M. Beehler, T. F. Spande, H. M. Garraffo, and J. W. Daly. 1992. Homobatrachotoxin in the genus Pitohui: Chemical defense in birds? Science 258: 799–801. Ficken, R. W., P. E. Matthiae, and R. Horwich. 1971. Eye marks in vertebrates: Aids to vision. Science 173: 936–939. Ficken, R. W., and Wilmot, L. B. 1968. Do facial eye-stripes function in avian vision? Am Mid Nat 79: 522–523. Forsman, A., and S. Merilaita. 1999. Fearful symmetry: Pattern size and asymmetry affects aposematic signal efficacy. Evol Ecol 13: 131–140. Fowlie, M. K., and O. Kruger. 2003. The evolution of plumage polymorphism in birds of prey and owls: The apostatic selection hypothesis revisited. J Evol Biol 16: 577–583. Galeotti, P., D. Rubolini, P. O. Dunn, and M. Fasola. 2003. Colour polymorphism in birds: Causes and functions. J Evol Biol 16: 635–646. Gavish, L., and B. Gavish. 1981. Patterns that conceal a bird’s eye. Z Tierpsychol 56: 193–204. Goldstein, G., K. R. Flory, B. A. Browne, S. Majid, J. M. Ichida, and E. H. Burtt, Jr. 2004. Bacteria degradation of black and white feathers. Auk 121: 656–659. Gomez, D., and M. Théry. 2004. Influence of ambient light on the evolution of colour signals: Comparative analysis of a Neotropical rainforest bird community. Ecol Lett 7: 279–284. Götmark, F. 1987. White underparts in gulls function in hunting camouflage. Anim Behav 35: 51–56. Götmark, F. 1993. Conspicuous coloration in male birds is favoured by predation in some species and disfavoured in others. Proc R Soc London B 253: 143–146. Götmark, F. 1994a. Does a novel bright colour patch increase or decrease predation? Red wings reduce predation risk in European Blackbirds. Proc R Soc London B 256: 83–87. Götmark, F. 1994b. Are bright birds distasteful? A re-analysis of H. B. Cott’s data on the edibility of birds. J Avian Biol 25: 184–197.

Natural Selection and Coloration Götmark, F. 1997. Bright plumage in the Magpie: Does it increase or reduce the risk of predation? Behav Ecol Sociobiol 40: 41–49. Götmark, F., and U. Unger. 1994. Are conspicuous birds unprofitable prey? Field experiments with hawks and stuffed prey species. Auk 111: 251–262. Gould, S. J. 1991. Bully for Brontosaurus. New York: W.W. Norton. Grande, J. M., J. J. Negro, and M. J. Torres. 2004. The evolution of bird plumage colouration: A role for feather-degrading bacteria? Ardeola 51: 375–383. Guilford, T., and M. S. Dawkins. 1991. Receiver psychology and the evolution of animal signals. Anim Behav 42: 1–14. Hafner, J. C., and M. S. Hafner. 1977. The cryptic occipital spot in the Accipitridae (Falconiformes). Auk 94: 293–303. Hailman, J. P. 1977. Optical Signals. Bloomington: Indiana University Press. Harvey, P. H., and M. D. Pagel. 1991. The Comparative Method in Evolutionary Biology. Oxford: Oxford University Press. Hinde, R. A. 1954. Factors governing the changes in strength of a partially inborn response, as shown by the mobbing behaviour of the Chaffinch (Fringilla coelebs). I. The nature of the response, and examination of its course. Proc R Soc London B 142: 306–331. Honkavaara, J., M. Koivula, E. Korpimäki, H. Siitari, and J. Viitala. 2002. Ultraviolet vision and foraging in terrestrial vertebrates. Oikos 98: 505–511. Huxley, J. S. 1938. Threat and warning coloration in birds, with a general discussion of the biological functions of color. In F. F. R. Jourdain, ed., Proceedings of the Eighth International Ornithological Congress, 430–435. Oxford: Oxford University Press. Jablónski, P. 1996. Dark habitats and bright birds: Warblers may use wing patches to flush prey. Oikos 75: 350–352. Jablónski, P. 1999. A rare predator exploits prey escape behavior: The role of tailfanning and plumage contrast in foraging of the Painted Redstart (Myioborus pictus). Behav Ecol 10: 7–14. Lee, D. S., and G. S. Grant. 1986. An albino Greater Shearwater: Feather abrasion and flight energetics. Wilson Bull 98: 488–490. Londei, T. 2004. Ground jays expand plumage to make themselves less conspicuous. Ibis 146: 158–160. Marler, P. 1956. Behaviour of the Chaffinch. Behav Suppl 5: 1–184. Mock, D. W. 1980. White-dark polymorphisms in herons. Proceedings of the 1st Welder Wildlife Foundation Symposium, 114–161. Montgomerie, R., B. Lyon, and K. Holder. 2001. Dirty ptarmigan: Behavioral modification of conspicuous male plumage. Behav Ecol 12: 429–438. Mottram, J. C. 1915. An experimental determination of the factors which cause patterns to appear conspicuous in nature. Proc Zool Soc London 1915: 383–419.

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gary r. bortolot ti Moynihan, M. 1968. Social mimicry; character convergence versus character displacement. Evolution 22: 315–331. Mumme, R. L. 2002. Scare tactics in a Neotropical warbler: White tail feathers enhance flush-pursuit foraging performance in the Slate-throated Redstart (Myioborus miniatus). Auk 119: 1024–1035. Negro, J. J., G. R. Bortolotti, J. L. Tella, K. J. Fernie, and D. M. Bird. 1998. Regulation of integumentary colour and plasma carotenoids in American Kestrels consistent with sexual selection theory. Funct Ecol 12: 307–312. Negro, J. J., J. H. Sarasole, F. Fasias, and I. Zorrilla. in press. Function and occurrence of facial flushing in birds. Comp Biochem Physiol A. Negro, J. J., J. M. Grande, and J. H. Sarasola. 2004. Do Eurasian Hobbies (Falco subbuteo) have “false eyes” on the nape? J Raptor Res 38: 287–288. Newton, I. 2003. The Speciation and Biogeography of Birds. New York: Academic Press. Oliphant, L. W., J. Hudon, and J. T. Bagnara. 1992. Pigment cell refugia in homeotherms—The unique evolutionary position of the iris. Pigment Cell Res 5: 367–371. Owens, I. P. F., and P. M. Bennett. 1994. Mortality costs of parental care and sexual dimorphism in birds. Proc R Soc London B 257: 1–8. Palleroni, A., C. T. Miller, M. Hauser, and P. Marler. 2005. Prey plumage adaptation against falcon attack. Nature 434: 973–974. Parker, J. W. 1985. Albinism and maladaptive feather wear in American Kestrels. Kingbird 35: 159–162. Phillips, G. C. 1962. Survival value of the white coloration of gulls and other sea birds. Ph.D. diss., Oxford University, Oxford. Preston, C. R. 1980. Differential perch site selection by color morphs of the Redtailed Hawk (Buteo jamaicensis). Auk 97: 782–789. Price, T., and M. Pavelka. 1996. Evolution of a colour pattern: History, development, and selection. J Evol Biol 9: 451–470. Price, T. D., and P. T. Boag. 1987. Selection in natural populations of birds. In F. Cooke and P. A. Buckley, ed., Avian Genetics, 257–287. New York: Academic Press. Promislow, D., R. Montgomerie, and T. E. Martin. 1992. Mortality costs of sexual dimorphism in birds. Proc R Soc London B Biol Sci 250: 143–150. Promislow, D., R. Montgomerie, and T. E. Martin. 1994. Sexual selection and survival in North American waterfowl. Evolution 48: 2045–2050. Rytkönen, S., P. Kuokkanen, M. Hukkanen, and K. Huhtala. 1998. Prey selection by Sparrowhawks Accipiter nisus and characteristics of vulnerable prey. Ornis Fenn 75: 77–87. Savalli, U. M. 1995. The evolution of bird coloration and plumage elaboration—A review of hypotheses. Curr Ornithol 12: 141–190.

Natural Selection and Coloration Scaife, M. 1976a. The response to eye-like shapes by birds. I. The effect of context: A predator and a strange bird. Anim Behav 24: 195–199. Scaife, M. 1976b. The response to eye-like shapes by birds. II. The importance of staring, pairedness and shape. Anim Behav 24: 200–206. Shawkey, M. D., and G. E. Hill. 2004. Feathers at a fine scale. Auk 121: 652–655. Simmons, K. E. L. 1972. Some adaptive features of seabird plumage types. Br Birds 65: 465–479, 510–521. Slagsvold, T., S. Dale, and A. Kruszewicz. 1995. Predation favours cryptic coloration in breeding male Pied Flycatchers. Anim Behav 50: 1109–1121. Spear, L., and D. G. Ainley. 1993. Kleptoparasitism by Kermadec Petrels, jaegers, and skuas in the eastern tropical Pacific: Evidence of mimicry by two species of Pterodroma. Auk 110: 222–233. Stahl, W., and H. Sies. 2002. Carotenoids and protection against solar UV radiation. Skin Pharmacol Appl Skin Physiol 15: 291–296. Thayer, A. H. 1896. The law which underlies protective coloration. Auk 13: 124–129. Thayer, G. H. 1909. Concealing-coloration in the Animal Kingdom. New York: Macmillan. Tickell, W. L. N. 2003. White plumage. Waterbirds 26: 1–12. Wallace, A. R. 1889. Darwinism. London: Macmillan. Walsberg, G. E. 1982. Coat color, solar heat gain, and conspicuousness in the Phainopepla. Auk 99: 495–502. Wheeler, B. K. 2003. Raptors of Eastern North America. Princeton, NJ: Princeton University Press. Willis, E. O. 1963. Is the Zone-tailed Hawk a mimic of the Turkey Vulture? Condor 65: 313–317. Willis, E. O. 1976. A possible reason for mimicry of a bird-eating hawk by an insecteating kite. Auk 93: 841–842. Wilson, R. P., P. G. Ryan, A. James, and M.-P. T. Wilson. 1987. Conspicuous coloration may enhance prey capture in some piscivores. Anim Behav 35: 1558–1559. Wolf, B. O., and G. E. Walsberg. 2000. The role of the plumage in heat transfer processes of birds. Am Zool 40: 575–584. Woodland, D. J., Z. Jaafar, and M.-L. Knight. 1980. The “pursuit deterrent” function of alarm signals. Am Nat 115: 748–753. Zahavi, A., and A. Zahavi. 1997. The Handicap Principle. Oxford: Oxford University Press.

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2 Intraspecific Variation in Coloration james dale

With some birds, it seems that if you’ve seen one, you’ve seen them all. American Crows (Corvus brachyrhynchos), for instance, appear remarkably similar from individual to individual: jet black from bill to tail. There is undoubtedly some degree of variability among individuals (especially from the perspective of a crow), but variation in crow patterning and blackness is unarguably low. Why are crows so uniformly black? At the other extreme, breeding male Ruffs (Philomachus pugnax) are among the most variably colored wild species of bird. Ruffs display impressive ornamental plumes around their necks and heads that range in color from white, cream, straw, rust, brown, to black. These plumes are often multicolored, with secondary colors appearing in diverse patterns (e.g., bands, bars, flecks, spots, splotches). The legs, bills, and facial wattles of male Ruffs also vary from yellow, orange, red, green, to black (Plate 7). All of these traits, which for the most part vary independently of one another (Lank and Dale 2001), make each Ruff appear unique. Why are Ruffs so variable? More generally, why are there such striking differences in the degree to which coloration is variable within species? In this chapter, I suggest that most intraspecific color variation (Box 2.1) can be understood from a framework based on communication theory, in which “signalers” use coloration to provide information to “receivers” (Wiley 1983; Krebs and Davies 1993; Johnstone 1997a). To understand color variability in this context, we therefore need to resolve the specific information that birds broadcast about themselves with color.

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Box 2.1. Properties of Intraspecific Color Variation Studying variability in color is challenging, because coloration varies in so many different dimensions. First, the actual color itself can vary along the tristimulus color variables of hue, saturation (or chroma), and brightness (HSB; see Chapters 2 and 3, Volume 1). Second, a patch of color can vary in its size and/or pattern. Third, there can be variability in the number of different patches of color (or traits). Often intraspecific color variability involves alternative appearances among different groups of classes of individuals within a species (Butcher and Rohwer 1989). For example, males often look different than females. Four basic groups of classes of individuals that differ in coloration can occur within a species: (1) age groups (e.g., delayed plumage maturation), (2) sexes (sexual dichromatism), (3) seasonally different populations (seasonal variation), and (4) geographically different populations (geographical variation). Once the color dimension of interest has been identified and this dimension has been measured in a sample of individuals, there are three basic properties of variability that can be considered: (1) the degree of variability can range from low to high, (2) the modality of variability can be unimodal or multimodal, and (3) the continuity of variability can be continuous or discrete (Figure B2.1). Across different species, these properties vary substantially, and this is the case whether one is looking at variability within (intra-) or between (inter-) different classes.

Number of individuals

Degree

Modality

Continuity

low

unimodal

continuous

high

bimodal

discrete

Color scale

Figure B2.1. Three basic properties of color variability in birds.

Dishonest (camouflage) Dishonest (apostatic)

Presence Honest (beacons)

Individual identity

Kinship

Mating Genetic compatibility Reinforcement Species recognition Within-population

Quality Indicators Amplifiers Attractiveness (Fisher traits) Strategy Gender Status-related

Signal type

Stabilizing Negative frequency dependent

Stabilizing

Negative frequency dependent Negative frequency dependent

Disruptive Stabilizing Diversifying

Mate attraction, distraction displays, flocking, startledisplays Avoid detection by predators or prey Avoid detection by predators or prey

Neighbor-stranger, kin and mate recognition, dominance hierarchies, reciprocal altruism

Mate choice—avoid fitness-reducing hybridization Mate choice—avoid interspecies breeding Mate choice—MHC signaling, increase offspring heterozygosity Cooperation, inbreeding avoidance

Sex recognition Delayed-plumage maturation, condition-dependent strategies Cooperative display, territorial versus parental strategies

Disruptive Disruptive

Disruptive

Mate-choice, competition, parent-offspring, predation Associated with indicators Mate-choice

Signaling contexts

Directional Stabilizing Directional

Selection

Table 2.1. Seven Different Types of Information That Can Be Signaled by Avian Coloration

Signal blends with ambient light conditions Avoidance-image hypothesis

Signal contrasts with ambient light conditions

Recognition of unfamiliar kin, recognition template based on receiver’s own phenotype, or phenotype of known kin Recognition of familiar individuals, receiver recognition template based on signaler’s phenotype

Signals compatibility alleles for any loci for which there are multiple optimal combinations

Condition dependent, differentially costly Reduce perception error of indicator variation by receivers Not required to be costly, but can be if signal elaboration is extreme Strategy-dependent cooperation required

Comment

Intraspecific Variation in Coloration

Typically, studies of communication focus on receivers of signals. They ask: Do receivers respond to signal variation? If so, why? In this chapter, however, I focus on the signaler. If a signaler has been selected to broadcast particular information using color (either honestly or dishonestly), then what is the outcome of such selection in terms of signal properties? In other words, what do signals that reveal (or conceal) different kinds of information look like? For color to reveal specific information, there have to be mechanisms whereby that information is coupled with specific expressions of color. Thus I consider both the information content of signal variability and the potential sources of that variability. All variability ultimately arises from two sources: genes and the environment. Genetic variation comes from genes that code directly for different color variants, or alternatively through genes that have pleiotropic effects on color development. Environmental variability arises through an interaction among various environmental parameters (e.g., social environment, parasites, territory quality, age, season, nutrition; Chapter 12, Volume 1) and the penetrance of genes coding for signal phenotypes. Birds use color to communicate information in at least seven broad categories: quality, attractiveness, strategy, genetic compatibility, kinship, individual identity, and presence (Table 2.1). I develop predictions about the nature of variability for each of these seven kinds of signals, under the assumption that color variation is directly related to variation in the specific information revealed. Table 2.1 summarizes the seven kinds of color-based signals that I discuss in this chapter, the nature of selection acting on the signals (e.g., stabilizing versus directional), and the signaling contexts expected to be associated with these signals. Table 2.2 summarizes the expected patterns of variability of color-based signals that function to reveal these types of information. Below, I review these signals, their relevant selective forces, expected forms of variability, and observed patterns in selected case studies. Although my focus is on visual signals in birds, the generalizations developed here should offer insight into signal properties in all sensory modalities in all taxa.

Quality Most recent research on bird colors has focused on their potential function as condition-dependent signals of quality (or “indicators”)—cues that communicate information about aspects of the bearer’s relative phenotypic and genetic constitution (Zahavi 1975; Hamilton and Zuk 1982; Kodric-Brown and Brown 1984; Grafen 1990; Andersson 1994; Olson and Owens 1998; Dale

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Species recognition Within-population composition Kinship Individual identity

Genetic compatibility Reinforcement

Mating

Status-related

Strategy Gender

Multimodal Multimodal

Moderate Moderate to high

Low Moderate

Bimodal (unimodal within) Unimodal Multimodal

Bimodal (assuming two strategies) Bimodal (assuming two strategies)

Bimodal

Unimodal Unimodal

Unimodal

Modality of variability

High between, low within

High (between strategies) Low (within strategies) High (between strategies) Low (within strategies) High (between strategies) Low (within strategies)

Low Low

Moderate

Quality Indicators

Amplifiers Attractiveness (Fisher trait)

Degree of variability

Signal type

Continuous Continuous

Continuous Continuous

Discrete

Discrete

Discrete

Discrete

Continuous Continuous

Continuous

Continuity of variability

Sex Sex

Sex Sex

Sex, geographic

Sex

Age, sex

Sexb

Sex, geographic

Age, sex, season, geographic

Interclass variabilitya

Genetically determined, polygenic Genetically determined, polygenic

Genetically determined, fixed Genetically determined

Genetically determined

Genetically determined, sexdependent Environmentally determined, age dependent Genetically determined

Environmentally determined and pleiotropic effects of additive genetic variance for condition, signal alleles fixed Genetically fixed Genetically determined, degree of genetic variance depends on equilibrium state

Source of variability

Table 2.2. Color-Based Signal Types in Birds and Their Expected Properties of Signal Variability, Differences among Classes, and Degrees of Genetic or Environmental Determination

Moderate to high

Dishonest (apostatic)

Multimodal

Unimodal (multimodal if ambient conditions variable)

Unimodal Continuous (Discrete if ambient conditions vary discretely) Discrete

Continuous

None

Sex, season, geographic

Sex

a. Possible (but not required) interclass variation resulting from differential selection on classes to broadcast particular information types. b. Required.

Low, (high if ambient conditions variable)

Low

Dishonest (camouflage)

Presence Honest (beacons)

Genetically determined, high additive variance

Genetically determined, low additive variance Genetically determined, low additive variance (high variance if ambient conditions variable)

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et al. 2001). Here I consider quality to be a broad concept that includes various aspects of a bird’s constitution (e.g., social status, parental care abilities, “good genes”). All quality indicators share in common the requirement of high and differential costs to their bearers for the signals to be reliable (Zahavi 1975; Kodric-Brown and Brown 1984; Grafen 1990). All three of the major mechanisms of color production in birds (carotenoids, melanins, and microstructures) have been demonstrated to be related to various aspects of individual quality (Chapter 12, Volume 1; Chapter 6; also see Figure 2.2). Even the presumably cheapest color to develop, white (no pigmentation), is related to quality in some species (Jones 1990; Pärt and Qvarnstrom 1997; Török et al. 2003). Currently there is a great deal of interest devoted to resolving the specific costs of color displays and the specific aspects of quality they reveal. Degrees of Variability Signals of quality have higher degrees of variability than nonsignaling morphological traits (Alatalo et al. 1988; Møller and Hoglund 1991; Møller and Pomiankowski 1993; Andersson 1994; Pomiankowski and Møller 1995; Cuervo and Møller 1999, 2001; Dale et al. 2001). However, our understanding of the nature of this variability in quality signals is rudimentary. Honesty in quality signals would break down if individuals did not vary in their ability to meet the theoretically required costs of signal elaboration (Zahavi 1975; KodricBrown and Brown 1984; Grafen 1990); without variation in the relative costs, receivers would not be favored to pay attention to the signals (Alatalo et al. 1988; Andersson 1994; Dale et al. 2001). High variability in quality signals is a product of the complex developmental processes involved in their expression. First, quality signals are strongly environmentally dependent. Indeed, aspects of the social environment (Griffith et al. 1999; Parker et al. 2002; McGraw et al. 2003), parasite exposure (McGraw and Hill 2000), nutritional conditions (McGraw et al. 2002), exposure to pollution (Eeva et al. 1998), and global climatic conditions (Garant et al. 2004) have all been shown to affect expression of quality signals. Second, quality signals express high degrees of additive genetic variance (Pomiankowski and Møller 1995), based on pleiotropic effects of genes affecting condition (Rowe and Houle 1996; Kotiaho et al. 2001). At equilibrium, the genetic basis for the signal traits themselves is expected to be fixed (Maynard Smith 1985; Andersson 1986; Kirkpatrick 1986; Pomiankowski 1987, 1988; Tomlinson 1988; Heywood 1989; Hill 1994), and all individuals in a population

Intraspecific Variation in Coloration

are expected to have similar “potential” to produce elaborate (costly) signals (Hill 1992, 1994). How individuals fulfill that potential (i.e., the degree of penetrance of the fixed signal genes) is influenced by a large number of pathways that independently contribute to trait expression, resulting in high phenotypic variability (Rowe and Houle 1996; Kotiaho et al. 2001). There are obvious differences across species in the extent to which colorbased quality signals vary, although this variability has not yet been quantified (see Box 2.2). For example, carotenoid-based plumage redness signals male quality in both House Finches (Carpodacus mexicanus; Plate 14; Hill 1991) and Northern Cardinals (Cardinalis cardinalis; Plate 25; Wolfenbarger 1999). Yet apparent intraspecific variability in plumage hue and saturation of male cardinals is considerably lower than it is in House Finches (Figure 2.1). Why do cardinals vary less than House Finches? One possibility is that carotenoids are more limiting in House Finches, perhaps due to an exclusively granivorous diet (Hill 1993), and so lower carotenoid availability is manifested in higher overall signal variability. In addition, as the color of quality signals approaches full expression, overall variability is expected to be lower, as directional selection compresses the trait against physical limitations of expression. Thus, as the mean saturation level gets higher, smaller differences in saturation might be more differentially costly than they are in less saturated species. In general, a coherent theoretical framework for understanding why there are differences among species in the variability of quality signals is badly needed, as is a comprehensive descriptive survey of overall patterns of variance in colorful signals of quality in birds. All we know so far is that quality signals tend to be variable (indeed, high variability in a signal is often argued as supportive of quality signaling; Box 2.2). Exactly why quality signals vary and why some vary much more than others is poorly understood. Frequency Distributions Quality is a quantitative trait affected by various environmental and genetic factors. Because quantitative traits generally demonstrate unimodal distributions, aspects of quality, and the signals that reflect them, are also expected to be unimodal (Dale et al. 2001). Indeed, analysis of putative color-based quality signals in most species typically reveals unimodal frequency distributions (Figure 2.2; also see Senar 1999; Dale et al. 2001; Ripoll et al. 2004). The only known exception to unimodal frequency distributions for colorful quality signals occurs in the bimodal distribution of badge size in Eurasian

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Box 2.2. Quantifying Color Variability Typically, biological comparisons of variability involve calculating coefficients of variation (CV ) for traits of interest (i.e., the standard deviation as a percentage of the mean). Studies demonstrating high CV for sexually selected traits (e.g., tail length in widowbirds; Alatalo et al. 1988) in comparison to morphological traits thought to be under stabilizing natural selection (e.g., tarsus length) form the empirical basis for the commonly accepted idea that sexually selected traits tend to be highly variable (Alatalo et al. 1988; Cuervo and Møller 2001). In general, sexually selected traits demonstrate CV on the order of 10–20%, whereas naturally selected traits demonstrate CV ranging from 2% to 5%. The use of CV to compare color variability is not possible, because the dimensions of color are often assigned along arbitrary numerical scales. Thus variance in color variables does not usually scale with the mean, and so the CV of a color variable is not directly comparable to the CV of a length measurement. Indeed, studies that have used the high CVs of color-based traits as empirical support for signaling functions are statistically flawed (e.g., McGraw and Hill 2000; Massaro et al. 2003; Mennill et al. 2003; McGraw 2004; Doucet et al. 2005). For example, consider variation in color brightness, a scale that ranges from 0 (no reflectance) to 100% (full reflectance). If two samples have mean brightness values of 10 and 90, and each sample has a standard deviation of 10, the CV of the two samples will be 100% and 11%, respectively. These values suggest the first sample is nine times more variable than the second. However, the opposite conclusion would be drawn if the brightness scale is redefined into an equivalent “darkness” scale that ranges from 0% (no absorption) to 100% (full absorption). CV calculated using hue values on the 360° color wheel (e.g., Massaro et al. 2003) are even more problematic, because the numerical value for any given hue is completely arbitrary (e.g., a mean hue of 359° is very similar in appearance to a mean hue of 1°, both red, because pure red is defined as hue = 0°). Consider variability in bill versus plumage hue in Red-billed Queleas (see Figure 2.9). Bill hue is strikingly less variable than plumage hue in this

Intraspecific Variation in Coloration

species, but CVs for bill and plumage are similar (29.03% and 34.82%, respectively), simply because red is assigned lower hue values than yellow. CV calculated on hue values from reflectance curves (e.g., peak wavelength; Doucet and Montgomerie 2003; Mennill et al. 2003; Shawkey et al. 2003) are also problematic. Equivalent variability in longer wavelength radiation (yellow and red light) will automatically generate lower CVs than shorter wavelength radiation (blue and ultraviolet light). These CVs are not biologically meaningful, because red does not appear “longer” than blue. I strongly recommend using standard deviations (SDs) alone (or interquartile range) to compare color variability for measurements of HSB. For example, in Red-billed Queleas, SDs for bill and plumage hue are 1.64 and 10.01, respectively, demonstrating that bill hue is indeed much less variable. When the range of hue values brackets 0, negative hue values (e.g., hue = –1° instead of 359°) could be used to calculate SD, or alternatively, circular statistics could be used to calculate indices of variance. Comparisons of variability between different color dimensions (e.g., SD in hue versus SD in saturation) should be avoided. Particular caution is required when comparing SD in hue, because as mean brightness and saturation decrease, equivalent variances in hue measures result in decreased degrees of perceivable color variability (e.g., see Figure 2.7). Ideally, comparisons of color variability should thus incorporate comparisons of areas or volumes occupied by the observed scatter along saturation versus hue plots (e.g., see Figure 2.1), or saturation versus brightness versus hue plots, respectively. For color variables based on reflectance spectra, statistical techniques that quantify differences in the shapes of reflectance curves need to be developed to quantify and compare variability among species and traits. Meaningful comparison of color variability to morphological character variability under natural selection, such as tarsus length (e.g., Massaro et al. 2003; Mennill et al. 2003), is not possible. However, comparisons between color traits thought to be sexually selected versus color traits thought to be naturally selected could potentially lead to important insights. Indeed, these kinds of comparisons are badly needed to truly evaluate if sexually selected coloration is more variable than naturally selected coloration, as expected by current theory.

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Figure 2.1. Saturation versus hue for red plumage in male Northern Cardinals (n = 80) and House Finches (n = 28). Apparent variability (amount of scatter) in plumage redness is lower in cardinals than in House Finches. Color scores were measured at the center of the breast on museum specimens at the Cornell University Vertebrate Collection (Ithaca, NY) using methodology described in Dale (2000).

Siskins (Carduelis spinus; Senar et al. 1993; Ripoll et al. 2004; Chapter 2; Figure 2.2; Plate 12), a trait that signals status. Rohwer and Ewald (1981) argued that bimodal distributions could be stable for status signals, provided they are maintained by negative frequency-dependent selection. A stable bimodal distribution can result if individuals of different dominance ranks play mutually beneficial roles (Rohwer and Ewald 1981; also see Ripoll et al. 2004; Chapter 3). In such cases, badge size, in addition to being a signal of quality (status), also signals a variable behavioral strategy. Bimodality then results from disruptive selection for honest strategy signaling (see the section on strategy below), as opposed to continuous and unimodal frequency distributions expected when there is directional selection on quality and the signals that reveal it. Amplifiers Recently there has been increased interest in the hypothesis that signal traits function as quality amplifiers (Hasson 1991; Brooks 1996; Taylor et al. 2000). Amplifiers do not reveal quality per se, but instead reduce perceptual errors by

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Figure 2.2. Frequency distributions of color-based quality indicators in 12 bird species. Graphs are arranged such that color expression associated with higher quality occurs toward the right. Note the unimodal, normal, or approximately normal distribution of color expression for a range of color types including carotenoid, structural, white, phaeomelanin, and eumelanin. Adapted or redrawn from Hill (1992), J. Dale and T. D. Williams (unpubl. data), J. Dale (unpubl. data), Massaro et al. (2003), Merila and Sheldon (1999), Senar et al. (2002), Sieffermann and Hill (unpubl. data), Török et al. (2003), Safran and McGraw (2004), Yezerinac and Weatherhead (1997), McGraw et al. (2003), and Senar et al. (1993).

receivers with respect to evaluating other traits that do signal quality (Hasson 1991). With color-based signals, amplifiers can be considered as portable “color standards” attached to quality signals, which help receivers accurately gauge true variance in a quality signal by comparing the quality signal with the amplifier. Because amplifiers are expected to result in tighter correlations between actual quality and apparent (perceived) variability in the “amplified” quality signal, they can be considered as a form of noncostly quality signaling.

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Color-based amplifiers can initially spread in a population as a form of male cheating. Noncostly traits that enhance the apparent expression of a color display will be favored and spread to fixation (Hasson 1991; Hill 1994; Taylor et al. 2000). Once all signalers have the amplifying trait, however, receivers can actually get a more reliable perception of variance in the quality signal (Brooks 1996). At equilibrium, amplifiers are therefore expected to express relatively low unimodally distributed variability and to be fixed, genetically determined traits unrelated to signaler condition (i.e., to be noncostly). In particular, black coloration may often be the best color amplifier because black offers a strong contrasting background for other bright colors. Many species with bright yellow or red patches that signal quality tend to have jet black borders that could function as amplifiers. McGraw and Hill (2000) noted that, in American Goldfinches (Carduelis tristis; Plate 30, Volume 1), cap blackness was not particularly variable and does not appear to be condition dependent. Experimentally diseased goldfinches showed no changes in the expression of their black caps, although they suffered significantly reduced expression of carotenoid-based yellow plumage. Because the cap borders yellow feathers, but is not itself related to quality, these authors speculated that black caps might function as amplifiers. Similarly, many birds have iridescent and glossy plumage (with a strong ultraviolet [UV] component) that is underlain with apparently uniform and fully melanized feathers. Such full melanization would provide a constant, and therefore noninterfering, background to UV reflectance, by absorbing the flanking regions of the spectrum and making the UV signal appear more saturated. In an aviary experiment, calorie restriction reduced the saturation of glossy blue-black dorsal plumage in male Brown-headed Cowbirds (Molothrus ater; McGraw et al. 2002; Plate 7, Volume 1), suggesting that iridescence was condition dependent. In contrast, melanization of the adjacent brown hood of the cowbirds was not affected (McGraw et al. 2002), implying that melanization may generally be more resilient to variability in the physical environment (also see Hill and Brawner 1998; McGraw and Hill 2000). In cowbirds and many other species, uniform melanization may therefore function as an amplifier of iridescent and glossy plumage.

Attractiveness Models of runaway sexual selection (Fisher 1930; Lande 1981; O’Donald 1983; review in Andersson 1994) assume that genes for the expression of traits (ex-

Intraspecific Variation in Coloration

pressed in males) and genes for mating preferences for those traits (expressed in females) become genetically correlated through assortative mating. Thereafter, trait genes and preference genes can co-evolve into extreme forms through a self-reinforcing positive feedback process. Runaway traits, or “Fisherian traits,” are therefore arbitrary signals of attractiveness. They are arbitrary because runaway selection can act on any traits with perceivable genetically determined phenotypic variance and an associated preference, and they are not expected to be related to male condition. How much variability should a color-based Fisherian trait express? Runaway selection can continue exaggerating traits until (1) all genetic variability is exhausted and either the trait or preference genes, or both, become fixed or (2) increased natural selection against extreme versions of the traits (or preferences) halts the runaway process. In the case of color-based Fisherian traits, physical constraints for color expression offer an obvious wall to halt phenotypic elaboration (i.e., saturation and brightness have limits beyond which further elaboration is impossible). Therefore Fisherian traits should display relatively low degrees of intrapopulation variance, provided population-level genetic variance in traits becomes fixed (Alatalo et al. 1988)—especially if strong directional sexual selection tends to run colors into full expression over evolutionary time. Alatalo et al. (1988) argued that runaway selection predicts high variance between different geographic locations, provided there are limitations to gene flow between populations and that the populations each arrive at different equilibrium states. Therefore runaway traits are expected to express high degrees of geographic variability (Alatalo et al. 1988). Indeed, runaway selection models suggest that the process can result in explosive speciation events within taxa with intense sexual selection, as traits and preferences in different ancestral populations diverge (Iwasa and Pomiankowski 1995; Pomiankowski and Iwasa 1998). Thus runaway traits are expected to express low degrees of intrapopulation variability (see above), but high degrees of interpopulation and interspecies variability. Interspecific diversity in plumage coloration in taxa with highly polygynous species, such as birds of paradise (Paradisaeidae), pheasants (Phasianidae) and manakins (Pipridae) (Anderson 1994; Prum 1997) provides promising candidates for signals that evolved through runaway sexual selection. Male coloration across different species in these taxa is extremely diverse, whereas female coloration tends to be rather uniform interspecifically. Indeed, Prum’s (1997) detailed study of manakins offers compelling support for the importance of

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Fisherian processes in the evolution of plumage ornamentation. When compared with closely related and monogamous tyrant flycatchers (Tyrannidae), the diversity of manakin traits suggests that manakin coloration has evolved by an explosive and unconstrained evolutionary mechanism not consistent with predictions based on quality-indicating mechanisms. If male coloration in manakins and other predominantly lekking taxa are the products of runaway selection, then intraspecific variability in these species is expected to be relatively low, unimodally distributed, geographically variable, and unrelated to male quality. These predictions have not been specifically tested, but Kodric-Brown and Brown (1984) noted that apparent intraspecific variability in manakin coloration appears to be particularly low.

Strategy Different individuals within a species often pursue alternative strategies (Rohwer and Ewald 1981; Gross 1996). When individuals form strategy-dependent cooperative alliances, signalers can be selected to broadcast information that honestly reveals their strategy, provided that it facilitates mutually fitness-enhancing interactions among strategy types (cooperation is considered here in the broadest sense of an ultimately mutualistic relationship, even if competitive elements remain between cooperators). Variability in coloration could therefore function to communicate strategy-related information (Rohwer and Ewald 1981). Strategy signals are expected to display bimodal and discrete distributions (assuming two nonoverlapping alternative strategies). Furthermore, variation in strategy signals is expected to be more strongly genetically determined when the strategy is fixed (e.g., Lank et al. 1995), but more strongly environmentally determined when the strategy is conditional (e.g., Greene et al. 2000). Signals of Gender: Sex Recognition Males and females represent the two fundamental alternative reproductive strategies, typically maintained at an equilibrium frequency close to 50:50 through negative frequency-dependent selection (Fisher 1930). Males and females obviously need to cooperate to successfully reproduce, so they must effectively communicate their sex. Sexually dichromatic traits, therefore, could function in sex recognition (Noble and Vogt 1935; Noble 1936). Visually based, specially evolved signals of gender should occur in species for which additional gender-revealing cues (i.e., sex-specific traits selected for

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Figure 2.3. Frequency distributions of plumage color are bimodal, as expected for strategy signals, in (a) both male and female Northern Flickers and (b) adult and (c) yearling Lazuli Buntings (redrawn from Greene et al. 2000). Data on flickers were collected from museum specimens at the Cowan Vertebrate Collection at the University of British Columbia (Vancouver, BC) using methodology described in McGraw et al. (2003).

by other processes) are less apparent. Presumably, signals of gender would not need to be particularly conspicuous, are expected to demonstrate completely distinct distributions between the sexes, and are expected to vary little within each sex (Figure 2.3a). Gender signaling is thus expected in species whose genders have very similar roles during courtship and reproduction (because such

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species are less likely to reveal gender through other cues) and in species that are sexually monomorphic in appearance (apart from the gender signal). Woodpeckers (Picidae) often have highly conspicuous coloration patterns, but usually there is one small difference between males and females (Short 1982; Moore 1987). Noble (1936) demonstrated that a female Northern Flicker (Colaptes auratus) was treated aggressively by her mate when experimentally given a black mustache streak typical of a male (see Figure 2.3a). The potential for visual signals of gender to play a role in reducing wasted mating effort has been demonstrated, paradoxically, in a sexually monochromatic species lacking obvious plumage variation between the sexes (Langmore and Bennett 1999). In Long-tailed Finches (Poephila acuticauda), plumage color scores in males and females overlap considerably, as demonstrated by detailed spectrophotometric analysis. Males were equally likely to court and copulate with both unfamiliar males and unfamiliar females. Langmore and Bennett (1999) argued that this species is monochromatic to allow individuals the opportunity to strategically conceal their gender to reduce sexual competition (Burley 1981). Signals of Status-Related Strategies Plumage variability can often reveal aspects of quality related to social status (see Chapter 3 and the section on quality above). Although quality signals are generally expected to be unimodally distributed, bimodal frequency distributions could arise if individuals of different statuses pursue different behavioral strategies (Rohwer and Ewald 1981). For example, status-related strategy signaling may provide a general explanation for patterns of delayed plumage maturation (DPM) (Chapter 3), wherein individuals in different age-groups have diagnostic color patterns. Indeed, many instances of DPM appear related to status signaling (Lyon and Montgomerie 1986), with subadult plumages reflecting subordinate status and adults being less aggressive to individuals in subadult plumage. DPM should be considered strategy signaling whenever individuals from different plumage types pursue alternative strategies involving mutually fitnessenhancing interactions among strategy types. For example, in socially monogamous, territorial species, adult males with subadult neighbors can enhance their reproductive success through extra-pair fertilizations (EPFs) gained in the nests of subadult males (Morton et al. 1990; Perreault et al. 1997; Richardson and Burke 1999; Greene et al. 2000). Honest signals of subadult status could

Intraspecific Variation in Coloration

reveal a strategy wherein younger individuals concede EPFs to adult neighbors in exchange for reduced territorial aggression from them, thereby increasing the subadults’ potential to acquire high-quality territories, as has been specifically argued for Lazuli Buntings (Passerina amoena; Greene et al. 2000). Thus bimodal distributions of plumage variability within a sample of all individuals is expected, and unimodally distributed variability is expected within each strategy type. Lazuli Buntings contrast with this general expectation, however, because yearling plumage color overlaps considerably with adult plumage color (Figure 2.3b,c). However, this exception appears to support the general expectation of nonoverlapping signals between strategies, because yearlings with bright plumage appear to successfully pursue the strategy typically adopted by adults, whereas yearlings with dull plumage (which is never expressed in adults; Figure 2.3b,c) are also able to successfully rear offspring through apparent mutually fitness-enhancing collaborative alliances with adult neighbors (Greene et al. 2000). Signals of Breeding Strategy Individuals often pursue alternative strategies independent of age, status, or gender. An instance of honest strategy signaling occurs in White-throated Sparrows (Zonotrichia albicollis), in which adults use plumage color to advertise, independently of sex, a genetically determined variable breeding tactic: territorial versus parental (reviewed in Tuttle 2003). Breeding tactic in these sparrows is associated with a bimodal distribution in plumage color: tan individuals are more parental and white individuals are more territorial (Atkinson and Ralph 1980; Figure 2.4a). As predicted for such a signal of strategy, pairs who mate disassortatively by strategy do much better, strongly suggesting a benefit associated with revealing their reproductive strategy honestly (Falls and Kopachena 1994). Male Ruffs also have color-based signals of breeding strategy that are genetically determined (van Rhijn 1991; Lank et al. 1995). Resident males (~85% of males) form territories on leks and display to females. Satellite males (~15%) do not defend territories, but instead form cooperative alliances with resident males for mutual display. Many residents allow satellites on their territory, and both males gain copulations from females (van Rhijn 1991). On average, territories with both types of male are more attractive to females than territories with only resident males (Hugie and Lank 1997; Widemo 1998). By signaling their strategies reliably, males could gain fitness through facilitation

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Figure 2.4. Frequency distributions of plumage morphs in (a) White-throated Sparrows (redrawn from Atkinson and Ralph 1980), and (b) Ruffs (adapted from Lank and Dale 2001). Variation in plumage coloration in both species is bimodally distributed, as expected for mating strategy signals. White-throated Sparrow coloration may actually be more distinct between strategy types than is shown in this figure, as Atkinson and Ralph (1980) measured composite coloration in a variety of plumage traits. Plumage color in Ruffs was measured along a brightness scale, which correlates strongly with the variety of different colors found in a population.

of these mutually fitness-enhancing cooperative displays. Indeed, satellites do not look like residents (van Rhijn 1991). They typically have very white and uniform ruffs and very light head tufts, and this plumage type does not overlap to any appreciable degree with the diverse plumage types expressed by residents (van Rhjin 1991; Lank and Dale 2001; Figure 2.4b; Plate 7).

Compatibility Recently there has been considerable interest in the hypothesis that individuals actively choose mates with whom they are genetically most compatible (Tregenza and Wedell 2000; Freeman-Gallant et al. 2003; Servedio and Noor

Intraspecific Variation in Coloration

2003; Mays and Hill 2004). Bird coloration could function as signals for such genetic compatibility if it revealed variability in the relevant loci. Compatibility signals are genetically determined traits whose phenotype predicts whether an individual carries particular alleles at any loci for which there are various optimal genetic combinations in a population of potential mating partners. How does selection maintain positive correlations between genes related to signals and genes that have alleles that are differentially compatible? Selection for reliable signals of compatibility increases with (1) the potential for matings among incompatible genotypes, (2) any reduced opportunity for multiple mating by signalers (thereby reducing selection for signalers to cheat; Wedekind 1994), and (3) strong and ongoing selection against offspring from parents with incompatible genotypes at particular loci (Servedio and Noor 2003), because strong selection maintains high linkage disequilibrium between signal and compatibility alleles. Genetic Compatibility among Populations Color signals related to genetic compatibility might be expected most often during the reinforcement processes of speciation (Dobzhansky 1940; Marshall et al. 2002; Servedio and Noor 2003). When locally adapted populations, subspecies, or closely related sister species overlap in geographic distribution and any hybrid offspring have reduced fitness, selection can favor traits that inhibit interbreeding (Servedio and Noor 2003). Under such conditions, any individual choosing a mate when both genotypes (taxa) are available will face a bimodal distribution of genetic compatibility among potential partners. Signals of taxon identity are thus expected to have bimodal distributions wherever the taxa are sympatric. Reproductive character displacement is a signature of this reinforcement process (Howard 1993; Sætre et al. 1997; Servedio and Noor 2003). Such character displacement occurs when taxa demonstrate more differentiated characteristics in zones of sympatry than they do in zones of allopatry. Signals of taxon identity are therefore expected to demonstrate high geographic variability. Specifically, within taxa, color variability should be lower and more differentiated in sympatry (where it is under strong selection) than it is in allopatry (where it is under weak selection; Figure 2.5a). Taxon reinforcement of signals requires that there is (1) selection against hybrids, (2) character displacement in sympatric populations, and (3) assortative mating arising from character displacement in the zone of sympatry

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Figure 2.5. Plumage variability and reinforcement. (a) Expected properties of variation in plumage characteristics that function at decreasing hybridization between genetically distinct taxa. (b) Plumage coloration in Ficedula flycatchers mapped onto a molecular phylogeny (adapted from Sætre et al. 1997). Populations of Pied Flycatchers occurring in sympatry with Collared Flycatchers have recently diverged in plumage color, increasing the degree of assortative mating within each taxon.

(Sætre et al. 1997). Such conditions appear to occur in Ficedula flycatchers. In areas of sympatry, the closely related Collared (Ficedula albicollis; Plate 18) and Pied (F. hypoleuca; Plate 27, Volume 1) Flycatchers occasionally interbreed. However, hybrid offspring have considerably reduced fitness and, in sympatry, plumage coloration is much more differentiated than in allopatry (Figure 2.5b). Furthermore, females have displaced mate preferences for plumage coloration in areas of sympatry, which results in increased assortative mating (Sætre et al. 1997).

Intraspecific Variation in Coloration

Species Recognition When reinforcement processes lead to complete assortative mating between genetically differentiated populations (distinct enough such that no viable offspring are produced during hybridization), then the association between respective signal genes and each species’ genome can be considered fixed. In such situations, signal traits might function as species recognition signals: the ultimate compatibility signals. Historically, the concept of species recognition (Wallace 1889; Fisher 1930; Mayr 1963) has received widespread interest as an explanation for interspecific variability in bird coloration (Andersson 1994, McNaught and Owens 2002). However, to date there has been little empirical support for the idea that species recognition has been a strong selective force in the evolution of the broad patterns of avian coloration. McNaught and Owens (2002) tested the species recognition hypothesis using a comparative approach applied to plumage coloration in various Australian species. Contrary to predictions based on species recognition, they found no evidence that sympatric pairs of species were more divergent in coloration than allopatric pairs. McNaught and Owens (2002) concluded that the species isolation hypothesis may be best suited to explain plumage diversity only in very closely related sister taxa for which frequent hybridization is a current and strong possibility. If species recognition signals do exist in bird colors, what are their expected characteristics? Under the assumption that any signal variation away from the species’ mean value would be selected against through increased recognition errors by receivers (i.e., strong stabilizing selection), then signals of species identity are expected to be fixed, genetically determined traits that demonstrate low degrees of unimodally distributed variability. In addition, such signals need not be particularly conspicuous (or costly), as receivers will only be realistically required to differentiate among a limited number of species similar to themselves. Species identity signals are therefore unlikely to explain fully the most conspicuous secondary sex traits, such as highly ornamental coloration (Andersson 1994). Genetic Compatibility within Populations Mate choice that is sensitive to genetic compatibility is also expected to occur within populations. However, variable coloration probably provides a poor

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james dale medium for reliable signaling of intrapopulational genetic compatibility. First, there are no simple mechanisms to couple variability in color alleles with variability in compatibility alleles. Second, with respect to condition-dependent (i.e., costly) plumage coloration, compatibility signaling is unlikely because females cannot use the same color traits to select for mates with overall highquality genotypes as well as for individual-specific compatibility (Mays and Hill 2004). One of the most common forms of mate choice for compatibility within populations occurs when females favor partners who are compatible with respect to genetic parasite resistance (e.g., disassortative mating for major histocompatibility complex [MHC] allelic composition; Wedekind 1994; Freeman-Gallant et al. 2003). However, all of the empirical support for MHC-driven mate choice comes from olfactory cues (Egid and Brown 1994; Wedekind and Füri 1997; Tregenza and Wedell 2000). Olfactory cues can be tightly linked to MHC composition because polymorphic MHC loci can create detectable odors via the highly variable glycoproteins they encode by (1) breakdown of the glycoproteins themselves into small evaporating molecules, and/or (2) determination of the specificity of odor-causing bacterial flora that inhabit an individual (Wedekind 1994; Tregenza and Wedell 2000). In strong contrast, there is no intrinsic mechanism whereby variance in plumage alleles will be necessarily coupled to allelic composition of MHC loci. Therefore, unless there is particularly strong and ongoing selection against nonoptimal MHC combinations (which would maintain high linkage disequilibrium between signal and MHC alleles), color cues are an unreliable medium for broadcasting MHC genotypes. Another form of mate choice for compatibility within populations occurs when individuals prefer mates who have optimal degrees of overall genetic similarity (Bateson 1983; Tregenza and Wedell 2000; Mays and Hill 2004). A signal of overall genetic similarity must be based on multiple polymorphic loci scattered throughout the functional genome (e.g., see Dawkins 1982; Sherman 1991; Sherman et al. 1997). However, the reliability of such signals as predictors of compatibility alleles will eventually deteriorate as signal alleles become independent of alleles at other loci through genetic shuffling at meiotic recombination. At equilibrium, such signals can only reflect similarity with respect to the genetic basis to signal variability, not to the rest of the genome, and are therefore unstable. However, if individuals frequently encounter unfamiliar genetic relatives as potential mates (e.g., through limited dispersal in both sexes), then color variability can reliably signal (shared) genetic similar-

Intraspecific Variation in Coloration

ity. This reliability comes about because, even in distant relatives, recombination will not have had sufficient opportunity to break up linkage disequilibrium between signal alleles and other parts of the genome. In such cases, shared signal alleles between receivers and signalers will predict genetic similarity at many other loci shared through common descent (i.e., linkage disequilibrium is higher in kin; Dawkins 1982). However, such signals can be considered signals of kinship, which I discuss next.

Kinship Kin recognition in birds can often be accomplished via the learning of distinctive characteristics of likely genetic relatives that have been identified using other cues, such as positional information (e.g., a nestling’s presence in an adult’s nest can be a good predictor of kinship). An alternative form of kin recognition occurs, however, when individuals discriminate unfamiliar kin (Dawkins 1982; Sherman et al. 1997). Correctly recognizing unfamiliar kin could increase fitness if receivers behave altruistically to the signaler (Sherman et al. 1997; Petrie et al. 1999). In addition, recognition of unfamiliar kin could facilitate inbreeding avoidance by revealing degrees of overall genetic similarity resulting from shared genetic descent (Sherman et al. 1997; Tregenza and Wedell 2000; Blomqvist et al. 2002; see the section on compatibility above). Signals of kinship are expected to be variable, genetically determined phenotypes based on multiple polymorphic loci scattered throughout the functional genome (Dawkins 1982; Sherman 1991; Sherman et al. 1997). Receivers could gauge genetic similarity of unfamiliar signalers by comparing the signal to a cognitive template based on their own phenotypes or the phenotypes of known close relatives (Burley and Bartels 1990; Sherman et al. 1997). Signals of kinship should not be particularly costly or conspicuous, but variability needs to be high enough for receivers to easily discriminate phenotypic differences related to kinship. Recognition of unfamiliar kin may be of widespread importance in avian social interactions (Höglund et al. 1999; Petrie et al. 1999; Shorey et al. 2000; Bloomqvist et al. 2002). For example, Peacocks (Pavo cristatus) were found to preferentially lek with close relatives, even in the absence of social learning or environmental cues (Petrie et al. 1999). Presumably the Peacocks were choosing a lek to join based on some sort of phenotypic variation among males that they used to ascertain potential relatedness. It is unclear, however, whether the cues were color-based or based on another signaling modality, such as sound.

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In Zebra Finches (Taeniopygia guttata), variability in plumage coloration provides a promising candidate for a visually based signal of kinship. Unfamiliar individuals were found to preferentially associate with relatives (Burley et al. 1990), and it appears as though they could use plumage cues, at least in part, to do so (Burley and Bartels 1990). Zebra Finch plumage is characterized by a variety of high contrasting lines and banding, the variability of which appears to be genetically determined (Burley and Bartels 1990). Plumage variability in Zebra Finches might therefore provide suitable variability for kin recognition, as has similarly been proposed for variability in chimpanzee and human facial features (Parr and de Wall 1990; DeBruine 2004).

Individual Identity The use of color variability for individual recognition appears to be widespread. When individuals interact repeatedly, selection can favor the production of identity cues that facilitate individual recognition (Beecher 1989; Johnstone 1997b; Dale et al. 2001). The defining property of a signal of identity (and the difference between an identity signal and a kinship signal) is that the receiver’s recognition template (Sherman et al. 1997) is based on the phenotype of the individual signaler. Once learned by receivers, signals of identity can be coupled with additional information, such as territorial residency (neighborstranger or “dear enemy” recognition; Wilson 1975), reliability in altruistic interactions (i.e., reputations; Nowak and Sigmund 1998), dominance (Barnard and Burk 1979), mate identity, or kin identity (see Whitfield 1987; Dale et al. 2001 for reviews).

Properties of Identity Signals In identity signaling, rare morphs are at a selective advantage because rare varieties are assumed to be more easily recognized than common varieties (i.e., less likely to be confused with other individuals). This negative frequencydependent selection increases phenotypic variability, and so identity signals are expected to be highly variable. Dale et al. (2001) developed the idea of negative frequency-dependence on identity signals to make specific predictions regarding the expected properties of such traits. In addition to expressing relatively high variability, identity signals are expected to express five other properties. First, they should have polymodal frequency distributions, because

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negative frequency-dependent selection is well known to maintain phenotypic variability and polymorphisms (Maynard Smith 1982). Second, they should be relatively cheap and not condition dependent, because phenotypes that are distinct but cheap will spread to a higher equilibrium frequency. Third, different signal variants should have equal fitness at equilibrium, because rare phenotypes will spread until all traits have equal fitness. Fourth, they should exhibit an independent assortment of component characters (Beecher 1982; Dale et al. 2001), because correlated traits have a reduced potential for being distinct. Finally, they should occur as fixed phenotypes with high degrees of genetic determination, because receivers can force reliable identity signaling by using inflexible characters for their recognition decisions (which tend toward strong genetic determination). Moreover, if polymorphic loci for signaling traits are located on separate chromosomes, then the theoretically favored low correlations between component traits will be automatically generated by independent assortment of chromosomes at meiosis (Dale et al. 2001). Candidate Identity Signals Plumage coloration in Red-billed Queleas (Quelea quelea) provides a promising candidate for a visually based signal of individual identity in birds (Dale 2000, 2001; Dale et al. 2001). The ornamental breeding plumage coloration of male queleas is remarkably variable (Ward 1966; Plate 6). It has the following properties consistent with identity signaling: (1) high variability; (2) complex frequency distributions, at least for some traits; (3) independent assortment of component characters; (4) no condition dependence; (5) no relation to reproductive success; and (6) no age/experience-related variation. In queleas, males breeding in colonies live in a social environment where being recognizable is likely critical—because cohesive social groups (neighborhoods of nesting males) frequently interact within a huge assemblage of unfamiliar individuals (Crook 1960; Dale 2001). Ruffs have the most variably colorful breeding plumages of any wild bird (van Rhijn 1991; Lank and Dale 2001; Plate 7). Lekking Ruffs are highly territorial, have frequent agonistic interactions with other males, and do not vocalize. Individual recognition between males on leks is obvious (van Rhjin 1991). In the absence of vocal communication, the only likely available recognition cue for Ruffs is plumage variability (Lank and Dale 2001). As in queleas, properties of plumage variability in Ruffs conform well to the expected properties of identity signals (Dale et al. 2001).

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Box 2.3. Testing Identity Signaling An important but inconclusive test of identity signaling is that color is used for recognition decisions. Because selection can favor receivers that recognize individuals independently of whether signalers benefit from being recognized ( Johnstone 1997b; Dale et al. 2001), the demonstration that coloration is used in recognition processes (e.g., Whitfield 1986; also see Tibbetts 2002) does not provide conclusive evidence that the phenotype of the signaler evolved to signal identity. The critical test centers around the fundamental assumption of the identity-signaling hypothesis—individuals who have rare signal phenotypes (more recognizable) must experience a selective advantage over those who have the most common signal phenotypes (and thus are less recognizable individually). To my knowledge, such a selective advantage has yet to be shown for any putative identity signal in any communication medium in any taxon. Attempts to demonstrate the benefits associated with recognizability should thus be an important focus for future studies of individual recognition. Indirect evidence suggests that such benefits might be widespread (Watt 1986; Rohwer and Røskaft 1989; also see Höjesjö et al. 1998). For example, Watt (1986) argued that decreased aggression observed among more variably plumaged groups of Harris’ Sparrows (Zonotrichia querula) was consistent with the hypothesis that increased individual recognition within groups facilitated the formation of stable dominance hierarchies. Furthermore, Rohwer and Røskaft (1989) speculated that Yellow-headed Blackbirds (Xanthocephalus xanthocephalus) with manipulated plumage (Plate 10) were better at maintaining their territories than unmanipulated birds, because they were more easily remembered by rivals as good fighters. Comparative studies offer great potential to provide insight into identity signaling. Early work on begging by swallow nestlings demonstrated the potential power of such an approach (Medvin et al. 1993). In swallows (Hirundinidae), variability in nestling calls is higher in species that nest in large colonies where parents could potentially confuse their own offspring with the many other nestlings in the colony (Medvin et al. 1993; also see Leonard et al. 1997). Furthermore, egg color variability tends to be higher in species with high degrees of brood parasitism, indicating strongly that variability

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can be increased through selection favoring traits that improve a female’s ability to discriminate her own eggs from foreign eggs (Soler and Møller 1996). Whitfield (1987) pointed out how a general comparative approach needs to be applied to avian plumage color variability and individual recognition. Almost 20 years later, this is still the case.

Falconiformes (e.g., hawks and falcons) are among the most variably colored orders of birds (Rohwer and Paulson 1987; Galeotti et al. 2003). Many species are highly territorial, staking large open territories over their hunting grounds, and visual signals of identity could function to reduce needless aggression among neighboring residents and also facilitate mate and kin recognition. Indeed, individual recognition is obvious in diurnal raptors, even at great distances (Tinbergen 1958). Plumage variability in raptors appears, in general, to be strongly genetically determined, typically melanin-based (i.e., presumably cheap), and often multimodal (Rohwer and Paulson 1987)—patterns consistent with identity signaling. Individual identity signaling has not been considered for color variability in raptors, despite a relatively large amount of research devoted to resolving its function. If plumage in birds of prey evolved primarily to facilitate individual recognition, then variability should correlate positively with increased territorial interactions, increased frequency of visual contact among individuals, and increased territory size. In species with sexual differences in the degree of color variability (Fowlie and Kruger 2003), the sex involved in territorial defense is expected to be more variable. Additional identity signaling systems include highly variable plumage coloration in Ruddy Turnstones (Arenaria interpres). In his pioneering study, Whitfield (1986) demonstrated that turnstone color variation is used for neighbor-stranger recognition (but see Box 2.3). Nestling Cliff Swallows (Petrochelidon pyrrhonota) have highly variable plumage patterns on their heads (Plate 9) that parents may use to identify their offspring in fledgling flocks (Stoddard and Beecher 1983). Similarly, nestling color in Royal Terns (Sterna maxima; Buckley and Buckley 1970), and Red-legged Shags (Phalacrocorax guimardi; Rasmussen 1988) is also quite variable and has been argued to be associated with the need for parents to identify young from large non-kin groups of nestlings. In Royal Terns, the observed frequency distributions of nestling coloration in a large sample of chicks offer strong support for the expected

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Figure 2.6. Frequency distributions of color traits in Royal Tern chicks (n = 400) demonstrate complex patterns, as expected for identity signals. Adapted from Buckley and Buckley (1970).

complex frequency distributions for identity signals (Figure 2.6). In addition, most of these variable traits in Royal Tern chicks vary independently of one another, thereby maximizing the number of color combinations and overall individuality of each nestling’s appearance (Buckley and Buckley 1970). Egg coloration is also often remarkably variable, and such variability may function in identity signaling, an idea that stands in contrast with the recently developed hypothesis positing a quality signaling role for egg coloration (Moreno and Osorno 2003). For example, in Common Murres (Uria aalge), the background color of eggs varies from white to deep blue, with a foreground of variably colored spots, splotches, and streaks (Plate 8). Murres nest in dense colonies, and eggs can get jostled away from nesting positions. Tschantz (1959) demonstrated that murre parents use egg coloration to discriminate their own eggs from those of neighbors. Egg coloration in murres appears to demonstrate the expected properties for identity signals. In particular, color saturation is

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Figure 2.7. Variability in the background (not spot or blotch) coloration of Common Murre eggs (n = 85) at a breeding colony on Triangle Island, British Columbia (J. Dale, unpubl. data, with color scored as in McGraw et al. 2003). (a) As egg color saturation approaches zero, hue becomes less meaningful as a measure of perceivable variability and hence becomes more variable (see Box 2.2). (b) Frequency distribution of background color saturation demonstrates an overall flat, possibly polymodal, pattern, as expected for identity signals.

highly variable among eggs, and the frequency distribution of saturation is remarkably uniform across the range of expression (Figure 2.7).

Presence One of the most important bits of information that individuals can signal about themselves is their presence—their immediate occupation of a particular

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location. Bright coloration makes an individual more conspicuous. Revealing presence can be crucial. For example, breeding males need to be easily located by females prior to courtship. In contrast, dull or cryptic coloration makes individuals less conspicuous. Concealing presence can also be crucial, for example, to avoid detection by predators or prey. Conspicuous and cryptic coloration are thus extremes of a range of color detectability (Endler 1988). Honest Signals of Presence Reliable signals of presence should contrast strongly with the ambient light environment (Endler 1990) and be tailored to the sensory biases of the intended receivers (Rowe and Skelhorn 2004). Sensory exploitation or sensory bias (Endler and Basolo 1998) hypotheses to explain male breeding displays argue that displays increase mating success through an increased stimulation of the female sensory system. Certain colors or patterns could thus function to make a male’s phenotype more obvious to potential mates. If a color pattern is selected to reveal only presence, what are the expected properties of such a signal? Under the assumption that strong stabilizing selection drives such signals to fixation, then presence signals should demonstrate relatively low variability, display unimodal distributions, be cheap to produce (or, more specifically, not be differentially costly), develop in a way that is not environmentally dependent, and express a high degree of genetic determination with low degrees of heritability (i.e., low degrees of genetic diversity). Signals of presence should contrast strongly with ambient background conditions and should be conspicuous to the particular receivers whose behavioral responses benefit the signaler. Presence signaling can easily give rise to sexual dichromatism. In bustards (Otididae) and plovers (Charadriidae), males tend to have more black coloration in species for which males include acrobatic aerial components to their breeding displays (Dale 1992; Bókony et al. 2003; Figure 2.8). Dark plumage contrasts strongly with the sky (Walsberg 1982) and could benefit males by making them more visible during display and therefore more easily located by females. Presence signaling can also have benefits outside mate attraction. For example, Greater Honeyguides (Indicator indicator) have conspicuous white outer tail feathers that they flash repeatedly during displays designed to encourage humans to follow them to honeybee colonies (Isack and Reyer 1989). Killdeers (Charadrius vociferus; Plate 6, Volume 1) have orange rumps that they

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Figure 2.8. Male melanization (percentage of frontal body region that is black) and melanin dichromatism [log (male melanization +1) – log (female melanization + 1)] in bustards (Dale 1992; J. Dale and J. Joy, unpubl. ms) and plovers (Bókony et al. 2003) as a function of male display type. Box plots show medians; 10th, 25th, 75th, and 90th percentiles; and all outlying data points. Data plotted are species values (bustards, n = 23; plovers, n = 45). In both groups, phylogenetically controlled analyses demonstrate that aerial displayers tend to be significantly more black than ground displayers.

flash to predators during distraction displays that lure predators away from their ground nests (Jackson and Jackson 2000). The bright yellow feet of Snowy Egrets (Egretta thula) are proposed to startle aquatic prey in murky pools (Parsons and Master 2000).

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Aposematic coloration patterns are also conspicuous signals directed toward potential predators (receivers) and coupled to information about aspects of prey (signaler) unprofitability, such as toxicity (Dumbacher et al. 1992), unpalatability (Cott and Benson 1970), or alertness (also see Lyon and Montgomerie 1985; Endler 1988; Andersson 1994). Aposematic colors should be distinctive to receivers, so that they are easily remembered, and should contrast strongly with the background (Endler 1988). Cryptic Coloration Cryptic color patterns are “dishonest signals of presence.” Signalers benefit from concealing their presence by minimizing their contrast with the surrounding habitat (Endler 1988; Chapter 1). The signal is deceitful because receivers suffer fitness costs as a result of the deception. Thus receivers will be under strong selection to discriminate these deceitful signals, and arms races are expected between increasingly cryptic signalers and increasingly perceptive receivers. Cryptic signals are expected to express similar properties as honest (i.e., conspicuous) signals of presence, except they should be difficult to detect. Because cryptic coloration often involves contrasting bands, patterns, and spotting typically involving a variety of earth-tone colors, such coloration should generally be more complex and variable than coloration designed to make signalers more obvious. Overall complexity (and variability) of cryptic coloration is thus expected to co-vary with the degree of heterogeneity of the usual background (Endler 1988). When a single species occupies different habitats with different backgrounds, cryptic coloration should vary across those habitats, such that contrast is minimized optimally across the different landscapes (Endler 1988). Thus increased intraspecific variability in cryptic coloration can occur when (1) there are seasonal changes in the habitat’s ambient conditions, (2) there are different ambient conditions at breeding and nonbreeding locations, or (3) the occupied habitat is naturally variable. The first two conditions increase interclass variability (i.e., seasonal variability) whereas the latter condition increases intraclass variability. Because background conditions can undergo dramatic seasonal changes, cryptic coloration is expected to track those changes. For example, Rock Ptarmigan (Lagopus muta) maintain residency throughout the year in the

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high arctic. During winter, when their world is a snowscape, ptarmigan are a uniform brilliant white. During summer, when the habitat is earth-tone, ptarmigan molt to a mottled, cryptic brown (Plate 19, Volume 1). Interestingly, males maintain their white winter plumage during early summer, despite the dangers of increased predation, possibly because white plumage may increase a male’s ability to attract females (Montgomerie et al. 2001). After males acquire mates, however, they smear dirt into their plumage to make it less conspicuous (Montgomerie et al. 2001; Chapter 9, Volume 1). Thus males actively manipulate their plumage from an honest to dishonest signal of presence. Birds often migrate to breeding and nonbreeding locations that vary dramatically in their backgrounds, and cryptic signaling is expected to co-vary with those changes. For example, in summer, Marbled Murrelets (Brachyramphus marmoratus) have a cryptic brown plumage that conceals their presence on the tree limbs on which they nest. In contrast, wintering murrelets live an entirely pelagic lifestyle, and in this environment, they display typical light below and dark above countershading commonly observed in oceandwelling birds (Nelson 1997). Such patterns are generally argued to conceal the birds to prey below and from predators above (Ruxton et al. 2004; Chapter 1). When a species occupies habitats with natural background variability, then cryptic coloration is expected to be polymorphic (i.e., the occurrence in one population of two or more sharply distinct and genetically determined forms; Huxley 1955). In the first comprehensive comparative survey of polymorphism of birds, Galeotti et al. (2003) found that polymorphic species (estimated to be 3.5% of all species) tended to be active during both day and night and tended to occupy multiple and/or semi-open habitats. They concluded that these patterns suggest that avian plumage polymorphism probably evolved under selective pressures related to bird detectability, as affected by variable backgrounds (although it is important to keep in mind that other signaling functions, such as conveying strategy or individual identity, can also give rise to polymorphisms). In Arctic Terns (Sterna paradisaea), for example, chicks are either gray or brown (Lemmetyinen et al. 1974), and this polymorphism appears to be maintained by the mosaic-like nature of their nesting environment. In areas dominated by gray rocks and sparse vegetation, gray chicks are more frequent, whereas in areas with more brownish soil and denser vegetation, brown chicks predominate.

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Apostatic Selection The avoidance image hypothesis (Paulson 1973; Rohwer and Paulson 1987) is a form of dishonest presence signaling that occurs independently of ambient backgrounds and is specifically based on receiver psychology. The hypothesis posits that receivers (prey or predators) form search images based on the most common phenotypes of the signalers (predators or prey, respectively). Rare signaler phenotypes can therefore be at a selective advantage, provided they are less likely to be recognized. The apostatic hypothesis has been developed with particular attention toward explaining high degrees of color variability in raptors (Paulson 1973; Rohwer and Paulson 1987). Alternatively, however, individual identity signaling could explain raptor plumage diversity (see the section on identity above). It is interesting to note that the two hypotheses are reversed versions of one another. In identity signaling, rare morphs benefit due to increased recognizability to conspecifics. In avoidance image signaling, rare morphs benefit due to decreased recognizability as a threat to prey. Although the assumptions regarding receiver psychology are completely different between the two hypotheses, the outcome of the two processes are the same and are expected to result in highly similar signal properties. That is, apostatic selection is negatively frequency-dependent (Rohwer and Paulson 1987; Endler 1988) and is thus expected to result in high degrees of genetically determined color variability that demonstrate complex frequency distributions (e.g., see Dale et al. 2001). Apostatic selection is not expected to result in increased interclass variability, such as sexual dichromatism (Fowlie and Kruger 2003). Although apostatic selection has been demonstrated to be a potentially important process with Blue Jays (Cyanocitta cristata) hunting virtual insect prey (Bond and Kamil 2002), the hypothesis has generally been argued to be an unlikely selective force driving increased variability in bird coloration (Preston 1980; Fowlie and Kruger 2003; Galeotti et al. 2003; but see Roulin and Wink 2004). One of the key predictions of apostatic selection is that polymorphic raptors should prey upon more intelligent prey, such as birds and mammals, because these prey are argued to be more likely to form search images of predators that they have previously encountered (Paulson 1973; Roulin and Wink 2004). However, intelligent prey should arguably be less likely fooled by alternative plumage patterns in raptors when other cues are readily available for identifying unfamiliar predators. For example, prey should be strongly selected

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to base their recognition template of predators on more reliable cues, such as a silhouette (Preston 1980; Galeotti et al. 2003). In my view, due to strong territorial behavior in birds of prey, individual identity signaling represents a promising and hitherto unexplored hypothesis to explain their remarkable plumage diversity.

Discussion I have restricted the hypotheses covered in this synthesis to signaling functions related to color variability. However, alternative nonsignaling functions are also critically important for understanding bird colors. For example, thermoregulation (Burtt 1981), mechanical benefits of pigmentation (Butler and Johnson 2004), and protection from bacterial degradation (Goldstein et al. 2004), solar UV radiation (Ward et al. 2002), and glare (Burtt 1984) are all important hypotheses (see Chapter 1). Because adaptive nonsignaling coloration will generally be under strong stabilizing natural selection, it is expected to be genetically fixed and express low degrees of phenotypic variability. Interclass variability (see Box 2.1) in coloration with nonsignaling functions is also expected to be reduced, although some hypotheses, such as thermoregulation, do predict geographical clines of variation (Galeotti et al. 2003). Variability in coloration can also have no function, resulting simply from mutations that are not influenced by selection (Kimura 1962, 1983). Indeed, one of the most obviously variably colored birds, the Snow Goose (Chen caerulescens), appears to have plumage variability not associated with any function (Cooke et al. 1995). Despite long-term observations and massive datasets, Snow Goose researchers have failed to find any fitness correlates with this highly conspicuous variability. Plumage variation is instead argued to be the result of different morphs evolving in allopatry, followed by a recent secondary introgression (Cooke et al. 1995; Lank 2002). The neutral hypothesis can clearly be highly relevant for understanding large-scale plumage variability, although Snow Geese represent the only well-developed case study so far. To refute the null hypothesis that plumage variability is not related to a communication function, the demonstration of fitness benefits associated with signaling is required (e.g., see Box 2.3). Additional evidence that can support the hypothesis that color displays have evolved as signals include (1) a trait has apparent signal design (e.g., if it is highly conspicuous, sexually dimorphic, or behaviorally enhanced during social interactions), (2) variability

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in coloration influences behavior in receivers (e.g., Whitfield 1986), or (3) an interspecific association occurs between color variability and the socioecological variables that are expected to relate to signaling (e.g., Galeotti et al. 2003). Nonmutually Exclusive Hypotheses The different dimensions of information revealed through plumage coloration (see Table 2.2) represent alternative explanations for variability. These hypotheses are not mutually exclusive, because any variability in coloration could potentially reveal multiple aspects of information about an individual to multiple receivers. Color patterns could therefore be compromises of various signaling functions (Endler 1988). For example, a sexually dimorphic color trait could have been shaped by selection through cumulative benefits associated with revealing quality, attractiveness, strategy, and presence. Alternatively, different color traits within an individual could reveal completely different information. Consider breeding male Red-billed Queleas, which have two separate color-based signaling systems: (1) complex and independently assorting variability in various plumage features reveals individual identity, whereas (2) unimodally distributed coloration in bare parts (bill, leg, and eye-ring) reveals quality (Shawcross and Slater 1983; Dale 2001; Figure 2.9). In the Ruff, males reveal at least three separate types of information about themselves with different color-based traits: (1) bimodally distributed plumage patterns reveal male strategy; (2) additional complex plumage variability within each strategy type reveals individual identity; and (3) facial wattle area (number of caruncles), which is age-dependent, presumably reflects quality (Dale et al. 2001; Lank and Dale 2001). Multiple Ornaments Currently there is widespread interest in why birds have multiple ornaments (Møller and Pomiankowski 1993; Johnstone 1996; Candolin 2003). The basic theoretical framework is centered around three hypotheses developed in a groundbreaking paper by Møller and Pomiankowski (1993): (1) multiple messages, (2) redundant messages, and (3) unreliable signals. These hypotheses essentially reduce the problem of multiple ornaments to only one kind of information: quality. The multiple messages hypothesis argues that the information content of the two traits reflect different aspects of quality. The redundant messages hypothesis argues that the information content of each trait

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Figure. 2.9. Dual signaling system of male Red-billed Queleas. Unimodally distributed bill hue (n = 324) signals quality, whereas bimodally distributed plumage hue (n = 897) signals individual identity. Color scores measured using methodology described in Dale (2000). Adapted from data in Dale (2000, 2001).

reveals similar aspects of quality. For receivers to be selected to favor redundant messages, the increased reliability of information provided by traits in combination must be high enough to offset the additional costs to receivers associated with processing multiple signals (Johnstone 1996). Finally, the unreliable signals hypothesis argues that ornaments do not reveal quality and are the product of, for example, separate instances of Fisherian runaway selection occurring independently on separate traits. To understand the origin of multiple ornaments, we need to understand all the potential information types revealed by traits (see Table 2.1), not just quality (Candolin 2003). Furthermore, we require an understanding of how different information types interact, overlap, and trade off with one another (Johnstone 1996; Candolin 2003) and who the intended receivers are for different signals (see Andersson et al. 2002). Resolving the different functions of multiple ornaments in birds is an exciting avenue for future research.

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By evaluating the properties of different traits within a species (see Table 2.2), we can gain insights into the diverse messages revealed by them (e.g., see Figure 2.9). Multiple messages are likely the norm in birds, and this will especially be true when all potential types of information revealed by color-based signals are considered, as well as additional “ornamental” phenotypes, such as song, smell, and behavioral display.

Conclusions At the beginning of this chapter, I asked why American Crows are so uniform and Ruffs are so diverse. With Ruffs, plumage likely signals multiple messages, including strategy, individual identity, and quality. With crows, I can only hazard some speculative guesses. Assuming that there is a signaling function to crow blackness, then crow plumage has the basic properties expected for signals that function as (1) amplifiers, (2) species identifiers, and (3) indicators of presence. First, crows could use UV coloration to signal quality. Indeed on close inspection, adults have a violet-blue gloss on the body and a greenishblue gloss on the wings. Therefore crows might not be so uniform, after all. However, putatively variable UV-signaling in crows still begs the question of the reason for the uniform blackness that underlies it. One possibility is that crow blackness functions as an amplifier to the UV signals. Second, low variability in crow blackness could function as a signal of species identity. However, it is unlikely that blackness signals species identity with respect to mate choice, because other species of sympatric and closely related corvids (e.g., Fish Crows [Corvus ossifragus]) are also completely black. Finally, crow blackness could function as a signal of presence to facilitate flocking or alternatively, to advertise territorial occupancy. Indeed, crows are known to form massive flocks during winter and at roosts (Verbeek and Caffrey 2002). Black coloration contrasts strongly against most natural backgrounds, including the sky (Walsberg 1982), so both perching and flying crows are highly visible, even at great distances. That crows are such noisy creatures does indeed suggest that selection has favored conspicuousness in this species. The problem of crow blackness illustrates a final point that is often overlooked. High variability in plumage coloration may be easier to explain than low variability. A challenge for future studies of plumage coloration is to explain why so many species are (apparently) so uniform. Moreover, what exactly is the distribution of color variability across different species? The question of why there is such high “variability in color variability” remains open for fu-

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ture studies of avian coloration. Indeed, the nature of intraspecific variability in all signaling media in all organisms is a rather poorly understood aspect of communication.

Summary There are considerable differences among bird species in the degree of color variation within populations. In some species, there appears to be little difference among individuals, whereas in other species, each individual seems to be unique. Why is there so much interspecific variation in within-species variability? Here I have argued that general patterns of intraspecific variation can be understood from a communication-based theoretical framework in which signalers reveal information about themselves to receivers. Birds use color to reveal seven broad kinds of information—quality, Fisherian attractiveness, behavioral strategy, genetic compatibility, kinship, individual identity, and presence. Quality signals reveal information about relative phenotypic and genetic constitution and are expected to express relatively high degrees of unimodally distributed, environmentally determined (condition-dependent) variability. In addition, quality signals can be associated with “amplifiers,” traits that increase the receiver’s perception of ornament elaboration. In contrast to quality signals, amplifiers are expected to be fixed and express low variability. Fisherian runaway selection results in traits that define attractiveness independent of quality. Fisherian traits are expected to be intense colors that demonstrate relatively low intrapopulation variability and high geographic variability (provided that different populations arrive at different equilibrium states). Strategy signals are expected when individuals form strategy-dependent cooperative alliances and include signals of gender, some forms of delayedplumage maturation, and signals of mating strategy. Strategy signals are expected to be bimodally distributed (one mode for each strategy) and can be genetically or environmentally determined, depending on the specific strategies revealed. Traits that reflect genetic compatibility for mate choice include species isolation signals and signals of genetic similarity. Species isolation processes (reinforcement and species recognition) provide the most promising scenarios in which to find color-based compatibility signals. Such signals are expected to be genetically fixed traits that express low variability within genetically distinct populations and high variability between them.

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Kinship signals facilitate discrimination of unfamiliar kin and can be stable for color-based signals, provided that signalers frequently encounter and interact with unfamiliar relatives. Such signals are expected to be based on multiple, variable, and independently assorting traits based on polymorphic loci scattered throughout the genome. Individual identity signals are “name tags” that increase overall recognizability. Signaling individual identity by color display might be widespread in birds and appears to be associated with the highest degrees of observed variability in coloration. Identity signals often display complex, multimodal distributions presumably arising from negative frequency-dependent selection acting on signal phenotypes. They are expected to express similar properties as kinship signals; however, identity signals are only used to discriminate familiar individuals (i.e., the signal must be learned by receivers). Finally, signals of presence either reveal (honest signals) or conceal (dishonest signals) an individual to receivers. Such signals should contrast (or blend) with the ambient environmental conditions and generally be fixed traits that express low degrees of unimodal variability. However, variable background conditions can easily give rise to increased phenotypic variability, particularly with cryptic coloration. These seven signal types represent non-mutually exclusive alternative communication functions for bird coloration and provide a rich arena for the provision of multiple messages by signalers. Furthermore, the framework developed here is expected to be general and should provide insight into signaling in all communication channels in all taxa.

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3 Color Displays as Intrasexual Signals of Aggression and Dominance juan carlos senar

Darwin (1871) proposed two modes of sexual selection: direct competition between individuals of the same sex (intrasexual selection) and mate choice (intersexual selection). Within both contexts, secondary sexual characters can function as signals of individual quality (Bradbury and Davies 1987; Andersson 1994; Berglund et al. 1996). In this chapter, I review and summarize studies of intrasexual signaling in birds, in which plumage and bare-part color is used to signal the fighting ability of individuals. Recently it has been stressed that sexual and natural selection are not the only selective forces shaping animal signals, but that social selection, in which the signal influences the fitness of signalers and receivers within a social context, can also shape signal evolution (Tanaka 1996; Wolf et al. 1999). The selective pressures that shape signals of fighting ability are probably similar whether or not they have evolved by sexual or social selection. The major advantage of these signals, independent of their origin, is that individuals of unequal fighting ability can gauge the status of rival competitors (e.g., for mates, food, territories) from their agonistic signals without having to fight over the resource and risk energy depletion, injury, or death (Rohwer 1975, 1982). There are differences, however, in the expected outcomes of sexual and social selection. The function of signals that evolved by sexual selection is to drive off rivals, but this should not be the aim of signals that evolved by social selection.

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Driving off rivals would lead to group disruption and, in social species, would be potentially costly for both contestants. In social species, therefore, the goal is to signal dominance rank in the group (Senar et al. 1989; Senar 1990). Most theoretical developments and empirical work in this area of behavioral ecology have focused on these signals from the view of “status signaling” and hence from the social perspective (Maynard Smith and Harper 2003). This focus is because communication in social species presents more evolutionary problems but also more complex and interesting patterns than in nonsocial species or when the motivation is only sexual (Rhijn 1980; Rhijn and Vodegel 1980; Rohwer 1982; Maynard Smith 1982a,b; Maynard Smith and Harper 2003). Hence I have outlined this chapter from this status-signaling perspective, but I also provide examples of signals with sexual motivations. Superior fighting ability is the most common type of information provided by elaborate color patches in the context of intrasexual signaling, but color displays can serve other functions, such as signaling youth or low competitive ability (in the context of delayed plumage maturation; Selander 1965; Rohwer 1978a; Plate 13). Bright colors can also function to attract conspecifics to feeding patches, which can increase the size of flocks and hence the likelihood of detecting predators (Beauchamp and Heeb 2001). These topics will be reviewed at the end of the chapter.

Signaling Fighting Ability or Identity? The first studies on the role of bird colors as social signals of fighting ability were conducted by Rohwer (1975, 1977, 1978b). In an attempt to explain the great variation in size and extent of color patches in the plumage of wintering birds, he proposed that colored patches could serve as badges of social status. Rohwer’s work led to a controversy regarding whether the colored patches of feathers in flocking birds in winter had evolved for status signaling or simply for individual recognition (Shields 1977; Rohwer 1978b). Whitfield (1987a) reviewed the topic and concluded that, in some species and especially those forming small and stable flocks, individual recognition was sufficient to explain plumage displays (Whitfield 1986; Ens and Goss-Custard 1986; Watt 1986a; Rohwer and Røskaft 1989). In other species, however, the correlation found between plumage badges and dominance (Table 3.1) and the results of experiments (Watt 1986a,b) strongly suggested that such patches of color had evolved as true signals of status.

Color Displays as Intrasexual Signals of Aggression and Dominance

Status Signals or Simply Correlates of Dominance? When success in agonistic encounters is related to plumage traits (Table 3.1), it suggests that plumage color displays can serve as signals of social status (Figure 3.1). It has been widely recognized, however, that a correlation between a plumage trait and dominance is not by itself evidence for signaling—individuals could assess their social status by other means, and plumage could simply be a correlated trait rather than a signal (e.g., Roper 1986; Jones 1990; Slotow et al. 1993; Figure 3.1). Three different approaches have been used to test for a signaling function of plumage traits (Table 3.2). In most experiments, a plumage trait is manipulated and the experimental individual introduced into a group to test for gains or reductions in social rank (Table 3.2; Figure 3.2). Alternatively, in territorial species, the manipulated bird is released into the wild and its behavior recorded (Figure 3.3). This experimental approach has produced mixed results, especially in cases of social species, probably because there are many different confounding variables that need to be taken into account. In the earliest such experiments (Rohwer 1977; Rohwer and Rohwer 1978), for instance, manipulated birds were reintroduced into existing social groups, so that either the experimental birds were known to flockmates as subordinate (Ketterson 1979) or they withdrew from recognized dominant flockmates (Shields 1977; Ketterson 1979). Alternatively if the manipulation prevented any recognition of flock companions, the experimental birds might have been disadvantaged just because of a prior-residence advantage by the birds in the group (Fugle et al. 1984; Järvi et al. 1987b; and see below). To avoid these problems, more recent experimental approaches have exposed manipulated birds to unfamiliar conspecifics in neutral cages (e.g., Järvi et al. 1987b; Lemel and Wallin 1993; McGraw and Hill 2000a), or the plumage of both dominants and subordinates has been manipulated (e.g., Grasso et al. 1996). However, the introduction of a manipulated bird into a group is not the best way to uncover the signal content of a trait, because, although the trait may function as a signal, there may also be mechanisms by which individuals detect cheaters. For instance, if a bird with an enlarged badge of dominance does not defeat presumed dominant flock companions (e.g., Rohwer 1977; Rohwer and Rohwer 1978; Järvi et al. 1987b; Møller 1987a), it does not mean that the trait is not a signal. Mechanisms to avoid cheating, such as assessing not only the trait but also behavior, may be operating (see below).

89

Carotenoid? Melanin Structural Melanin

Size Size Size Color

Scarlet pectoral tuft Brown streaking in breast White frontal patch Black cap and bib

Carotenoid+melanin

Color/size

Red throat patch

Carotenoid+melanin

Size

Carotenoid+melanin

Melanin

Color

Size

Structural Melanin

Size Size

Carotenoid

Mixed

Color

Size

Yellow-headed Blackbird (Xanthocephalus xanthocephalus) Red-shouldered Widowbird (Euplectes axillaris) Red-collared Widowbird (E. ardens) Scarlet-tutfed Malachite Sunbird (Nectarinia johnstoni) Yellow Warbler (Dendroica petechia) Collared Flycatcher (Ficedula albicollis) Black-capped Chickadee (Poecile atricapilla)

Melanin

Plumage type

Size

Traita

Yellow on head and breast Red epaulets

Black/white contrast on head General body surface White underpart Black lateral breast band Area of chestnut lower breast Red epaulets

Nature of plumage variability

African Penguin (Spheniscus demersus) Ring-necked Pheasant (Phasianus colchicus) Least Auklet (Aethia pusilla) Kentish Plover (Charadrius alexandrinus) White-throated Dipper (Cinclus cinclus) Red-winged Blackbird (Agelaius phoeniceus)

Species

Table 3.1. Relationship between Plumage Color and Dominance

No

Yes

Yes

Yes

Yes

Yes

Yes

No

Yes Yes

Yes

No

Manipulation

94

93

75

Fights won (%)b

Mennill et al. (2003)

Pärt and Qvarnström (1997)

Studd and Robertson (1985b)

Evans and Hatchwell (1992)

Pryke et al. (2001); Pryke et al. (2002)

Pryke and Andersson (2003)

Peek (1972); Smith (1972); Røskaft and Rohwer (1987); Eckert and Weatherhead (1987) Rohwer and Røskaft (1989)

Bryant and Newton (1994)

Jones (1990) Lendvai et al. (2004)

Mateos and Carranza (1997)

Ryan et al. (1987)

Reference

Melanin Melanin

Size Size

Carotenoid Melanin Structural Melanin Melanin

Color Size Size Size Size

Red on general body Blackness of head and bib White in tail Blackness of head and bib Black/white on head

Melanin

Size

Black bib

Yes

No Yes

No

Yes

No

Yes Yes

No

Yes Yes Yes No Yes

Yes

87–96

72 75

69

r 2 = 50–70 rs2 = 27–79

r 2 = 92–96

r 2 = 74

Parsons and Baptista (1980); Fugle et al. (1984)

Balph et al. (1979) Rohwer (1975)

Balph et al. (1979); Ketterson (1979)

Wolfenbarger (1999)

Senar et al. (1993) Møller (1987b); Maynard Smith and Harper (1988); Solberg and Ringsby (1997) Liker and Barta (2001); González et al. (2002); McGraw et al. (2003) Maynard Smith and Harper (1988)

Maynard Smith and Harper (1988)

Järvi and Bakken (1984b); Maynard Smith and Harper (1988); Wilson (1992); Lemel and Wallin (1993) Alonso-Alvarez et al. (2004) Hogstad and Kroglund (1993) Brotons (1998) Marler (1955) McGraw and Hill (2000a,c)

a. Size, area of colored feathers; color, hue, saturation, or brightness of colored patch. b. r2, percentage of dominance explained by the size of the plumage trait (according to a regression); when only a percentage is provided, it refers to the proportion of contests in which the bird with the larger badge won agonistic encounters. In all cases, the relationship between the two variables is positive, except in the House Finch and the Northern Cardinal. In those species, natural plumage color is correlated to dominance, but the relationship disappears in manipulated birds.

Harris’ Sparrow (Zonotrichia querula) White-crowned Sparrow (Z. leucophrys)

Corn Bunting (Emberiza calandra) Northern Cardinal (Cardinalis cardinalis) Dark-eyed Junco ( Junco hyemalis)

Carotenoid

Color

Yellowness of general plumage Black bib Black bib

UV Melanin Melanin Melanin Carotenoid

Presence Size Size Color Color

UV of crown Black breast stripe Black breast stripe Red breast Red breast

Melanin

Blue Tit (P. caeruleus) Willow Tit (P. montanus) Coal Tit (P. ater) Chaffinch (Fringilla coelebs) House Finch (Carpodacus mexicanus) Eurasian Greenfinch (Carduelis chloris) Eurasian Siskin (C. spinus) House Sparrow (Passer domesticus)

Size

Black breast stripe

Great Tit (Parus major)

juan carlos senar

92

adult

young

Dominance score

100

50

0

–50

–100 0

20

40

Bib size (mm2)

Figure 3.1. Relation between dominance score and bib size in captive Eurasian Siskins (r = 0.71, p < 0.01, n = 6 adults, 6 young). Note that the correlation is independent of the age of the birds. Such a correlation, however, is not sufficient as evidence for signaling, and manipulation experiments are needed as a definitive test (see Figure 3.5). Redrawn from Senar et al. (1993).

In dominance experiments in which plumage coloration is manipulated, there is additional confusion regarding which bird is being tested—the individual whose color has been altered or the individual(s) reacting to the manipulated bird. Some of these experiments were designed to test whether the manipulated bird was able to rise in a dominance hierarchy. Although these experimental tests of dominance implicitly assume a change in the behavior of unmanipulated birds as a result of the opponents’ badge enlargement, they should also test whether these unmanipulated birds show any avoidance of individuals differing in apparent dominance. In other words, the bird being tested is the individual reacting to the color manipulation. Another critical point if tests of status signaling are to be convincing is that the observer should record whether birds avoid probable dominants on first encounters (Geist 1966; Watt 1986a), or else other factors may mask assessment of the color display (see below). In several studies, dominance relationships were observed over long periods (e.g., 30 minutes in Lemel and Wallin 1993, 1 month in Fugle et al. 1984), making them unsuitable as tests of whether plumage signals dominance. Additionally, traits under study should not only be enlarged,

a. Badge of status enlarged. b. Badge of status reduced.

Choice tests

Model presentation

Dyeing dominantsb

Dyeing

subordinatesa

Experiment

Least Auklet (Aethia pusilla) Yellow Warbler (Dendroica petechia) American Redstart (Setophaga ruticilla) Red-collared Widowbird (Euplectes ardens) Great Tit Willow Tit (P. montanus) House Sparrow Eurasian Siskin (Carduelis spinus)

Model avoided Heightened aggression No effect Reduced aggression Model avoided Model avoided Model avoided Large badges avoided

Increased dominance No effect Increased dominance No effect Increased dominance Increased aggression Reduced territory

Dark-eyed Junco (Junco hyemalis) Northern Cardinal (Cardinalis cardinalis) Chaffinch (Fringilla coelebs) House Finch (Carpodacus mexicanus) House Sparrow (Passer domesticus) Common Yellowthroat (Geothlypis trichas) Red-winged Blackbird (Agelaius phoeniceus)

White-crowned Sparrow (Z. leucophrys)

Harris’ Sparrow (Zonotrichia querula)

Red-shouldered Widowbird (E. axillaris)

Yellow-browed Leaf Warbler (Phylloscopus inornatus) Great Tit (Parus major)

Effect Increased dominance Improved territory defense Increased dominance Improved territory defense Increased territory size Increased dominance No effect Increased dominance No effect Increased dominance

Red-collared Widowbird (Euplectes ardens)

Species

Table 3.2. Experiments Testing for the Status-Signaling Role of Plumage Traits

Pryke et al. (2002) Pryke et al. (2002) Pryke and Andersson (2003) Pryke et al. (2002) Marchetti (1998) Lemel and Wallin (1993) Järvi et al. (1987) Rohwer (1985) Rohwer (1977) Parsons and Baptista (1980); Fugle et al. (1984); Fugle and Rothstein (1987) Holberton et al. (1989); Grasso et al. (1996) Wolfenbarger (1999) Marler (1955) McGraw and Hill (2000a) González et al. (2002) Lewis (1972) Peek (1972); Smith (1972); Røskaft and Rohwer (1987) Jones (1990) Studd and Robertson (1985b) Procter-Gray (1991) Pryke et al. (2001) Järvi and Bakken (1984) Hogstad and Kroglund (1993) Møller (1987b) Senar and Camerino (1998)

Reference

juan carlos senar

94 experimental manipulation (n = 7)

Proportion of wins by original dominant

sham control (n = 2)

1.0

0.8

0.6

0.4

0.2

0

Before manipulation

After manipulation

Figure 3.2. The proportion of interactions (mean ± standard error) won by previously dominant Dark-eyed Juncos before and after a plumage manipulation in which the sizes of status badges were reduced. Birds that had white removed from their tails won fewer fights than controls. Redrawn from Grasso et al. (1996).

but they should also be reduced, a robust technique that is often difficult to perform and has rarely been used (e.g., Rohwer 1977; Grasso et al. 1996; Senar and Camerino 1998). The problems associated with the use of manipulated live birds introduced into a group may be solved by the use of models (either stuffed or completely artificial birds). Alternatively, the researcher may use a caged bird (Slagsvold 1993). This approach has been used for several species (Table 3.2). Results of studies that have used presentations of models or live birds have been more conclusive than manipulations of birds in groups, with test birds avoiding models with enlarged badges of status on their first encounter (Figure 3.4). These results strongly suggest that plumage color traits can be recognized as signals of social rank. The third approach that has been used to test for status signaling is choice experiments (Table 3.2), in which individuals are tested to see whether they can recognize dominant competitors by color alone. Senar and Camerino (1998) recorded the active choice between feeding close to a cage containing a live dominant bird or close to a cage containing a live subordinate (Figure 3.5). This approach has the advantage that, when working with flocking species,

Encounter rate (min–1)

enlarged 0.3

control

a

0.2 0.1

0 1.5

Territory size (ha)

reduced

b

1

0.5

0 red orange Manipulation

control

Figure 3.3. The effects of manipulations of the size and hue of collar patches of the Redcollared Widowbirds on (a) the number of aggressive interactions for males establishing territories and (b) their mean (± standard deviation) territory size. Redrawn from Pryke et al. (2002).

Test birdʼs breast stripe width:

>dummyʼs

1 but close to 1 for i = 1, Κ, n (see Ripoll et al., 2004, for details). The model allows for the establishment of conditions necessary for the development of evolutionarily stable strategies. Let us consider a strategy defined by a vector η containing as components a given subset of the transition probabilities τij . This will be a suitable choice for a strategy if, for instance, one accepts that it is possible to change the value of some τij behaviorally to maximize fitness. The evolutionarily stable values of the transition probabilities τij appearing in η, using the net reproductive number R0(η, N*) as a fitness measure, are those values ηess of η that render an equilibrium N * such that si (φi*) + fi (φi*) = 1 for i = 1, κ, n, where φi* = φi (N *(ηess)). Note that these equalities indicate that, at the equilibrium determined by ηess, all dominance classes have the same fitness (measured by the sum of survival plus fertility) and, in fact, all of them have the same reproductive value. In other words, there exists a sort of “ideal free distribution” of individuals among dominance classes. However, it is easy to see that any strategy ηess is evolutionary neutral in the sense that, in a resident equilibrium population adopting ηess, any mutant population with a different strategy ηmut will be also at equilibrium: R0(ηmut; N *(ηess)) = 1 for all ηmut ∈[0, 1]. That is, the function η → R0(η, N*(ηess)) does not have a strict maximum at η = ηess. However, using a 2 × 2 matrix model, it is easy to show that a necessary condition for ηess to be the limit of trait substitution sequences

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(TSSs) in the trait space Ω = {(η1, η2) ∈[0, 1] × [0,1]}; that is, like-versuslike aggression among individuals of the dominant class is a neccessary condition for the mathematical convergence to be stable. Consider, for instance, the model with the following transition and aggression matrices

T=

(

1 – η1 η2 , η1 1 – η2

)

W=

ω1 1 – ω2

(

1 – ω1 , ω2

)

with 0 ≤ ηi , ωi ≤ 1 (i = 1, 2). To have a unique equilibrium N * = W –1C defined by ηess, det(W ) = ω1ω2 – (1 – ω1)(1 – ω2) = ω1 + ω2 – 1 ≠ 0. Note that this expression is, in fact, a measure of the balance of an average of aggression within (ω1ω2) and between (1 – ω1)(1 – ω2) dominance classes. So, when ω1 + ω2 > 1, we talk about like-versus-like aggression because then ω1ω2 > (1 – ω1)(1 – ω2). The simplest way to check the necessity of this sort of aggression for the convergence stability of ηess is by computing the fitness gradient (∂R0/∂η1, ∂R0/∂η2) at the boundary of trait space Ω given by {(0, η2): 0 ≤ η2 ≤ 1}. Then it follows that, at any point of this boundary, ∂R0/∂η2 = 0 and ∂R0/∂η1 > ( ( 1 do TSSs escape from the boundary {(0, η2): 0 ≤ η2 ≤ 1}, which is a necessary condition for the convergence of TSSs toward a ηess, as such a strategy never has the form (0, η2) for any 0 ≤ η2 ≤ 1.

ability compared to adults and they display colors that are unattractive to females, thus avoiding competition with adults (Lawton and Lawton 1986; Lyon and Montgomerie 1986). In other words, it could be argued that the presence of ornamental plumage traits signals dominance, whereas the presence of DPM traits signals subordinance. Several well-designed experiments with bird models and detailed behavioral observations have shown how birds in immature plumage (DPM) succeed in eliciting less aggression from adult birds (Table 3.5). Hence I stress that DPM signals have their own selection pressures and can be treated as signals that are distinct from signals of social status.

Color Displays as Intrasexual Signals of Aggression and Dominance

Box 3.2. Bimodality of the Equilibrium Even though the model in Box 1 is nonlinear, an explicit expression of N *(ηess ) is easily obtained under the hypotheses on si and fi and assuming that W is an invertible matrix. This fact allows one to establish precise conditions for the bimodality of N * under evolutionarily stable transition rates among dominant classes. From the condition si (φi*) + fi (φi*) = 1, it immediately follows that the equilibrium is given by: N *(ηess ) = W –1C, where C is a constant vector with components ci = Fi –1(1/si0 + fi 0 )). In particular, for a 3 × 3 matrix model:

W=

(

ω1 (1 – ω1)/2 0 ω2 0 1 – ω3

)

(1 – ω2)/2 1 – ω2 , ω3

and Fi (φ) = F(φ) for i = 1, 2, 3, it immediately follows that N2* < N3* is equivalent to c3 > c2, as long as ω1 > 0 and ω2 + ω3 > 1 (i.e., under like-versuslike aggression), which implies that the sum of potential survival and fertility rates of dominant individuals (s30 + f30 ) has to be higher than that of subdominants (s20 + f20 ). However, the second condition for bimodality, namely, N1* > N2*, is satisfied for a wide range of values of si0, fi 0, and ωi for any N *(ηess) > 0, as long as the probability of aggressive encounters among subordinates ω1 is small enough (for details, see Ripoll et al., 2004).

Alternative Hypotheses on DPM Although the more general view of DPM is that the trait signals a low competitive ability, other hypotheses have been proposed to explain DPM. The female-mimicry hypothesis proposes that the aim of DPM is to allow males to mimic females, avoiding in this way attacks from adult males (Rohwer 1978a; Rohwer et al. 1980). Work on Pied Flycatchers (Ficedula hypoleuca; Plate 27, Volume 1; Slagsvold and Sætre 1991) and European Kestrels (Falco tinnunculus;

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Hakkarainen et al. 1993), in which adult males do not distinguish females from immatures, supports this view (see also Table 3.5). The juvenile-mimicry hypothesis proposes that immature birds with DPM mimic nonreproductive juveniles, in this way avoiding aggression from the adult class (Lawton and Lawton 1986; Foster 1987; Table 3.5). Both hypotheses assume that the reduced aggression that immatures receive from adults is through deception rather than signaling. It is very difficult, however, to ascertain this intention (Semple and Mccomb 1996), and because the aim underlying all of these hypotheses is the same, I think it is more parsimonious to take all of these hypotheses as equivalent, irrespective of the plumage that immatures are wearing (female-like, juvenile-like, or immature per se) to reduce the aggression they receive from adults (see also Lawton and Lawton 1986; Thompson 1991). The remaining alternative hypotheses to explain DPM assume a nonsignaling function of the trait. The cryptic hypothesis proposes that immature plumage allows birds to avoid the attack of predators (Selander 1965; Procter-Gray and Holmes 1981; Hill 1988; Stutchbury 1991; Table 3.5). Some work has found that the more cryptic plumage of immature birds makes them less vulnerable to predation (de Vries 1976; Slagsvold et al. 1995; Götmark 1997; Götmark et al. 1997). However, although DPM may reduce predation, this is probably not the evolutionary force selecting for this plumage. There are many species for which the difference between immatures and adult birds appears as just a few feathers (e.g., greater coverts; Jenni and Winkler 1994), and although these feathers do not confer to immatures a cryptic appearance, they are enough to reduce the aggression they may receive from adult birds (Lyon and Montgomerie 1986; Senar et al. 1998). Additional discredit for the hypothesis comes from reasoning that, if crypsis was the main selective pressure, immatures should behave cryptically and should retain the cryptic brown and streaked plumage of most juvenile birds, which is not the case (Rohwer et al. 1980). The nonadaptive hypothesis suggests that DPM is the result of an energetic constraint that prevents an additional feather molt (Rohwer 1986; Rohwer and Butcher 1988). That some birds undertake a complete molt to obtain again an immature appearance, however, falsifies this hypothesis (Rohwer and Butcher 1988). Adult-Plumaged Immatures Although DPM refers to birds with a distinctively immature appearance, immature plumage can be highly variable, and some individuals may strongly resemble adults (Rohwer et al. 1980; Lyon and Montgomerie 1986). Detailed

Color Displays as Intrasexual Signals of Aggression and Dominance

behavioral observations have shown how these birds with an “advanced plumage maturation” (APM) enjoy a higher mating and breeding success than do individuals with DPM (Ralph and Pearson 1971; Rohwer and Niles 1979; Payne 1982; Price 1984; Hill 1988; Grant 1990). Analyses of patterns of aggression show that adult-plumaged immatures are distinguished by the adult class from adults and immature-plumaged birds, and are the target of aggressive interactions from the adult class, probably because these APM individuals are highly successful in attracting females (Hill 1989; Smith 1992; Gosler 1993; Senar et al. 1998; Table 3.5). Under harsh environmental conditions, APM birds lose body condition and have higher mortality rates compared to DPM birds (Grant 1990; Senar et al. 1998), which emphasizes the trade-off between sexual signaling and survival. Adaptation to Winter or Spring? It has been debated whether DPM is an adaptation to winter or to spring conditions (Rohwer 1983; Rohwer and Butcher 1988). Earlier hypothesis on DPM assumed that the trait had evolved as an adaptation to spring, when competition with adult birds is thought to be more intense. However, it could be that DPM had appeared as an adaptation to winter, to aid immatures in avoiding aggression from adult birds. Winter adaptation could cause birds to be less attractive to mates in the spring (Rohwer and Butcher 1988). That several bird species may pair during winter (Senar and Borras 2004) additionally complicates the situation. A way to resolve this controversy is to focus on species that develop a spring molt and to compare plumages in winter and spring. Immature Indigo Buntings (Passerina cyanea), for instance, display a female-like plumage during autumn and winter, but molt in spring to an adult-like plumage, supporting the view that DPM is functional during the wintering period (Rohwer 1986). In contrast, Painted Buntings (Passerina ciris) molt into a female-like plumage in spring, which suggests that DPM is functional in both periods (Thompson 1991). In spite of interspecific variation, however, most species with spring molt change from a delayed to an adult-like plumage, whereas species that display DPM throughout the year do not molt in spring (Rohwer and Butcher 1988). This led Rohwer and Butcher (1988) to suggest that DPM was an adaptation for the winter (when aggression is probably more costly) and that most species displayed DPM during the breeding season because of a molt constraint that prevented these species from molting in spring to a more colorful plumage. Comparative analyses support this view (Beauchamp 2003).

119

— — — —

— — — — — I

Tree Swallow

Elepaio (Chasiempis sandwichensis)

I

—

— — —

S — — —

I — — S — — —

I — S

S S —

Baltimore Oriole Orchard Oriole (I. spurius) Long-tailed Manakin (Chiroxiphia linearis) Long-tailed Manakin Purple Martin (Progne subis) Purple Martin Tree Swallow (Tachycineta bicolor)

—

—

European Kestrel (Falco tinnunculus) Mute Swan (Cygnus olor) Indigo Bunting (Passerina cyanea) Orange-breasted Bunting (P. leclancherii) Painted Bunting (P. ciris) Lazuli Bunting (P. amoena) Lazuli Bunting Baltimore Oriole (Icterus galbula)

FM

CA

Species

Winter

—

—

— — — —

— — —

S — — —

I S I

—

C

S

S

S I — S

S I S

I S S —

— I I

I

CA

I

—

I I S —

S I I

S I — —

I I I

S

FM

—

—

S — — —

I I I

I — — —

I I I

—

C

Spring

I

—

S — — —

— I I

I — — —

— I —

—

JM

Table 3.5. Studies of Delayed Plumage Maturation and the Different Hypotheses They Support

—

—

S I — —

— — I

I — — —

I I —

—

MC

Model presentation

Behavioral observation

Behavioral observation Model presentation Behavioral observation Model presentation

Model presentation Model presentation Model presentation

Molt phenology Model presentation Behavioral observation Molt phenology

Behavioral observation Molt phenology Molt phenology

Decoy presentation

Method

Foster (1987) Stutchbury (1991) Brown (1984) Stutchbury and Robertson (1987) Lozano and Handford (1995) VanderWerf and Freed (2003)

Conover et al. (2000) Rohwer (1986) Thompson and Leu (1995) Thompson (1991) Muehter et al. (1997) Greene et al. (2000) Rohwer and Manning (1990) Flood (1984) Enstrom (1992) McDonald (1993)

Hakkarainen et al. (1993)

Reference

—

I — S I

— — I — — S

Black Redstart

Black Redstart Cedar Waxwing (Bombycilla cedrorum) House Finch (Carpodacus mexicanus) Eurasian Siskin (Carduelis spinus) I

—

I —

—

—

—

—

—

S —

—

— —

—

—

—

— S

I

I

S

I

S

I S

—

S I

S

—

—

— I

I

I

I

S

—

I I

I

I I

—

—

—

— I

—

I

—

—

—

I I

S

S —

—

—

—

— —

I

I

—

—

—

I —

—

— I

—

—

—

— —

S

S

—

—

—

— —

—

— —

—

Behavioral observation

Behavioral observation

Behavioral observation Behavioral observation

Model presentation

Behavioral observation

Behavioral observation

Decoy presentation

Behavioral observation

Molt phenology Behavioral observation

Behavioral observation

Behavioral observation Model presentation

Model presentation

Senar et al. (1998)

Landmann and Kollinsky (1995a) Landmann and Kollinsky (1995b) Cuadrado (1995) Mountjoy and Robertson (1988) Brown and Brown (1988)

Slagsvold and Sætre (1991); Sætre and Slagsvold (1996) Weggler (1997)

Karubian (2002)

Procter-Gray and Holmes (1981) Rohwer et al. (1983) Grant (1990)

Hill (1988, 1994) Procter-Gray (1991)

Hill (1989)

Notes: CA, competitive-ability-signaling hypothesis; FM, female-mimicry hypothesis; C, cryptic hypothesis; JM, juvenile-mimicry hypothesis; MC, molt constraint hypothesis; S, hypothesis is supported; I, available data are inconsistent with hypothesis; —, no data available.

—

—

—

—

—

—

—

—

— — —

— —

— —

S —

—

—

Black Redstart (Phoenicurus ochruros) Black Redstart

American Redstart Medium Ground Finch (Geospiza fortis) Red-backed Fairy-wren (Malurus melanocephalus) Pied Flycatcher (Ficedula hypoleuca)

Black-headed Grosbeak (Pheucticus melanocephalus) Black-headed Grosbeak American Redstart (Setophaga ruticilla) American Redstart

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Evolutionary History of DPM A key point to the understanding of DPM is whether this is an ancestral or derived trait. Comparative analyses on House Finches (Carpodacus mexicanus) have shown that DPM in this group has evolved recently (Hill 1996). Data from gulls, fulmars, and waders, however, suggest that DPM in this group is the result of collateral selection on reduced molt, implying that DPM per se has no function (Chu 1994). Comparative analyses from nine-primaried oscines suggested that DPM in these birds is an ancestral character and that the evolutionary novelty had been the appearance of immatures with an adult-like plumage (Björklund 1991). Consequently Björklund (1991) proposed that it would be more suitable to refer to a process of “advanced plumage maturation” rather than DPM. In any case, until more data are available from a broader range of taxa, comparative data show that DPM may have evolved several times and probably for different reasons in different groups (Weggler 1997).

Intrasexual Signaling Not Related to Fighting Ability Bird colors may function as signals in other intrasexual social contexts not related to aggression and dominance (Chapter 4). Some early work proposed that white patches on wings and on other body parts could function as signals to recruit conspecific individuals at feeding areas (Armstrong 1971; Kushlan 1977). The increased size of the flock would then improve vigilance and the probability of detecting predators (Hinde 1961). Recent comparative data support this function for white patches (Beauchamp and Heeb 2001). Conversely, it has been suggested that white patches in rump feathers, tails, or wings could act as warning flashes, signaling to flock companions the presence of a predator (Brooke 1998). Such a signal could be beneficial to the signaler by getting flock companions to take flight, creating a dilution effect. Some detailed work (Alvarez 1989, 1993), however, suggests that other alternatives, such as startling predators, better explain the appearance of these flashes (e.g., Brooke 1998).

Summary Nearly three decades after the original description of the status signaling hypothesis and after several reviews, the role of color displays in intrasexual sig-

Color Displays as Intrasexual Signals of Aggression and Dominance

naling remains controversial. Nevertheless, we can now safely state that, at least for several bird species, colors can act as true signals of fighting ability. Such signaling may be particularly relevant for species in which many unfamiliar individuals interact, so that individual recognition is unlikely. Signaling between but not within age and sex classes should not be regarded as true status signaling. Most descriptions of status signaling refer to species displaying melanin-based plumage coloration, but carotenoid and structural color displays can also signal status. Fighting ability is normally signaled by the size of the trait, and there are only a few examples in which color quality is of importance. I identify cases for which the relationship between fighting ability and plumage badges may reverse. Different hypotheses have been proposed to explain the reliability of badges of status. Three of them may be especially relevant: (1) the social control hypothesis, which proposes that only high quality individuals can afford the levels of aggression that high status individuals generally experience; (2) the immunocompetence handicap, which proposes that only high-quality birds can withstand the immunosuppression of hormones (e.g., testosterone) necessary to produce melanin and become dominant; and (3) the mixed ESS hypothesis, which views large-badged dominants and small-badged subordinates as displaying different but equally fit strategies, so that there is no reason for subordinates to pretend to increase their rank. Recent theoretical and empirical data link social and physiological costs, which could nicely explain signal reliability for melanin-based signals. I additionally discuss drawbacks of some of the experiments used up to now to test the reliability of the status-signaling system. Nevertheless, it is probable that there is no single evolutionary route to badges of status and therefore, there is no unique mechanism to maintain the honesty of the signals. Finally, I present a model that explains why the frequency distribution of status badges generally follows a normal distribution but also provide instances in which it should be bimodal, as it is in the case of a few species. Although fighting ability is the most common information provided by color patches, other social interactions can also be of importance. Delayed plumage maturation, in which immature birds display a plumage different from that of adult birds, is used by subadults to signal to adults their youth and lower mate-competitive ability, avoiding in this way aggression from the adult class. Color patches can also be used to attract conspecifics, thereby increasing the size of the flock and hence the possibilities of detecting food or staying safe from predators (e.g., dilution effect).

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Color Displays as Intrasexual Signals of Aggression and Dominance Rohwer, S. A. 1983. Testing the female mimicry hypothesis of delayed plumage maturation: A comment on Procter-Gray and Holmes. Evolution 37: 421–423. Rohwer, S. A. 1985. Dyed birds achieve higher social status than controls in Harris’ Sparrows. Anim Behav 33: 1325–1331. Rohwer, S. A. 1986. A previously unknown plumage of first-year Indigo Buntings and theories of delayed plumage maturation. Auk 103: 281–292. Rohwer, S. A., and G. S. Butcher. 1988. Winter versus summer explanations of delayed plumage maturation in temperate passerine birds. Am Nat 131: 556– 572. Rohwer, S. A., and P. W. Ewald. 1981. The cost of dominance and advantage of subordination in a badge signaling system. Evolution 35: 441–454. Rohwer, S. A., and D. M. Niles. 1979. The subadult plumage of Purple Martins: Variability, female mimicry and recent evolution. Z Tierpsychol 51: 282–300. Rohwer, S. A., and J. Manning. 1990. Differences in timing and number of molts for Baltimore and Bullock’s Orioles: Implications to hybrid fitness and theories of delayed plumage maturation. Condor 92: 125–140. Rohwer, S. A., and F. C. Rohwer. 1978. Status signalling in Harris’ Sparrows: Experimental deceptions achieved. Anim Behav 26: 1012–1022. Rohwer, S. A., and E. Røskaft. 1989. Results of dyeing male Yellow-headed Blackbirds solid black: Implications for the arbitrary identity badge hypothesis. Behav Ecol Sociobiol 25: 39–48. Rohwer, S. A., S. D. Fretwell, and D. M. Niles. 1980. Delayed maturation in passerine plumages and the deceptive acquisition of resources. Am Nat 115: 400–437. Rohwer, S. A., W. P. Klein, and S. Herad. 1983. Delayed plumage maturation and the presumed prealternate molt in American Redstarts. Wilson Bull 95: 199–208. Roper, T. J. 1986. Badges of status in avian societies. New Sci 109: 38–40. Røskaft, E., and S. Rohwer. 1987. An experimental study of the function of the red epaulettes and the black body colour of the male Red-winged Blackbirds. Anim Behav 35: 1070–1077. Ryan, P. G., R. P. Wilson, and J. Cooper. 1987. Intraspecific mimicry and status signals in juvenile African penguins. Behav Ecol Sociobiol 20: 69–76. Sætre, G. P., and T. Slagsvold. 1996. The significance of female mimicry in male contests. Am Nat 147: 981–995. Selander, R. K. 1965. On mating systems and sexual selection. Am Nat 99: 129–141. Semple, S. and K. Mccomb. 1996. Behavioural deception. Trends Ecol Evol 11: 434–437. Senar, J. C. 1990. Agonistic communication in social species: What is communicated? Behaviour 112: 270–283. Senar, J. C. 1994. Vivir y convivir: La vida en grupos sociales. In J. Carranza, ed., Etología: Introducción a la Ciéncia del Comportamiento, 205–233. Cáceres, Spain: University of Extremadura.

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juan carlos senar Senar, J. C. 1999. Plumage coloration as a signal of social status. In N. Adams and R. Slotow, eds., Proceedings of the 22nd International Ornithological Congress, Durban, 1669–1686. Johannesburg: BirdLife South Africa. Senar, J. C. 2004. Mucho Más que Plumas. Monografies del Museu de Ciències Naturals. Volume 2. Barcelona: Museu de Ciències Naturals. Senar, J. C., and A. Borras. 2004. Sobrevivir al invierno: Estratégias de las aves invernantes en la Península Ibérica. Ardeola 51: 133–168. Senar, J. C., and M. Camerino. 1998. Status signalling and the ability to recognize dominants: An experiment with siskins (Carduelis spinus). Proc R Soc Lond B 265: 1515–1520. Senar, J. C., and D. Escobar. 2002. Carotenoid derived plumage coloration in the siskin Carduelis spinus is related to foraging ability. Avian Sci 2: 19–24. Senar, J. C., M. Camerino, and N. B. Metcalfe. 1989. Agonistic interactions in Siskin flocks: Why are dominants sometimes subordinate? Behav Ecol Sociobiol 25: 141–145. Senar, J. C., M. Camerino, and N. B. Metcalfe. 1990a. Familiarity breeds tolerance: The development of social stability in flocking siskins (Carduelis spinus). Ethology 85: 13–24. Senar, J. C., J. L. Copete, and N. B. Metcalfe. 1990b. Dominance relationships between resident and transient wintering siskins. Ornis Scand 21: 129–132. Senar, J. C., P. J. K. Burton, and N. B. Metcalfe. 1992. Variation in the nomadic tendency of a wintering finch Carduelis spinus and its relationship with body condition. Ornis Scand 23: 63–72. Senar, J. C., M. Camerino, J. L. Copete, and N. B. Metcalfe. 1993. Variation in black bib of the Eurasian Siskin (Carduelis spinus) and its role as a reliable badge of dominance. Auk 110: 924–927. Senar, J. C., M. Camerino, and N. B. Metcalfe. 1997. A comparison of agonistic behaviour in two Cardueline finches: Feudal species are more tolerant than despotic ones. Etología 5: 73–82. Senar, J. C., J. L. Copete, and A. J. Martin. 1998. Behavioural and morphological correlates of variation in the extent of postjuvenile moult in the siskin Carduelis spinus. Ibis 140: 661–669. Senar, J. C., V. Polo, F. Uribe, and M. Camerino. 2000. Status signalling, metabolic rate and body mass in the siskin: The cost of being a subordinate. Anim Behav 59: 103–110. Senar, J. C., J. Figuerola, and J. Domènech. 2003. Plumage coloration and nutritional condition in the Great Tit Parus major: The roles of carotenoids and melanins differ. Naturwissenschaften 90: 234–237. Senar, J. C., J. Domènech, and M. Camerino. 2005. Female siskins choose mate by the size of the yellow wing stripe. Behav Ecol Sociobiol 57:445–469.

Color Displays as Intrasexual Signals of Aggression and Dominance Shields, W. M. 1977. The social significance of avian winter plumage variability: A comment. Evolution 31: 905–907. Slagsvold, T. 1993. Sex recognition and breast stripe size in Great Tits. Ardea 81: 35–42. Slagsvold, T., and G. P. Sætre. 1991. Evolution of plumage color in male Pied Flycatchers (Ficedula hypoleuca): Evidence for female mimicry. Evolution 45: 910–917. Slagsvold, T., S. Dale, and A. Kruszewicz. 1995. Predation favours cryptic coloration in breeding male Pied Flycatchers. Anim Behav 50: 1109–1121. Slotow, R., J. Alcock, and S. I. Rothstein. 1993. Social status signalling in Whitecrowned Sparrows: An experimental test of the social control hypothesis. Anim Behav 46: 977–989. Smith, D. G. 1972. The role of the epaulets in the Red-winged Blackbird (Agelaius phoeniceus) social system. Behaviour 41: 251–268. Smith, R. D. 1992. Age determination, wing-feather colour and wing-length change in Snow Buntings Plectrophenax nivalis. Ringing Migration 13: 43–51. Solberg, E. J., and T. H. Ringsby. 1997. Does male badge size signal status in small island populations of House Sparrows, Passer domesticus? Ethology 103: 177–186. Studd, M. V., and R. J. Robertson. 1985a. Life span, competition, and delayed plumage maturation in male passerines: The breeding threshold hypothesis. Am Nat 126: 101–115. Studd, M. V., and R. J. Robertson. 1985b. Evidence for reliable badges of status in territorial Yellow Warblers (Dendroica petechia). Anim Behav 33: 1102–1113. Studd, M. V., and R. J. Robertson. 1985c. Sexual selection and variation in reproductive strategy in male Yellow Warblers (Dendroica petechia). Behav Ecol Sociobiol 17: 101–109. Stutchbury, B. J. 1991. The adaptive significance of male subadult plumage in Purple Martins: Plumage dyeing experiments. Behav Ecol Sociobiol 29: 297–306. Stutchbury, B. J., and R. J. Robertson. 1987. Signaling subordinate and female status: Two hypotheses for the adaptive significance of subadult plumage in female Tree Swallows. Auk 104: 717–723. Számado, S. 2000. Cheating as a mixed strategy in a simple model of aggressive communication. Anim Behav 59: 221–230. Tanaka, Y. 1996. Social selection and the evolution of animal signals. Evolution 50: 512–523. Thompson, C. W. 1991. The sequence of molts and plumages in Painted Buntings and implications for theories of delayed plumage maturation. Condor 93: 209–235. Thompson, C. W., and M. Leu. 1995. Molts and plumages of Orange-breasted Buntings (Passerina leclancherii): Implications for theories of delayed plumage maturation. Auk 112: 1–19. Tuttle, E. M. 2003. Alternative reproductive strategies in the White-throated Sparrow: Behavioral and genetic evidence. Behav Ecol 14: 425–432.

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juan carlos senar Vaclav, R., and H. Hoi. 2002. Different reproductive tactics in House Sparrows signalled by badge size: Is there a benefit to being average? Ethology 108: 569–582. VanderWerf, E. A., and L. A. Freed. 2003. Elepaio subadult plumages reduce aggression through graded status-signaling, not mimicry. J Field Ornithol 74: 406–415. Veiga, J. P. 1993. Badge size, phenotypic quality, and reproductive success in the House Sparrow: A study on honest advertisement. Evolution 47: 1161–1170. Watt, D. J. 1986a. A comparative study of status signalling in sparrows (genus Zonotrichia). Anim Behav 34: 1–15. Watt, D. J. 1986b. Relationship of plumage variability, size and sex to social dominance in Harris’ Sparrows. Anim Behav 34: 16–27. Weggler, M. B. 1997. Age-related reproductive success and the function of delayed plumage maturation in male Black Redstarts Phoenicurus ochruros. Ph.D. diss., Universität Zürich, Zürich, Switzerland. West-Eberhard, M. J. 1975. The evolution of social behaviour by kin selection. Q Rev Biol 50: 1–33. Whitfield, D. P. 1986. Plumage variability and territoriality in breeding turnstone Arenaria interpres: Status signalling or individual recognition? Anim Behav 34: 1471–1482. Whitfield, D. P. 1987. Plumage variability, status signalling and individual recognition in avian flocks. Trend Ecol Evol 2: 13–18. Wiley, R. H. 1990. Prior-residency and coat-tail effects in dominance relationships of male Dark-eyed Juncos Junco hyemalis. Anim Behav 40: 587–596. Wilson, J. D. 1992. A re-assessment of the significance of status signalling in populations of wild Great Tits, Parus major. Anim Behav 43: 999–1009. Wingfield, J. C., G. F. Ball, A. M. Dufty, Jr., R. E. Hegner, and M. Ramenofsky. 1987. Testosterone and aggression in birds. Am Sci 75: 602–608. Wolf, J. B., E. D. Brodie, III, and A. J. Moore. 1999. Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. Am Nat 153: 254–266. Wolfenbarger, L. L. 1999. Is red coloration of male Northern Cardinals beneficial during the nonbreeding season? A test of status signaling. Condor 101: 655–663. Yezerinac, S. M., and P. J. Weatherhead. 1997. Extra-pair mating, male plumage coloration and sexual selection in Yellow Warblers (Dendroica petechia). Proc R Soc Lond B 264: 527–532.

4 Female Mate Choice for Ornamental Coloration geoffrey e. hill

Studies of female mate choice are inexorably linked to the colorful displays of birds. Many of the original formulations of sexual selection models for the evolution of display traits used avian coloration as examples and inspirations. Honest signaling theory was developed in large part to explain plumage coloration. Since Darwin, many biologists have assumed that a primary function of the colorful displays of male birds is to attract mates and that the bright coloration of birds evolved in response to selection resulting from female choice for colorful displays (see Blaisdell 1992 and Cronin 1991 for summaries). Until relatively recently, however, this basic assumption that males with superior color displays are preferred as mates by females remained largely untested. Despite keen interest in resolving this question, neither Darwin nor any of his contemporaries attempted to test whether females choose mates based on expression of integumentary coloration. In 1907, Frank Finn wrote an explicit description for the sort of experiments that might test the idea that female birds choose mates based on the ornamental coloration of males, but Finn never conducted the experiments that he proposed. Although much of the debate between Darwin and Wallace focused on plumage coloration in birds (Cronin 1991; Blaisdell 1992), and Finn used birds as his model for devising tests of mate choice theory, all of the early attempts to quantify or test for female mate choice based on male coloration were conducted with fishes.

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geoffrey e. hill In the same year that Finn outlined his ideas for mate choice experiments, Reeves (1907) published observations of wild Rainbow Darters (Etheostoma caeruleum) in a stream in Michigan and concluded that, although males had variable red coloration, females did not appear to base their choice of mates on male coloration. It was not until 1936, however, that Noble and Curtis published the first experimental confirmation of Darwin’s hypothesis that females prefer to mate with males showing the most elaborate color displays. They experimentally increased and decreased the red coloration of male Jewel Fish (Hemichromis bimaculatus) and found that females laid more eggs in proximity to the brightly colored males. Soon thereafter, Pelkwijk and Tinbergen (1937) published experimental evidence for female mate choice for bright red coloration in Three-spined Sticklebacks (Gasterosteus aculeatus). These studies validated Darwin’s hypothesis that male color displays are used by females in choosing mates. Despite the great importance of these first experimental tests of female mate choice to a general understanding of the evolution of animal color displays, the work of Noble and his colleagues and Pelkwijk and Tinbergen was largely ignored for 40 years. It was not until theoretical models showed that intersexual selection could lead to the evolution of ornamental traits (Fisher 1958; Maynard Smith 1958; O’Donald 1962) that biologists returned to empirical studies of sexual selection, this time with a focus on birds as well as fish, but with little memory of the pioneering studies conducted in the 1930s. There is now substantial experimental and correlational evidence that color displays in the plumage, bills, and legs of at least some bird species are used by females to assess potential mates. In this chapter, I review studies that have addressed the idea that birds use the coloration of potential mates in deciding who to choose both as social mates and as the sires of offspring. I focus on female choice of male coloration, but include a few studies of male choice for female coloration (male mate choice is also reviewed in Chapter 7). I consider carotenoid pigmentation, melanin pigmentation, and structural coloration separately, because these traits are under very different environmental, hormonal, and genetic control (Part III, Volume 1). I also consider the few studies that have been conducted on coloration that results from pigments other than carotenoids or melanins. Other chapters in this volume focus on the signal content of coloration used outside the context of sexual selection (Chapter 5) and the benefits to females of choosing males based on color display (Chapter 6), so these topics will not be reviewed in depth here. In reading this chapter on mate choice, however, it is important to keep in mind that differ-

Female Mate Choice for Ornamental Coloration

ent types of color displays have been shown to signal different things. Carotenoid and structural colors seem most often to reflect the foraging ability and the health of a male, whereas melanin displays more commonly reflect hormonal status and fighting ability (Chapter 12, Volume 1; Chapter 3). Whether females use particular color displays as criteria in mate choice will obviously be affected by the information content of those displays. Throughout this chapter I distinguish between studies of the size of color patches, the quality of coloration of a given patch, and, in the few studies in which it has been considered, the symmetry of coloration. When considering color quality, various studies have used hue; chroma/saturation (used interchangeably here, see Chapter 3, Volume 1); brightness (both including and excluding the ultraviolet [UV]); or combinations of these colorimetrics either measured with spectrometers or visually assessed relative to color swatches or as ranks on relative scales (see Chapter 3, Volume 1, for a detailed discussion of techniques). Some studies have also used subjective assessments of “brightness” or “ colorfulness.” Most studies have focused on chromatic coloration, but a few studies have also considered achromatic (black and white) coloration, and I review these as well. The reader should be mindful of the very different color quantification systems that have been used in different studies. In Table 4.1, I list studies of mate choice relative to male coloration in birds and the approach that was used in the studies. Studies of female mate choice in birds range from weak correlative field studies and uncontrolled aviary observations to carefully controlled experimental tests in both the lab and the field. Many studies are based on observations of wild populations in which date of pairing, breeding onset, assortative mating, or success at extra-pair mating are used as evidence for mate choice for a color display. These correlative studies may be consistent with the hypothesis that females use male coloration in mate choice, but generally they cannot rule out the possibility that other features that are correlated with color display, such as age or health, might be the real object of mate selection or that male-male interactions might create such patterns (Chapter 3). Better, but much more difficult to conduct, are field manipulations in which color is randomly or systematically assigned to males, thus eliminating correlated effects. If males that are dyed to be more colorful pair faster or at a higher frequency, nest earlier, or are more successful in extra-pair mating than control males or males made less colorful, this can be convincing evidence that color is affecting female choice. Male-male competition, however, can usually be completely eliminated only in aviary experiments.

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Table 4.1. Studies of Female Mate Choice Relative to Male Color Displays in Birds, Grouped by the Color Mechanism That Was the Primary Focus Color mechanism or type Carotenoid plumage

Eumelanin plumage

Species

Trait a

Typeb

Variablec

Descriptord

American Goldfinch (Carduelis tristis) American Goldfinch

plum/bill

car

cq

hue, sat, br

plum

car

cq

comp

Common Rosefinch (Carpodacus erythrinus) Eurasian Siskin (Carduelis spinus) House Finch (Carpodacus mexicanus) House Finch House Finch House Finch

plum

car

cq/pz

size

plum

car

pz

size

plum

car

cq/pz

comp

plum plum plum

car car car

cq cq/cs cq/cs/ pz/ps

comp comp/hue hue/sym/ size

House Finch Northern Cardinal (Cardinalis cardinalis) Northern Cardinal Northern Cardinal Red-backed Fairy-wren (Malurus melanocephalus) Red-collared Widowbird (Euplectes ardens) Red-shouldered Widowbird (Euplectes axillaris) Red-winged Blackbird (Agelaius phoeniceus) Village Weaverbird (Ploceus cucullatus) Yellow-browed Leaf Warbler (Phylloscopus inornatus) Yellowhammer (Emberiza citrinella) Yellowhammer

plum plum

car car

cq cq

comp comp

plum plum/bill plum

car car car/eu

cq cq cq/pz

comp comp comp

plum

car + mel cq/pz

plum

car + mel cq/pz

plum

car + mel cq/pz

hue, sat, br, size hue, sat, br, size nomea

plum

car

cq/pz

nomea

plum

car?

pz

size

plum

car

cq/pz

comp

plum

car

pz

comp

plum plum

eu eu

pz pz

size size

plum

eu

pz

size

plum

eu

pz

size

plum

eu

pz

size

American Goldfinch Cactus Finch (Geospiza scandens) Common Yellowthroat, (Geothlypis trichas) Eurasian Siskin (Carduelis spinus) Great Tit (Parus major)

Field/lab

Experimental or corre

Color manipulationf

Control for dominance?

Choice for elaborate color?g

Reference

Lab

corr

None

Yes

Yes, ap

Johnson et al. (1993)

Field

corr

None

No

Yes, am

Field

corr

None

No

No, ps

MacDougall and Montgomerie (2003) Bjorklund (1990)

Lab

exp

nat

Yes

Yes, ap

Senar et al. (2005)

Lab

exp

nat

Yes

Yes, ap

Hill (1990, 1994)

Field Field Field

exp corr corr

nat None None

No No No

Yes, ps Yes, ps Yes, ps

Hill (1991) Hill (1990); Hill et al. (1999a) Badyaev and Hill (2002); Badyaev et al. (2001)

Field Lab

corr exp

None nat

No Yes

No, cuck No, ap

Hill et al. (1994) Wolfenbarger (1999a)

Field Field Lab

corr corr corr

None None None

No No Yes

Yes, ed Yes, am Yes, ap

Wolfenbarger (1999b) Jawor et al. (2003) Karubian (2002)

Field

corr

None

No

No, ps, ed

Pryke et al. (2001a)

Field

exp

No

No, ps

Pryke and Andersson (2003)

Field

exp

black, nat black

No

No, ps

Peak (1972); Smith (1972)

Lab

exp

black

No

Yes, ps

Collias et al. (1979)

Field

exp

nat

No

No, ed

Marchetti (1998)

Lab

exp

nat

Yes

Yes, ap

Sundberg (1995)

Field

corr

nat

No

Yes, cuck

Sundberg and Dixon (1996)

Lab Field

corr corr

None None

Yes No

No, ap Yes, ps

Johnson et al. (1993) Price (1984)

Field

corr

None

No

Thusius et al. (2001)

Lab

corr

None

Yes

Yes, ps, cuck No, ap

Senar et al. (2005)

Field

corr

None

No

Yes, ps, ed

Norris (1990a)

Table 4.1. (continued) Color mechanism or type

Phaeomelanin plumage

Multiple sources of UV

Species

Trait a

Typeb

Variablec

Descriptord

House Sparrow (Passer domesticus) House Sparrow House Sparrow House Sparrow House Sparrow House Sparrow House Sparrow House Sparrow House Sparrow House Sparrow Kentish Plover (Charadrius alexandrinus) Medium Ground Finch (Geospiza fortis) Northern Cardinal Pied Flycatcher (Ficedula hypoleuca) Pied Flycatcher Pied Flycatcher Pied Flycatcher Pied Flycatcher Pied Flycatcher Pied Flycatcher Pied Flycatcher Pied Flycatcher

plum

eu

pz

size

plum plum plum plum plum plum plum plum plum plum

eu eu eu eu eu eu eu eu eu eu

pz pz pz pz pz pz pz pz pz pz

size size size size size size size size size size

plum

eu

pz

size

plum plum

eu eu

pz cq

size br

plum plum plum plum plum plum plum plum

eu eu eu eu eu eu eu eu

cq cq cq cq cq cq cq cq

br br br br br br br br

plum

phae

cq

comp

plum

phae

pz

size

plum

phae

pz

size

plum

phae

cq

comp

plum

phae

cq

comp

plum

phae

cq/pz

comp

plum

phae

cq

comp

plum plum

phae phae

cq pz

comp size

all

mult

cq

uvchr

Barn Swallow (Hirundo rustica) Chestnut-sided Warbler (Dendroica pensylvanica) Eastern Bluebird (Sialia sialis) European Kestrel (Falco tinnunculus) Mallard (Anas platyrhynchos) Orchard Oriole (Icterus spurius) Red Junglefowl (Gallus gallus) Red Junglefowl Yellow Warbler (Dendroica petechia) Blue Tit (Parus caeruleus)

Field/lab

Experimental or corre

Color manipulationf

Control for dominance?

Choice for elaborate color?g

Reference

Lab

exp

nat

Yes

Yes, cd

Møller (1988)

Field Field Lab Field Lab Field Field Field Field Field

corr corr corr corr exp corr corr corr corr exp

nat nat None None nat None None None None nat

No No No No Yes No No No No No

Yes, ps Yes, cuck Yes, cop Yes, ps No, ap No, ps No, cuck No, cuck Yes, ps No, ps

Møller (1988) Møller (1988) Riters et al. (2004) Kimball (1997) Kimball (1996) Veiga (1993) Cordero et al. (1999) Whitekiller et al. (2000) Griffith et al. (1999) Lendvai et al. (2004)

Field

corr

None

No

Yes, ps

Price (1984)

Lab Field

corr corr

None None

Yes No

No, am No, ps

Jawor et al. (2003) Alatalo et al. (1984)

Field Field Field Field Field Lab Field Field

corr corr corr corr corr exp corr corr

None None None None None nat None None

No No No No No Yes Yes No

No, ps Yes, ps Yes/no, ps No, ps Yes, ps Yes, nb Yes, ps No, cuck

Slagsvold (1986) Järvi et al. (1987) Lifjeld and Slagsvold (1988) Dale and Slagsvold (1990) Dale and Slagsvold (1996) Sætre et al. (1994) Sætre et al. (1994) Lifjeld et al. (1987)

Field

corr

None

No

Yes, am, ed

Safran and McGraw (2004)

Field

corr

None

No

Yes, ed

King et al. (2001)

Field

corr

None

No

Yes, ed

Siefferman and Hill (2003)

Lab

corr

None

Yes

Yes, ap

Palokangas et al. (1994)

Lab

exp

clip

Yes

Yes, ps

Omland (1996a)

Lab

corr

None

Yes

Yes, ap

Enstrom (1993)

Lab

exp

gene

Yes

No, cop

Ligon and Zwartjes (1995)

Lab Field

corr corr

None None

Yes No

Yes, cop Yes, cuck

Zuk et al. (1990) Yezerinac and Weaherhead (1997)

Lab

exp

fil

Yes

Yes, ap

Hunt et al. (1999)

Table 4.1. (continued) Color mechanism or type

Coherent structural plumage

Incoherent (white) structural

Species

Trait a

Typeb

Variablec

Descriptord

Budgerigar (Melopsittacus undulatus) European Starling (Sturnus vulgaris) Red-billed Leiothrix (Leiothrix lutea) Zebra Finch (Taeniopygia guttata)

all

mult

cq

uvchr

all

mult

cq

uvchr

all

mult

cq

uvchr

all

mult

cq

uvchr

Barn Swallow Blue Grosbeak (Passerina caerulea) Blue Grosbeak Blue Tit Blue Tit Blue Tit Bluethroat (Luscinia svecica) Bluethroat Eastern Bluebird European Starling Mallard Northern Pintail (Anas acuta) Pied Flycatcher Purple Martin (Progne subis) Pinyon Jay (Gymnorhinus cyanocephalus) Ring-necked Pheasant (Phasianus colchicus) Superb Fairy-wren (Malurus cyaneus)

plum plum

str str

cq cq

uvchr uvchr

plum plum plum plum plum

str str str str str

cq cq cq cq cq

comp uvchr uvchr hue uvchr

plum plum plum plum plum

str str str str str

cq cq cq cq cq

uvchr comp uvchr comp nomea

plum plum

str str

cq cq

uvchr nomea

plum

str

cq

comp

plum

str

cq

nomea

plum

str

pz

size

Barn Swallow Black-capped Chickadee (Poecile atricapillus) Black-capped Chickadee Collared Flycatcher (Ficedula albicollis) Dark-eyed Junco (Junco hyemalis) Great Snipe (Gallinago media) Great Snipe Northern Pintail

plum plum

wh wh

pz cq

size br

plum plum

wh wh

cq pz

br size

plum

wh

pz

size

plum

wh

pz

size

plum plum

wh wh

pz cq

size nomea

Field/lab

Experimental or corre

Color manipulationf

Control for dominance?

Choice for elaborate color?g

Reference

Lab

exp

fil

Yes

Yes, ap

Pearn et al. (2001)

Lab

exp

fil

Yes

Yes, ap

Bennett et al. (1997)

Lab

exp

fil

Yes

Yes, ap

Maier (1993)

Lab

exp

fil

Yes

Yes, ap

Bennett et al. (1996); Hunt et al. (1997)

Field Lab

corr exp

None nat

No Yes

No, ed, ps No, ap

Perrier et al. (2002) Ballentine and Hill (2003)

Field Field Field Field Lab

corr corr exp corr exp

nat None sun None sun

No No No No Yes

Yes, cuck Yes, am Yes, sexr Yes, cuck Yes, ap

Field Field Lab Lab Lab

exp corr corr exp exp

sun None None clip nat

Yes No Yes Yes Yes

Yes, ps, Yes, ed Yes, ap Yes/no, ps Yes, ps

Estep et al. (2005) Andersson et al. (1998) Sheldon et al. (1999) Delhey et al. (2003) Andersson and Amundsen (1997) Johnsen et al. (1998) Siefferman and Hill (2003) Bennett et al. (1997) Omland (1996a) Sorenson and Derrickson (1994)

Lab Field

exp exp

sun black

Yes No

Yes, nb No,ps

Siitari et al. (2002) Stutchbury (1991)

Lab

corr

None

Yes

Yes, ap

Johnson (1988)

Lab

exp

nat?

Yes

No, cd

Mateos and Carranza (1995)

Field

corr

None

No

Yes, cuck

Dunn and Cockburn (1999)

Field Field

exp corr

nat nat

No No

Yes, ps, ed Yes, cuck

Kose and Møller (1999) Doucet et al. (2005)

Lab Field

exp corr

nat None

Yes No

Yes, ps Yes, ps

Woodcock et al. (in press) Gustafsson et al. (1995)

Lab

exp

nat

No

No, ap

Hill et al. (1999a)

Field

exp

nat

No

Yes, ps

Höglund et al. (1990)

Field Lab

corr exp

None nat

No Yes

No, ps Yes, ps

Sæther et al. (2000) Sorenson and Derrickson (1994)

Table 4.1. (continued) Color mechanism or type

Species

Trait a

Typeb

Variablec

Descriptord

Pied Flycatcher Pied Flycatcher

plum plum

wh wh

pz pz

size size

Fluorescent plumage

Budgerigar Budgerigar

plum plum

fluor fluor

cq cq

uvchr uvchr

Unknown penguin

King Penguin (Aptenodytes patagonicus) King Penguin Yellow-eyed Penguin (Megadyptes antipodes)

plum

png

pz

size

plum plum

png png

pz cq

size hue

Psittacifulvin plumage

Burrowing Parrot (Cyanoliseus patagonus)

plum

psit

pz

size

Bare part coloration

American Goldfinch Blue-footed Booby (Sula nebouxii) Double-bar Finch (Taeniopygia bichenovii) Eurasian Blackbird (Turdus merula) Great Frigatebird (Fregata minor) Zebra Finch

leg oth

None str, car

cq cq

hue hue

leg

mel, str

cq

hue

bill

car

cq

comp

oth

hem?

cq

sat

leg

car

cq

hue

Zebra Finch Zebra Finch Zebra Finch Zebra Finch Zebra Finch Zebra Finch Zebra Finch Mallard Ring-necked Pheasant

leg bill bill bill bill bill bill bill oth

car car car car car car car car hem?

cq cq cq cq cq cq cq cq cq

hue hue hue hue hue hue hue comp sat

Common Buzzard (Buteo buteo) Gouldian Finch (Chloebia gouldiae) Parasitic Jaeger (Stercorarius parasiticus) Parasitic Jaeger

plum

mel

mph

mph

plum

mph

mph

plum

car, mel mel

mph

mph

plum

mel

mph

mph

plum

mel

mph

mph

Polymorphic plumage

Snow Goose (Chen caerulescens)

Field/lab

Experimental or corre

Color manipulationf

Control for dominance?

Choice for elaborate color?g

Reference

Field Field

corr exp

None nat

No No

Yes, ps No, ps

Potti and Montalvo (1991) Dale et al. (1999)

Lab Lab

exp exp

fil sun

Yes Yes

No, ap Yes, ap

Pearn et al. (2001) Arnold et al. (2002)

Field

exp

black

No

Yes, ps

Jouventin (1984)

Field Field

exp corr

Nat None

No No

Yes, ps Yes, am

Jouventin et al. (2005) Massaro et al. (2003)

Field

corr

None

No

Yes, ps

Masello and Quillfeldt (2003)

Lab Field

exp exp

legb nat

Yes No

Yes, ap Yes, ps

Johnson et al. (1993) Torres and Velando (2003)

Lab

exp

legb

Yes

Yes, ap

Burley (1986)

Field

corr

None

No

No, ed

Faivre et al. (2001)

Field

corr

None

No

No, ed

Dearborn and Ryan (2002)

Lab

exp

legb

Yes

Yes, ap, sexr

Field Lab Lab Lab Lab Lab Lab Lab Lab

exp exp corr corr corr exp exp corr corr

legb nat None None None nat nat None None

Yes No No No No No No No Yes

Yes, ap Yes, ap Yes, ap Yes, ap No, ap No, ap No, ap Yes, ps No, cd

Burley (1981); Burley et al. (1982) Burley et al. (1988) Burley and Coopersmith (1987) De Kogel and Prijs (1996) Blount et al. (2003) Collins et al. (1994) Sullivan (1994) Weisman et al. (1994) Omland (1996b) Mateos and Carranza (1995)

Field

corr

None

No

Yes, am

Kruger et al. (2001)

Lab

corr

None

Yes

No, ps

Fox et al. (2002)

Field

corr

None

No

Yes, ps, am

O’Donald (1980, 1983)

Field

corr

None

No

Phillips and Furness (1998)

Field

corr

None

No

Yes, am, no, am Yes, am

Cooch and Beardmore (1959)

geoffrey e. hill

148 Table 4.1. (continued) Color mechanism or type

Color symmetry

Species

Trait a

Typeb

Variablec

Descriptord

White-throated Sparrow (Zonotrichia albicollis) White-throated Sparrow

plum

mel

mph

mph

plum

mel

mph

mph

Bluethroat House Finch House Finch Rufous Bush Chat (Cercotrichas galactotes) Common Shelduck (Tadorna tadorna) Zebra Finch Zebra Finch Zebra Finch

leg plum plum plum

None car car eu, wh phae, wh mel car car

cs cs pz, cs cs

sym sym sym sym

imm

imm

cs cs cs

sym sym sym

plum plum leg leg

a. Colored trait under study: plum = plumage, leg = leg, bill = bill, oth = other bare part, all = entire body. b. Type of color: car = carotenoid; eu = eumelanin; phae = phaeomelanin; mel = melanin; str = structural; wh = white structural; psit = psittacofulvin; por = porphyrin; fluor = florescence; hem = hemoglobin; none = artificial color added; mult = multiple color types; pgn = unknown penguin pigment. c. Color variable measured: cq, color quality; pz, patch size; mph, morph; cs, color symmetry; ps, patch symmetry; imm, immaculateness. d. Color descriptor used: size = size of colored area; hue = hue; sat = chroma or saturation; br = brightness; comp = composite color variable; uvchr = ultraviolet (UV) chroma; nomea = no color measurements taken; sym = symmetry; mph = morph; imm = immaculateness. e. Color manipulated or correlations with natural coloration used: exp, experimental; corr, correlative. f. Type of color manipulaltion: nat = painted or dyed within natural variation; legb = colored leg bands; clip = feathers clipped; black = color covered with black; sun = UV color blocked with sunscreen; fil = UV color blocked with UV filter; gene = mutation for loss of color trait. g. Choice for elaborate color: ap = association preference; cd = copulation display; nb = nest building; ps = pairing success; am = assortative pairing; cop = copulation; ed = first egg date; cuck = cuckoldry rate and extra-pair mating; sexr = change in offspring sex ratio.

In the lab, females can be presented with males displaying natural variation in coloration, but as in field studies, there remains the possibility that the choice is really for a trait correlated to the color display and not for the color display per se. Alternatively, coloration can be manipulated, breaking links between the color trait and any correlated traits. Finally, to eliminate the effects of male-male competition in lab studies, males can be housed in individual compartments to eliminate direct contact, but then females usually do not have physical access to potential mates and cannot copulate with them. In many studies, because females do not have physical access to males, the time in as-

Female Mate Choice for Ornamental Coloration

149

Field/lab

Experimental or corre

Color manipulationf

Control for dominance?

Choice for elaborate color?g

Reference

Field

corr

None

No

Yes, am

Knapton and Falls (1983)

Lab

corr

None

Yes

No, ps

Houtman and Falls (1994)

Field Field Field Fiel

exp corr corr corr

legb None None None

No No No No

Yes, ps Yes, ps Yes, ps Yes, ps

Fiske and Amundsen (1997) Hill et al. (1999a) Badyaev et al. (2001) Alvarez (2000)

Field

corr

None

No

Yes, ps

Ferns and Lang (2003)

Lab Lab Lab

exp exp exp

nat legb legb

Yes Yes Yes

Yes, ap Yes, ap Yes, ap

Swaddle and Cuthill (1994a) Swaddle and Cuthill (1994b) Bennett et al. (1996)

sociation with males is taken as a measure of female choice. More convincing are experiments in which females solicit copulations with unambiguous behaviors or initiate nests in front of a preferred male. The best circumstances for captive mate choice experiments are when males are tethered and hence kept from interacting, but females have full physical access to the males and can mate with them. This design works with large birds, such as Wild Turkeys (Meleagris gallopavo) and Red Junglefowl (Gallus gallus), but not with small birds, such as songbirds. The downside of lab studies is that animals are removed from their natural habitat, which can alter mating behaviors. All approaches to testing mate choice have strengths and weaknesses. Lab studies are not fundamentally better than field studies or vice versa. The best overall approach is to study mate choice in the lab and in the field, assessing natural correlations and conducting controlled experiments. If such a multifaceted approach leads to a consensus regarding mate choice for a color display, then the result can be considered robust.

Mate Choice and Carotenoid Pigmentation Early Studies The first avian studies of carotenoid coloration using color manipulation were conducted on the Red-winged Blackbird (Agelaius phoeniceus; Plate 11) by Peek

150

geoffrey e. hill

Box 4.1. Definitive Mate Choice Experiments with Fish In the early 1980s, Endler (1980, 1982, 1983) pioneered a new approach to the study of ornamental coloration in animals. He looked at the influence of female mate choice as well as predation, background matching, and light environment on the maintenance and evolution of color displays. Endler conducted his research on Guppies (Poecilia reticulata), a species of fish in which males have bright carotenoid-, melanin-, and structurally based skin coloration. He presented correlative evidence that females used the carotenoid coloration of males as a criterion in mate choice (Endler 1983). He also conducted an experiment in which he tested female mate preference for males with more red or blue spots. The results of this experiment showed that males that stand out from their background color had a mating advantage (Endler 1983), but both Endler’s correlative and experimental studies were hard to interpret for the overall importance of blue or orange coloration to female mate choice. Endler’s Guppy studies were tremendously influential on studies of avian coloration. First, they framed questions related to ornamental coloration in explicit evolutionary terms. Second, they pointed out the importance of considering different types of ornamental coloration (carotenoid, melanin, and structural coloration) as fundamentally different traits. Third, and perhaps most importantly, for the first time they focused on naturally occurring variation in male coloration. Endler’s studies stimulated increased interest particularly in carotenoid-based ornamental coloration and they established Guppies as the premier study organism for investigations of ornamental coloration. In the studies of Guppies that shortly followed Endler’s work, definitive and detailed evidence for female mate choice relative to male carotenoid coloration was established (Kodric-Brown 1985, 1989; Houde 1987). The bird literature on mate choice and carotenoid coloration still pales (no pun intended) in comparison with the fish literature. Numerous studies of fish have since corroborated the importance of both the size and color of carotenoid spots in female mate choice (Guppy: Kodric-Brown 1989; Long and Houde 1989; Houde and Torio 1992; Nicoletto 1993; Brooks and Caithness 1995; Kodric-Brown and Nicoletto 1996, 1997; Nicoletto and Kodric-Brown 1999; Grether 2000; Three-spined Stickleback: McLennan

Female Mate Choice for Ornamental Coloration

and McPhail 1989; Milinski and Bakker 1990, 1992; Bakker and Milinski 1991; McLennan 1991; Bakker and Mundwiler 1994; Kunzler and Bakker 2001; salmon: Craig and Foote 2001; Damselfish [Chrysiptera cyanea]: Gronell, 1989; Tail Spot Wrasse [Halichoeres melanurus]: Kuwamura et al. 2000; killifish [Nothobranchius guentheri ]: Haas 1976; and Upland Bully [Gobiomorphus breviceps]: Hamilton and Poulin 1999).

(1972) and Smith (1972). In both studies, researchers covered the bright red epaulets of wild males with black shoe polish and observed the effect of the manipulations on territory defense and mate attraction. In both studies, blackening of the epaulets caused males to be less effective at holding territories, and Peek (1972) but not Smith (1972) also found what he thought was weak evidence that males with blackened epaulets had more difficulty in attracting females than normally colored males. Collias et al. (1979) carried out another plumage-blackening experiment on captive Village Weaverbirds (Ploceus cucullatus) and observed that yellow males were more successful at attracting mates than were males with blackened plumage. These color-removal experiments suggested that female birds do pay attention to male plumage coloration during mate choice. Feather-blackening experiments could not, however, address the more interesting issue of female choice relative to natural variation among males in the expression of ornamental coloration (see below), because color was manipulated outside the range of natural variation (Plate 10). Zebra Finch Band Colors Early studies of carotenoid-based coloration in birds lagged behind studies of carotenoid-based coloration in fish (Box 4.1). One important exception is a series of studies by Burley and colleagues on leg coloration of Zebra Finches (Taeniopygia guttata), which were conducted at the same time as many of the studies of fish coloration in the early 1980s. In an aviary study of parental behavior, Burley noticed that male Zebra Finches with pink or red leg bands paired and bred at a higher rate than did males with light green leg bands (Burley et al. 1982; Figure 4.1). In subsequent mate choice experiments that eliminated male-male competition and controlled for correlated effects of leg color by switching the bands of stimulus males between each trial, Burley et al.

151

geoffrey e. hill

152

female

male

Average within-trial rank

4

3 mean score 2

1 red

orange

green

no band

Band color

Figure 4.1. Mean preference rankings by domestic male and female Zebra Finches in response to potential mates with red, orange, green, or no leg bands. Both males and females showed nonrandom patterns of association (p < 0.001, Friedman’s Test), with females showing a significant preference for red-banded males (p < 0.05) and males showing equal preference for red-banded and unbanded females (p < 0.05). Redrawn from Burley et al. (1982).

showed that females in breeding condition preferred to associate with males banded with red bands, and females spent the least time in proximity to males with green bands. Orange-banded and unbanded males were equally preferred over green-banded males (Burley et al. 1982). They also showed that females paired to red-banded males produced more sons, which was interpreted as further evidence that red-banded males were viewed by females as being desirable mates worthy of above-average resource investment (Burley 1981). These patterns of female mate preference for males wearing redder leg bands were also observed in wild-caught Zebra Finches (Burley 1988). Choice for plastic bands on the legs of Zebra Finches seems like a preference for arbitrary and novel ornamental traits, but Zebra Finches have orange-red legs and bills that are colored with carotenoid pigments (McGraw et al. 2002; Plate 18), and it seems reasonable to interpret the leg-band manipulations as enhancing or diminishing natural bare-part coloration. In support of the idea that manipulation of leg band color is perceived by birds as manipulation of leg color, when Burley (1986) tested the mate preferences of female Double-bar Finches (Taeniopygia bichenovii), which is a sister species of the Zebra Finch but with bluegray bills and legs and no red or orange (Plate 16), they preferred males with blue bands over wild type or red-banded males (see also Johnson et al. 1993).

Female Mate Choice for Ornamental Coloration

The studies on leg-band color by Burley and colleagues were extremely influential because they provided the first well-controlled experimental demonstrations of mate choice for a color display in birds in which male-male competition was eliminated. It would be interesting to conduct follow-up studies on Zebra Finches in which, rather than using blue, green, and red leg bands, researchers used leg bands that spanned a natural range of leg coloration. Such a study would help put the classic work of Burley and colleagues into a more natural context. Carotenoid-Based Plumage Coloration The first carefully controlled experimental studies of female mate choice relative to carotenoid-based plumage coloration were conducted by Hill in the early 1990s on House Finches (Carpodacus mexicanus), a cardueline finch in which males have carotenoid pigmentation on their crowns, breasts, and rumps (Plate 14). It had long been noted that male House Finches are extremely variable in expression of ornamental plumage (Keeler 1893; Grinnell 1911). Using a choice design like that employed by Burley et al. (1982) in their study of leg color in Zebra Finches, Hill (1990, 1994) gave wild-caught, captive female House Finches a choice of males with a full range of natural variation in plumage coloration. For these experiments, he assigned males to color groups by controlling their access to carotenoid pigments during molt (see Chapter 12, Volume 1; Plate 31, Volume 1). In a series of experiments, females in breeding condition preferred to associate with males with redder and more saturated plumage (Hill 1990, 1994; Figure 4.2). Female preference for the extent of red carotenoid pigmentation on the underside of males (patch size) was also tested in the lab, and females were found to prefer large-patched over small-patched males (Figure 4.2). When forced to choose between males with large drab or small bright patches, however, females chose small bright patches (Hill 1994; Figure 4.2). Thus plumage redness and saturation seemed to be the primary criteria in female choice in the House Finch, and patch size served as a secondary choice criterion. These studies of mate selection in the House Finch were convincing in that they involved manipulated color and controlled for male-male interactions, but female mate choice was assessed by time in proximity and not by mating behavior per se. Results from field studies of House Finches corroborated observations with captive birds. In two populations from eastern North America (Michigan and Alabama), males that formed social pairs with females had redder plumage hues

153

geoffrey e. hill

154

Mean preference rank

a

b

3

2

1 yellow

orange

red/ orange

red

small drab

large drab

small bright

large bright

Plumage color and patch size of stimulus male

Figure 4.2. Mean (± standard error) preference ranks of male House Finch phenotypes presented to wild-caught female House Finches during aviary mate-choice trials. (a) Females were given a choice among males that were experimentally manipulated to vary in plumage hue from yellow to red. Females showed a significant preference for red males. (b) Females were given a choice among males with patches that were either large or small and either drab or bright. They showed a preference for large and bright patches over any other combination. Redrawn from Hill (1990, 1994).

than males that did not pair (Hill 1990; Hill et al. 1999a). A field experiment also showed that a higher proportion of males with red dye added to plumage paired than did sham-treated males or those whose plumage was made drabber with hair lightener (Hill 1991; Plate 14). A study of paternity in the same population, however, failed to find a relationship between rates of cuckoldry and male plumage coloration (Hill et al. 1994), suggesting that carotenoid coloration may be less important for female House Finches choosing extrapair mates. These field studies failed to control for male-male interactions, but Hill (1991) argued that male-male interactions did not affect pair formation in this nonterritorial species. Taken together, the laboratory and field studies of House Finches present convincing evidence for female choice relative to male carotenoid coloration. Experimental aviary studies of a few other species of passerine birds support the idea that females prefer to mate with males that have redder or more intense carotenoid displays. In an aviary mate choice experiment in which male coloration was manipulated, Senar et al. (2005) showed that female Eurasian

Female Mate Choice for Ornamental Coloration

Siskins (Carduelis spinus; Plate 12) prefer males with larger patches of yellow carotenoid pigmentation in their wings. Sundberg (1995) conducted mate choice trials in the lab with Yellowhammers (Emberiza citrinella), a sexually dichromatic emberizid sparrow in which males have bright yellow carotenoidbased coloration over much of their plumage (Plate 15). He implanted females with estradiol to bring them into reproductive condition and presented them with stuffed male models. In one experiment, a naturally drab and a naturally bright male were presented to the female; in the second experiment, dummy males were made more or less colorful by coloring their plumage with a marker or by clipping brown feathers that covered bright yellow feathers. Thus the males in the “yellow” group had both more intense yellow coloration and larger patches of yellow, and males in the “drab” group had smaller and less intense yellow patches. Sundberg (1995) found that females spent significantly more time in association with yellow than with drab males (Figure 4.3). This study is particularly convincing because, by using stuffed models as stimulus birds, it removed all potential complications with behavior (including song) and male condition. In a companion field study, Sundberg and Dixon (1996) found the extent of yellow coloration in the plumage did not affect a male’s risk of being cuckolded, but the males that sired extra-pair young had more extensive yellow coloration than average breeding males. Other aviary studies of mate choice and carotenoid coloration have relied on natural variation in coloration. Karubian (2002) conducted an aviary mate choice experiment with Red-backed Fairy-wrens (Malurus melanocephalus) in which first-year males vary from having brilliant black-and-scarlet plumage like adult males to having drab female-like plumage. He gave females a choice between bright or drab first-year males, and females showed a preference for brightly colored males. This preference could have been a choice for either red carotenoid or black eumelanin-predominated pigmentation. In an aviary experiment with American Goldfinches (Carduelis tristis), a sexually dichromatic species in which the beak and body plumage of males has bright orange and yellow coloration, respectively, Johnson et al. (1993) also observed female preference for brightly colored males. Female goldfinches spent more time and performed more courtship behaviors in front of males with more intensely pigmented bills and feathers versus drabber males. With no manipulations of color, however, there is no way to rule out choice for a trait correlated with plumage coloration rather than plumage color per se. Only one aviary experiment testing for mate choice relative to carotenoidbased plumage coloration has failed to support the idea the female birds use

155

geoffrey e. hill

156

Mean time (min)

15

10

5

0 yellow

drab

Plumage color of male

Figure 4.3. Mean (± standard deviation) time spent by hormone-induced female Yellowhammers on a perch in front of stuffed skins of male Yellowhammers that were painted to be either drab or bright yellow. Females spent significantly more time near the yellow males ( p < 0.05). Drawn from data in Sundberg (1995).

expression of carotenoid coloration as a criterion in mate selection. Wolfenbarger (1999a) tested mate preferences of female Northern Cardinals (Cardinalis cardinalis; Plate 25) in aviaries using both natural variation in male carotenoid coloration and variation created by coloring feathers with hair dye. She found no tendency for females to associate with more brightly colored males. Correlative field studies of Northern Cardinals, however, suggest that carotenoid coloration is a criterion in mate choice in the wild (Wolfenbarger 1999b; Jawor et al. 2003). More studies of mate preferences in Northern Cardinals are needed. Correlational field studies have generally, but certainly not universally (e.g., Bjorklund 1990), supported the hypothesis that carotenoid coloration is used by females to choose mates. In a field study of American Goldfinches, MacDougall and Montgomerie (2003) found assortative mating by yellow coloration, based on a composite brightness score, suggesting that both males and female goldfinches use expression of carotenoid-based feather coloration as a

Female Mate Choice for Ornamental Coloration

basis for mate choice. Marchetti (1998) looked at the relationship between pairing success and natural variation in the size of yellow wing bars in the Yellowbrowed Leaf Warbler (Phylloscopus inornatus). The drab yellowish coloration of wing bars is presumably due to carotenoid pigments, but this assumption has not been tested. Marchetti (1998) found that males with larger patches of yellow bred earlier than did males with smaller color patches. However, she subsequently manipulated the size of the yellow patches with paint, and males with larger natural yellow patches still bred earlier, regardless of whether their patches were made larger or smaller. This latter observation suggests that females were not assessing patch size per se, but rather were attracted to males with large patches for other reasons, such as better physical condition. As described previously, in two House Finch populations in eastern North America, paired males were significantly more colorful than unpaired males (Hill 1990, 1994), and males with redder and more saturated plumage coloration nested earlier than males with drabber plumage (Hill et al. 1994, 1999a; McGraw et al. 2001). In a Montana population of House Finches, however, the patterns of mate choice were more complex. The size and symmetry of red patches were better predictors of pairing success than were hue or saturation of the red patch (Badyaev et al. 2001), and it appeared to be primarily young females who chose redder males (Badyaev and Hill 2002). The differences in female mate preferences between Montana and eastern populations of House Finches underscores that female preferences can change with context, as the signal content of different choice criteria change. Such changes can potentially occur both spatially, as in the case of House Finches, or temporally, although the latter has yet to be shown. The most detailed field studies of carotenoid coloration that have failed to find evidence for female mate choice were conducted on Red-collared (Euplectes ardens) and Red-shouldered Widowbirds (E. axillaris). Pryke et al. (2001a) found that tail length was a strong predictor of male reproductive success in Red-collared Widowbirds, but that neither the size nor the hue, chroma, or brightness of the carotenoid-containing red collar were related to male reproductive success. In a field experiment in which they manipulated the color and size of the wing epaulets of Red-shouldered Widowbirds, Pryke and Andersson (2003) found no effect of color treatment on the rate at which females visited males or settled in their territories. For both the Red-collared and Red-shouldered Widowbirds, these authors presented convincing evidence that the primary function of red coloration was intrasexual signaling (Pryke et al. 2001b; Pryke and Andersson 2003).

157

geoffrey e. hill

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Taken together, studies of plumage coloration, and in particular lab and field experiments in which plumage coloration was manipulated, demonstrate that in some species of birds, females use expression of male carotenoid coloration as an important criterion in mate choice. The available evidence suggests that female mate choice based on expression of carotenoid coloration is widespread among passerine birds, but there are several convincing studies in which expression of coloration was found to have no effect on female choice. Mate choice for carotenoid coloration outside of passerines is virtually unstudied. These patterns emerging from studies of songbirds are consistent with studies of fish in which carotenoid coloration also commonly serves as a criterion in mate selection (Box 4.1). In many species of songbirds, expression of carotenoid coloration has been shown to be dependent on key aspects of individual condition, including history of parasite infection and foraging success (Chapter 12, Volume 1), and in such species, females would choose males in good condition by choosing males with elaborate expression of carotenoid pigmentation (Chapter 6).

Melanin Coloration As reviewed in Chapter 6 in Volume 1, there are two classes of melanin pigments —eumelanins and phaeomelanins—that are synthesized via different pathways and that produce different feather coloration. Although both types of pigments are present in all of the melanin-based plumage colors that have been studied biochemically to date, black coloration is characteristically eumelanindominated and brown/rufous coloration is phaeomelanin-dominated. Thus I refer to black color displays as eumelanin and brown and rufous color displays as phaeomelanin in this chapter. The majority of research on female mate choice relative to melanin pigmentation has been conducted on black eumelanin coloration. There are fewer published studies on mate choice relative to reddish phaeomelanin pigmentation, but this is a topic of growing interest. Eumelanin Plumage Studies Female mate choice relative to eumelanin ornaments has been studied extensively in several bird species, but studies on the Pied Flycatcher (Ficedula hypoleuca) and the House Sparrow (Passer domesticus) comprise the majority of the literature. The studies focused on the plumage coloration of Pied Flycatchers were among the first studies of mate choice in birds, and a long pro-

Female Mate Choice for Ornamental Coloration

gression of papers has been produced on the topic. Male Pied Flycatchers typically have bold black-and-white plumage (Plate 27, Volume 1), but some males have drab brown feathers in place of black feathers. This variation in plumage blackness is closely tied to age—yearling males tend to have more extensive brown coloration and older males tend to be mostly or entirely black and white ( Järvi et al. 1987; Lundberg and Alatalo 1992). Such age-dependent coloration makes it hard to disentangle effects of age from effects of coloration per se. In a correlative field study that was the first to consider female choice relative to plumage coloration in the Pied Flycatcher, Alatalo et al. (1984) found no evidence for female choice of males based on plumage blackness when controlling for age. Soon thereafter, Slagsvold (1986) conducted an experiment in which he manipulated nest-box quality and then looked at female settlement patterns relative to male plumage coloration and nest-box quality. He observed that females chose good nest sites regardless of the appearance of males, and he too concluded that there was no convincing evidence that females used the melanin coloration of males to select mates. Järvi et al. (1987) later found that males with blacker plumage paired earlier, suggesting that they were preferred by females, but blacker males also had better territories and nest boxes. In a 2-year field study, Lifjeld and Slagsvold (1988) found that male pairing success was positively correlated with plumage blackness in one year but not the other, but no attempt was made to account for age in this study. Dale and Slagsvold (1990) looked at settlement pattern in relation to a variety of male and territory characteristics and concluded that the most consistent model was random female settlement and choice of partner. Several years later, with more detailed data on the sampling behavior of females, the same authors concluded that females based their choice of mates on male mating status, plumage blackness, and box quality, in that order (Dale and Slagsvold 1996). The first definitive evidence that female Pied Flycatchers use plumage blackness as a criterion in mate choice was published by Sætre et al. (1994). They conducted an aviary study with birds from Norway in which they manipulated the plumage coloration of males, thus uncoupling any potential correlated effects of age or condition. In controlled experiments that eliminated male dominance interactions, they showed that females initiated nests significantly more often in association with blacker males (Figure 4.4). They also tested the preferences of females when they were presented with males with natural variation in plumage coloration and again showed that females chose blacker males. They confirmed their lab results in the field by following mate-searching

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Figure 4.4. Number of wild-caught female Pied Flycatchers that initiated nests with males in an aviary. (a) Choice in relation to males that were naturally black and white (bright) or brown and white (dull). (b) Choice in relation to dull males that were painted to be black and white or that remained brown and white. Redrawn from Sætre et al. (1994).

females in a wild population and showing that the color of accepted males was darker than the color of rejected males. Interestingly, a study of extra-pair paternity in the same population of Pied Flycatchers revealed that blacker males were cuckolded more than browner males, which suggests that feather blackness was not an important criterion in choice of extra pair mates in this species (Lifjeld et al. 1987). Although the study of Sætre et al. (1994) showed conclusively that male plumage blackness can be an important criterion in female mate choice, it does not negate the many studies of mate choice in Pied Flycatchers that preceded it and that found no effect of plumage color on mate choice. Indeed, it seems that in many populations of Pied Flycatchers, females select a breeding site and choose a mate based on resource quality, not male coloration, and that plumage blackness aids males in holding territories with better resources (see Chapter 3). The cuckoldry data mentioned above remain difficult to explain, but in choosing extra-pair mates, female Pied Flycatchers may focus on genetic complementarity or male heterozygosity (Mays and Hill 2004). Behavioral ecologists have also long been interested in whether female House Sparrows select mates based on the variably sized black throat patch of males (Plate 23, Volume 1). This badge is expressed largely independent of age

Female Mate Choice for Ornamental Coloration

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Figure 4.5. Mean (± standard error) badge scores of male House Sparrows that were mated or unmated during weekly spring surveys of a free-living wild population in Denmark in 1985. Redrawn from Møller (1988).

(Møller 1987) and varies little in darkness among individuals. In the first study of mate choice in House Sparrows, Møller (1988) presented captive females in reproductive condition from a Danish population with taxidermy mounts of males that either had large or small black patches. Females performed significantly more displays soliciting copulations in front of large-patched models than in front of small-patched models. In the same paper, using field observations of House Sparrows in Denmark, he reported that large-patched males paired faster than small-patched males and that throughout the early nesting period the mean patch size of unpaired males was significantly smaller than that of paired males (Figure 4.5). Møller (1990b) also reported that largepatched males were more often accepted as extra-pair partners than were smallpatched males. In another study of captive House Sparrows, Riters et al. (2004) found a significant positive relationship between male badge size and the number of times a male was approached by a receptive female. In this study, the researchers controlled for dominance statistically rather than experimentally. In a field study in New Mexico, Kimball (1997) observed that larger-patched male House Sparrows obtained mates sooner and had higher reproductive success than did smaller-patched males.

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geoffrey e. hill Other studies of House Sparrows have failed to observe female mate choice for larger-patched males. In laboratory mate choice experiments using birds from New Mexico, Kimball (1996) found no evidence of female preferences for larger-patched males. In field studies in Spain, Veiga (1993) found no effect of enlarged or reduced badge size on pairing success, but this conclusion was based on a small number of observations. In paternity analyses conducted on broods of House Sparrows from British, Spanish, and central North American populations, large-patched and small-patched males were cuckolded at the same rate (Cordero et al. 1999; Whitekiller et al. 2000), which could be interpreted as lack of female preference for larger-patched males (Griffith et al. 1999). Finally, Griffith et al. (1999) observed that in a wild population on the small British island of Lundy, small-patched males were more likely to obtain a mate and to be polygynous than were larger-patched males. Smallerpatched males also had higher reproductive success. All of these studies, except the experimental mate choice experiments of Møller (1988) and Kimball (1996), are based on correlative field data, however, from which it is impossible to be certain that the patterns of apparent female choice were not actually the result of male badge size affecting nest box quality or retention of other resources on which female choice was actually based (see Kimball 1996). Overall, there appears to be variation across years and among populations of House Sparrows in whether females use male badge size in mate choice, as well as in what sort of badge—large or small—they find attractive. Such variation in mate choice may be linked to the relative value of choice criteria and the aspects of mate quality they signal under fluctuating environmental conditions. Male Great Tits (Parus major) have black breast stripes that vary in width (Plate 11) and are much reduced in females. In a correlative analyses of field observations, Norris (1990a) observed that male Great Tits with broader breast bands paired with females that laid larger clutches and that, in one of three years, initiated nesting earlier. He found no relationship between breastband size and territory quality and concluded that it was likely that female mate choice was responsible for the pattern. However, several studies have shown that breast-band size in male Great Tits is related to social status and resource holding potential (Chapter 3), and a companion study showed that males with larger breast patches provided more resources to females (Norris 1990b). It is possible, therefore, that female Great Tits chose males based on resources rather than melanin badge size. Lendvai et al. (2004) conducted one of the few studies of mate choice relative to plumage coloration in a nonpasserine bird. They manipulated the

Female Mate Choice for Ornamental Coloration

black, eumelanin breast bars of male Kentish Plovers (Charadrius alexandrinus; order Charadriiformes, family Charadriidae), making some larger and shammanipulating others. They then removed the mates of males and recorded how long it took them to attract a new female. Badge size had no effect on the time to find a new mate. This experiment did not control of male-male competition, however, and indeed the authors suggest that the badges may function primarily in male-male interactions. In a study of another nonpasserine bird, the Barn Owl (Tyto alba; order Strigiformes, family Tytonidae), females with more black spots (Plate 29, Volume 1) had higher pairing success than those with fewer black spots, and when female spot size was manipulated, males provided more resources to females whose spot number was not reduced (Roulin 1999). Correlative field studies of other species of songbirds have provided mixed support for the use of eumelanin badges in mate choice. In the lab, Senar et al. (2005) and Johnson et al. (1993) found no evidence for female preference relative to the size of black eumelanin patches in the Eurasian Siskin and American Goldfinch, respectively. In contrast, correlative field studies of Northern Cardinals (Jawor et al. 2003), and Common Yellowthroats (Geothlypis trichas; Thusius et al. 2001; Figure 4.6) found evidence for mate choice based on mask size. In two species of Darwin’s finches, the Medium Ground Finch (Geospiza fortis) and the Cactus Finch (G. scandens), in which males have variable amounts of black in their plumage, field observations indicated that males with less black were at a mating disadvantage compared to males with more black (Price 1984). As in the Pied Flycatcher, in both of these species of Darwin’s finches, plumage blackness was highly age dependent—older males had blacker plumage. Price (1984) statistically controlled for age in his analysis, however, and still found an association between plumage blackness and breeding success. Summary of Eumelanin and Carotenoid Coloration Studies Overall, there is convincing evidence for female mate choice for larger patches of eumelanin pigmentation in some species of songbirds. The evidence for mate choice for eumelanin-based coloration is about as strong as the evidence for mate choice for carotenoid-based coloration. If we consider all studies in Table 4.1 (experimental and correlative), then 12 of 20 studies on carotenoid coloration (60%) found evidence for female choice, whereas 15 of 27 studies on eumelanin coloration (56%) reported female choice for this trait. If we

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Figure 4.6. Relation between the size of the black mask of male Common Yellowthroats in a wild population and (a) the date on which they were first seen with a female and (b) the number of extra-pair young in their nests. Redrawn from Thusius et al. (2001).

only consider experimental studies (excluding blackening of carotenoid coloration), four of seven carotenoid studies (57%) and two of four eumelanin studies (50%) found evidence for female mate choice. This is a very crude comparison, glossing over many important differences in methodologies in

Female Mate Choice for Ornamental Coloration

the different papers and counting five studies of House Finches in the carotenoid totals and nine and 10 studies of Pied Flycatchers and House Sparrows, respectively, in the eumelanin totals. This tally also excludes studies of mate choice for carotenoid-pigmented legs and bills (see below). The proportions of supportive studies for female mate choice for carotenoid and eumelanin plumage pigmentation are so similar, however, that it seems unlikely that changing criteria for comparisons could alter the basic conclusion from this initial set of studies: both melanin and carotenoid-based plumage coloration can be criteria in female mate choice. That females use both eumelanin and carotenoid coloration in mate choice is particularly interesting when we consider the very different information content of the two types of color displays (Chapter 12, Volume 1). Carotenoid coloration most commonly serves as a signal of the health and foraging ability of males, whereas the size of eumelanin badges appears to be more buffered against the effects of parasites and nutrition, and generally under hormonal control (Chapter 12, Volume 1). Female choice for these two very different signals suggests that females seek a diverse range of information about potential mates in assessing ornamental traits. The social status and resource holding potential of a prospective mate might be at least as important to a choosing female as his parasite load or foraging ability. Phaeomelanin Coloration All the above studies of mate choice relative to melanin-based plumage coloration concern bold, black eumelanin coloration. Almost equally common among bird species (and curiously absent from fish and other poikilothermic vertebrates) is brown and rufous phaeomelanin coloration. Phaeomelanin plumage coloration has been the subject of less study than black eumelanin coloration. In the only study of mate choice involving careful manipulation of phaeomelanin coloration, Ligon and Zwartjes (1995) created half-sib Red Junglefowl that either had full male plumage with extensive orange and reddish phaeomelanin coloration or carried a hen-feathered gene and completely lacked bright colors or elongated feathers (Plate 26, Volume 1). They tested the choice of females relative to the ornamented and nonornamented brothers and found that females chose the nonornamented brothers as often as they chose ornamented ones (Figure 4.7). Earlier correlative studies of Red Junglefowl had found that brightness of phaeomelanin coloration was associated with

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Figure 4.7. Number of captive female Red Junglefowl mating with males that were either wild type (red), with extensive phaeomelanin pigmentation, lacking phaeomelanin coloration in their plumage (silver), or lacking all sexually selected plumage attributes (henny). Females had unrestricted access to males, but males were tethered and could not see or interact with other males. Females showed no tendency to mate with ornamented males. Drawn from data in Ligon and Zwartjes (1995).

female mating preference (Zuk et al. 1990). The lack of female response to the complete removal of ornamental coloration, however, argues strongly against phaeomelanin coloration being used as an important criterion in mate choice in the Red Junglefowl. Other attempts to manipulate male phaeomelanin coloration suffered from methodological problems. Omland (1996a) showed that clipping phaeomelanin-based plumage color in male Mallards (Anas platyrhynchos) decreased their attractiveness to females, but he could not control for the effects of feather clipping independent of the effects of altering coloration. Correlative studies generally provide support for female choice for phaeomelanin-containing plumage coloration in males. Patterns of mate choice and coloration have been studied in two species—the Barn Swallow

Female Mate Choice for Ornamental Coloration

(Hirundo rustica; Plate 7, Volume 1) and the Eastern Bluebird (Sialia sialis; Plate 32, Volume 1)—in which rufous ventral coloration has been confirmed to result entirely from melanin pigments, with a higher proportion of phaeomelanin than eumelanin (McGraw et al. 2004b). In a study of Barn Swallows, Safran and McGraw (2004) reported assortative mating by saturation and brightness of rufous breast coloration. They also found that male swallows with brighter breast coloration had higher reproductive success. In a study of Eastern Bluebirds, Siefferman and Hill (2003) found that males with larger and darker patches of rufous breast coloration nested earlier, fed offspring more often, and fledged larger offspring; in this study, however, it was not possible to assess the effects of the phaeomelanin patch independent from the effects of blue structural coloration. In a subsequent study with more years of data, Siefferman and Hill (unpubl. data) found that males with larger and darker phaeomelanin breast patches nested earlier and fed offspring more often than less ornamented males. Similar indirect evidence for mate choice and rusty coloration has been reported for species in which rusty plumage is presumed, but not known, to result from melanin pigments. Yezerinac and Weatherhead (1997) found that in Yellow Warblers (Dendroica petechia), the extra-pair mating success of males was positively related to the amount of brown streaking on the breast. Enstrom (1993) found a preference for rust-colored adult plumage over yellow yearling plumage in Orchard Orioles (Icterus spurius; Plate 30), but color was completely confounded by age in this study. In a mate-choice experiment with captive European Kestrels (Falco tinnunculus) that used natural variation in the brightness of reddish back plumage and blueness of tail color (which could be either structural blue or gray eumelanin), Palokangas et al. (1994) found that females preferred more colorful males. Choice for color was only significant, however, when the effects of blue and red were combined. In a companion field study, males with brighter reddish back plumage produced more young than did males with drabber back plumage (Palokangas et al. 1994), but this observation is only indirect evidence for mate choice. In the Chestnut-sided Warbler (Dendroica pensylvanica), the size of rusty breast streaks was also related to nest initiation date, but not to reproductive success (King et al. 2001). Overall, the role of phaeomelanin pigmentation in mate choice is less well studied than eumelanin pigmentation, with only one experimental test to date. Interestingly, unlike eumelanin coloration, for which badge size rather than color quality seems to be the object of female choice, phaeomelanin pigmentation seems to be assessed by females for both color quality and badge

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size. The signal content of phaeomelanin pigmentation and hence the benefits to females of choosing mates based on this trait remain to be determined.

Structural Coloration Early papers looking at structurally based plumage coloration, which relied on the human visual system to assess coloration, came to the conclusion that there was little or no variation in chroma or hue of blue structural coloration. In their studies of Satin Bowerbirds (Ptilonorhynchus violaceus), a species in which males have glossy blue-black iridescent plumage coloration, Borgia and colleagues concluded that there was essentially no variation on which sexual selection could act among males in definitive plumage (Borgia 1986; Borgia and Collis 1989). Although Borgia was one of the few authors to state in print that variation was lacking from structural color displays of birds, this was conventional wisdom among ornithologists through the mid-1990s, and this misconception was undoubtedly responsible for the dearth of studies on structural coloration through 1997 (but see Johnson 1988). Interest in structural coloration of feathers increased exponentially with the publication of reviews by Maier (1993), and Bennett, Cuthill, and colleagues (Bennett and Cuthill 1994; Bennett et al. 1994) that pointed out that most birds see UV coloration as well as they see blue or green or red coloration (Chapter 1, Volume 1). These papers stimulated a surge of research showing that plumage coloration of many species of birds does indeed have a UV component and that females notice if the UV component is removed from a male’s appearance. At the same time, ornithologists began to focus on the function of structurally based coloration as distinct from that of pigment-based colors (Fitzpatrick 1998; Andersson 1999; Keyser and Hill 1999). Because structural mechanisms generally produce short-wavelength color displays, most UV coloration is also structural in nature (Chapter 7, Volume 1). Thus the literature on “UV” plumage coloration and the literature on structurally based plumage color displays are thoroughly muddled. UV-Blocking Studies With a new appreciation for the importance of UV color perception in birds, one of the first questions addressed was whether the UV component of plumage coloration was used by females in assessing mates. This hypothesis was

Female Mate Choice for Ornamental Coloration

tested in a number of species by presenting females with males behind UVblocking or UV-transmitting light filters. In all species that have been tested in this manner, including the Red-billed Leiothrix (Leiothrix lutea; Plate 1, Volume 1; Maier 1993), Zebra Finch (Plate 18; Bennett et al. 1996; Hunt et al. 1997), Blue Tit (Parus caeruleus; Plate 18; Hunt et al. 1999), Budgerigar (Melopsittacus undulatus; Plate 17; Pearn et al. 2001), and European Starling (Sturnus vulgaris; Plate 23, Volume 1; Bennett et al. 1997), it was demonstrated that females preferred males viewed without the UV component of color blocked. Although these experiments showed definitively that females see UV light (which had been established for many species by more direct means; Chapter 1, Volume 1) and avoid odd-looking males during mate choice, they provided little information regarding whether natural variation in expression of structural plumage coloration affected mate choice (Box 4.2). In other manipulations, UV-blocking oil was applied to feathers with ornamental structural coloration to remove the UV component of these ornaments. This approach avoided the problem of changing the background and nonornamental traits in the birds, but it still gave the ornaments of these birds a coloration that was unnatural. Using such techniques in lab studies, it was shown that captive female Bluethroats (Luscinia svecica; Plate 19) preferred males with a UV component to their ornamental coloration versus males lacking UV coloration (Andersson and Amundsen 1997). In a companion field manipulation, male Bluethroats with artificially reduced UV reflectance paired later, spent less time advertising for extra-pair mates, and had lower success achieving extra-pair fertilizations than did males whose plumage color still had a UV component (Johnsen et al. 1998). In an aviary study with Pied Flycatchers, females initiated nests more often with males whose UV reflectance of dark dorsal plumage was increased with fly fishing oil versus males whose UV reflectance was removed with sunblock (Siitari et al. 2002). Although the males treated with sunblock in this study still had odd plumage unlike any wild male, this study at least showed that females were not simply avoiding oddly plumaged males, because the preferred males that were treated with the fly fishing oil had plumage with an exaggerated UV peak, higher than that of any wild male. This study also shows that the “black” plumage of Pied Flycatchers has a distinct peak in the UV portion of the spectrum and calls into question earlier plumage-manipulation experiments with Pied Flycatchers (see the section on melanin above) that ignored the UV component of plumage coloration.

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Box 4.2. Manipulating Plumage Coloration Experimental manipulations are among the most powerful investigative tools available to biologists. For researchers interested in deducing the function of color displays, experiments in which the coloration of individuals is modified provide a means to uncouple male appearance from all other attributes. Modifying the colors of feathers and bare parts would appear to be relatively straightforward, given that many coloring agents (paints, dyes, and marking pens) are commercially available. The problem, however, is that all commercially available coloring agents were designed for human visual systems and often lack an appropriate UV component. So although it is relatively easy to match natural feather or bare-part colors within the humanvisual range, one has to be mindful of the short-wavelength portion of the spectrum that is visible to birds but invisible to us. From the inception of experiments with animal coloration, the most common color manipulation has been complete removal of the display. This approach began with the use of black dyes and shoe polish to cover the red and yellow epaulets of male Red-winged Blackbirds (see Plate 10 for an example with Yellow-headed Blackbird [Xanthocephalus xanthocephalus]). Thirty years later, with a surge of interest in the UV perception in birds and UVcolor display in feathers, the complete removal of the display traits under study once again became a widely used experimental technique. Researchers used either filters that blocked transmission of UV light or a UV-blocking oil that was applied directly to feathers (Figure B4.1). The use of filters changes not just the appearance of the ornamental color under study, but the coloration of all other parts of the bird and the color of the bird’s environment. Such complete removal of an ornamental trait can provide grosslevel analysis of trait function—if females do not respond to complete removal of the trait, it is unlikely that it functions in mate choice—but such traitremoval experiments tell us nothing about how females respond to natural variation in the trait. A better approach than trait removal is to manipulate the color display of individuals toward the extremes of natural trait expression. For longwavelength color displays, such as those that result from carotenoid pigments, this alteration can be done using hair dyes or, more easily, using marking pens. The results of such manipulation of red/orange/yellow plumage can

Female Mate Choice for Ornamental Coloration

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Figure B4.1. Manipulation of blue/UV feathers. (a) The use of filters or oils that absorb UV-wavelengths creates an unnatural spectral curve. (b) Black and blue markers applied to feathers with noniridescent structural coloration change the intensity of coloration but not the characteristic shape of the curves.

be a close match to natural coloration, although carotenoid-based yellow coloration often has a UV peak that can be lost upon color application. Black marking pens are also excellent for making feathers black. Marking pens also can be used to manipulate the coloration of blue/UV structural feathers, which is a fundamentally better approach than simply blocking UV reflection using filters or oils. When applied to noniridescent blue feathers, several commercially produced blue marking pens enhance the blue coloration of the feathers but retain the same shape of reflectance curve and a natural UV component (Figure B4.1). A common problem with manipulation of feather coloration is that it is easier to add color to feathers than to remove color. Yellow feathers can easily be made red, but red feathers cannot easily be made yellow. A patch of black plumage can readily be made larger but not smaller. The one exception that I have experienced is structural blue/UV coloration. A black marker applied to noniridescent structural blue/UV feathers reduces the brightness and chroma of the feather, but it does not change the shape of the reflectance curve (the hue remains unchanged; Figure B4.1). To conduct symmetrical manipulation of carotenoid coloration in aviary experiments, it is best to raise all birds on carotenoid-deficient diets, which creates a set of birds with little ornamental coloration, then to add colors to these “blank slates.”

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Natural Variation in Structural Coloration Other studies have assessed the natural variation in structural coloration. Bennett et al. (1997) tested the preferences of female European Starlings held in aviaries and found that females preferred males with brighter, glossy purple plumage coloration. Interestingly, they found that greater reflectance in the UV portion of the spectrum, but not the human-visible spectrum, predicted attractiveness. Because of the problems with experiments that use UV-blocking filters or sunscreens to alter plumage, this study is the first clear demonstration of females basing choice of mates on natural variation in structurally based plumage coloration. The best experimental approach to test for female preference for variation in expression of structurally based plumage coloration is to manipulate plumage so that the treatment moves males toward the extremes of natural color expression (Box 4.2). Only one study has manipulated structural plumage coloration within a range of natural coloration. Ballentine and Hill (2003) used blue and black markers to change the plumage coloration of captive male Blue Grosbeaks (Passerina caerulea; Plate 7, Volume 1). The black marker decreased plumage brightness in one group of males, and the blue marker increased plumage reflectance in another group, but the shapes of the reflectance curves did not change (Box 4.2). Females showed no preference for males with brighter plumage. In a companion field study of Blue Grosbeaks, the plumage blueness of males was correlated with territory size and quality but not nest initiation date (Keyser and Hill 2000). In this same population, however, dull males were cuckolded more often than bright males (Estep et al. 2005). One explanation is that female grosbeaks use plumage color to choose extra-pair but not social mates, but more study is needed. Other attempts to manipulate structural coloration in mate choice experiments have methodological problems. Mateos and Carranza (1995) used “make-up powder” to dust the green and bronze structurally colored plumage of Ring-necked Pheasants (Phasianus colchicus), which gave them an appearance “quite similar to that of an ill animal” but had no effect on female choice. In an experiment with Mallards by Omland (1996a), clipping the iridescent green head and rusty breast feathers of males had a negative effect on mate choice, but there was no way to assess an effect of color change separately from a clipping effect. In the same study, removing the blue speculum of the wings of males by clipping had no significant effect on pairing success. In an aviary study of natural variation in structural coloration of Northern Pintails (Anas acuta), Sorenson and Derrickson (1994) found a correlation between the

Female Mate Choice for Ornamental Coloration

brightness (as judged by human visual assessment) of the iridescent green speculum of males and female association preference. Several correlative field studies have looked at natural variation in structural coloration in relation to mate choice in Blue Tits. The crown feathers of male and female Blue Tits (Plate 18) look equally brightly colored to human observers, but spectral analysis of blue plumage indicates that there are nonoverlapping differences in the reflectance spectra, and particularly hue, of males and females (Andersson et al. 1998; Hunt et al. 1998). Andersson et al. (1998) looked at pairs of Blue Tits in a wild population in Sweden and found assortative mating by structural plumage coloration—brightly colored males tended to pair with brightly colored females (Figure 4.8). Moreover, in a subsequent study, there was a significant positive correlation between the proportion of male offspring in a nest and the plumage reflectance of the attending male (Sheldon et al. 1999; Figure 4.8). This positive correlation between plumage brightness and offspring sex ratio actually reversed, however, when the UV component of feather reflectance was masked by a UV-absorbing oil—males that had been bright had a higher proportion of female offspring and males that had been drab had a higher proportion of male offspring (Sheldon et al. 1999; Figure 4.8). Resource allocation theory predicts that females will produce sons if they perceive their mate to be of high quality and daughters if they perceive their mate to be of low quality (Trivers and Willard 1973), so these observations were used as evidence that females view bright structural coloration as attractive. Finally, in this same Blue Tit population in Sweden, males with UV-shifted crown hue were cuckolded less often than males with crown hue shifted toward longer wavelengths (Delhey et al. 2003). Assuming that females paired to preferred males engaged in fewer extra-pair matings than did females paired to less-preferred males, this observation could be interpreted as evidence for female choice for structural plumage coloration. None of these field studies with Blue Tits was able to definitively rule out the effects of male-male competition in driving patterns of pairing. Correlative field studies on a few other species of songbirds have looked at mate choice relative to natural variation in structural plumage coloration. In a field study of Eastern Bluebirds, Siefferman and Hill (2003) found that chroma of structural blue/UV coloration of male bluebirds was positively associated with breeding onset, paternal provisioning rates, size of fledglings, and male reproductive success, but the authors did not assess the effects of blue structural coloration independent of phaeomelanin breast coloration. Subsequent analyses with more years of data revealed that chroma of structural coloration, independent of rusty chest coloration, significantly predicted male feeding rates

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Figure 4.8. Relation between UV chroma of blue/UV structural plumage of male Blue Tits and (a) the UV chroma of the plumage of female Blue Tits with whom they were paired and (b) the sex ratio of their offspring. In (b), deviation is from 1:1 sex ratio, with positive values male-biased and negative values female-biased. A positive relationship between sex ratio and the chroma of crown feathers (solid line) was reversed when the coloration of crown feathers was manipulated by coating them with UV-blocking oil (dashed line). Redrawn from (a) Andersson et al. (1998) and (b) Sheldon et al. (1999).

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to incubating mates and feeding rates to offspring (L. Siefferman and G. E. Hill, unpubl. data), but these observations are at best indirectly related to mate choice. Perrier et al. (2002) analyzed a large data set on the iridescent dorsal plumage of the Barn Swallow and found no differences in UV reflectance between mated and unmated males and no relationship between UV coloration and the time that it took males to attract a mate. Moreover, breeding date or reproductive success of male Barn Swallows was not related to UV reflectance. Finally, in a study of the Superb Fairy-wren (Malurus cyaneus), the quality of the blue coloration was not assessed, but speed to complete molt and acquire blue coloration was a good predictor of female choice of extra-pair mates (Dunn and Cockburn 1999). It was proposed that in Superb Fairy-wrens, molt speed is related to male condition (Mulder and Magrath 1994). This study suggests that the brilliant blue structural coloration in this species serves as an amplifier of molt speed, which is the actual target of sexual selection. Summary of Structural Coloration Studies If we consider all studies of female choice and structural coloration (excluding studies using UV-blocking filters, because this methodology changes melanin and carotenoid coloration as well), then 13 of 17 studies (76%) found evidence for choice. If we just consider experimental studies, including studies that used UV-filtering oils, then six of nine studies (67%) found evidence for choice. These proportions of positive studies are slightly higher than what has been observed in studies of female choice for melanin or carotenoid coloration (see above), suggesting that structural coloration is used as a criterion in mate choice as least as frequently as are pigment-based color displays. However, in very few studies to date has structural coloration been manipulated within the natural range of variation, so there are not nearly as many convincing studies of mate choice for structural coloration compared with those for carotenoid and melanin coloration. It is interesting that, like carotenoid but unlike melanin coloration, color quality and not patch size seems to be the criterion most commonly used in mate choice for structural coloration (Box 4.3). Structural coloration may serve as an indicator of nutritional condition and history of parasitism (Chapter 12, Volume 1; but see Chapter 7, Volume 1), which would make it more like carotenoid pigmentation in its condition-dependent expression. Perhaps the focus on color quality rather than badge size is related to signal content. More experimental manipulations of blue/UV structural coloration within the natural range of color expression both in the lab and in the field are needed.

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Box 4.3. Color Quality versus Patch Size From the early studies of female mate choice relative to male coloration, researchers have focused on either the extent of the surface of an animal with coloration (patch size or badge size) or the quality (hue, chroma, and brightness) of the color display within a patch. For instance, in the series of studies of Guppies in the mid-1980s that became the foundation of much of the work on birds and fishes that followed, patch size and color quality were both referred to as “carotenoid ornamentation,” often with no distinction between them. It turns out that in Guppies, females prefer males with both large and well pigmented color spots (Kodric-Brown 1985, 1989; Houde 1987). A similar preference for both large and well pigmented patches has been observed in House Finches (Hill 1994). Few bird studies, however, have considered mate choice relative to both patch size and color quality within the same species. Moreover, researchers studying particular types of color display tend to focus on one color attribute or the other; almost all studies of carotenoid and structural coloration focus on color quality, whereas the great majority of studies of eumelanin coloration focuses on patch size. In Guppies, the area of orange spots is largely genetically determined and is generally not affected by carotenoid intake or parasites. In contrast, the chroma of orange spots is affected both by dietary access to carotenoids and parasites. Thus, spot size and the orange chroma of the color of spots represent two fundamentally different components of color display (Badyaev et al. 2001), with different ontogenetic control, condition dependency, and heritabilities. No comparable data on genetic versus environmental control of patch size and color quality are available for birds. The Guppy studies, however, point out the fallacy of discussing spot size and color quality as if they were interchangeable measures of trait elaboration.

White Coloration and Achromatic Brightness The coloration of feathers has both a chromatic component, which results from the relative stimulation of different cone types in the retina, and an achromatic component, which results from stimulation of rod cells (Chapter 1, Volume 1). Throughout this chapter, I have focused on mate choice

Female Mate Choice for Ornamental Coloration

relative to chromatic coloration. Much less work has been conducted on achromatic, black-and-white coloration (with the exception of size of black patches as described in previous sections). White plumage is the result of structural components of feathers that incoherently scatter light (Fox 1976; Chapter 7, Volume 1). In most studies of white plumage, the extent rather than spectral properties of the colored plumage has been the focus, and several studies have found evidence for female mate choice for larger spots of white. Barn swallows have white spots on their tail feathers that are larger in adult males than in females or juveniles, suggesting that they are sexually selected (Kose and Møller 1999). In an experiment in which spot size was altered with a black marker, Kose and Møller (1999) found that male barn swallows with reduced spot size paired and bred later, less frequently had second broods, and had lower reproductive success. Similarly, Höglund and Lundberg (1987) found a correlation between mating success and the amount of white in the tails of Great Snipe (Gallinago media), which varies substantially among males. They then showed that experimentally increasing the amount of white in the tails of males increased the mating success of males compared to controls (Höglund et al. 1990). A more recent study of Great Snipe using more years of data, however, found no evidence for female mate choice of males with whiter tails (Saether et al. 2000). Moreover, observations of females searching for mates showed that females did not mate preferentially with males with whiter tails among those males that they visited (Saether et al. 2000). Female Dark-eyed Juncos (Junco hyemalis) preferred males with increased amounts of white in their tails (Hill et al. 1999b), but male juncos did not show the same preference for tail white in females (Wolf et al. 2004). Perhaps the most thorough study of the sexual significance of white plumage concerns the forehead patch of Pied and the closely related Collared Flycatcher (Ficedula albicollis; Plate 18). In populations of Collared Flycatchers in Sweden (Gustafsson et al. 1995) and Pied Flycatchers in Spain (Potti and Montalvo 1991), correlational field studies indicated that females prefer to mate with males having larger white forehead spots. In a population of Pied Flycatchers in Norway, however, both correlational analyses and experimental manipulations of the size of the white forehead spot revealed that spot size was not related to any measure of male condition and was not used by females in choosing mates (Dale et al. 1999). An explanation for this pattern is that, in allopatry, females of both species prefer males with large forehead patches, but in sympatry, as occurs in Norway, choice for divergent traits in males selects

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against female choice for white crown plumage in Pied Flycatchers (Sætre et al. 1997). As indicated by these studies, the extent of white coloration rather than achromatic brightness appears to be the object of female mate choice in several species of songbirds. Rarely are spectral characteristics, and particularly achromatic brightness, of white color displays measured, however, so the importance of size over color quality might reflect a bias of observers. Female mate choice in relation to the achromatic brightness of white displays has been studied in two species. Sorenson and Derrickson (1994) studied Northern Pintails in an aviary and looked for male traits that predicted female choice. They found that the whiteness of breast plumage (as ranked by human observers) significantly predicted female mate preference. Doucet et al. (2005) studied paternity in relation to the brightness, as determined by spectrometry, of the white cheeks of Black-capped Chickadees (Poecile atricapillus). They found that males with brighter white cheeks were cuckolded less often and had higher reproductive success than did males with drabber white cheeks. In a subsequent aviary mate-choice study, Woodcock et al. (in press) found that female chickadees preferred males with brighter white cheeks as well as higher UV chroma in black bibs and caps. White patches of feathers make for bold plumage displays in birds, and the evidence is strong that females prefer males with larger white patches in at least several species of birds. The intensity of white coloration—achromatic brightness—has rarely been studied, but should be included in future studies of white coloration. Although there are no known production costs of large versus small patches of white coloration, it is easy to imagine that it is challenging to keep a white patch of feathers clean and brilliantly white (see Chapter 9, Volume 1) and that the ability to maintain such a bright white plumage may signal male quality. Mate choice relative to achromatic brightness should be a fruitful area for future research.

Fluorescence The yellow plumage of some species of parrots fluoresces under UV light (Völker 1937; Plate 16, Volume 1). Fluorescence occurs when light is absorbed by an object and then re-emitted at a longer wavelength. In the case of parrot plumage, the short wavelength light is in the UV-A region of the spectrum (short-wavelength UV) and is re-emitted as yellow light. The crown and cheek feathers of Budgerigars show this sort of fluorescence. Arnold et al. (2002)

Female Mate Choice for Ornamental Coloration

tested whether the fluorescent plumage of Budgerigars served as a signal in mate attraction. They presented both male and female Budgerigars with oppositesex birds that either had UV-blocking oil or UV-transparent petroleum jelly applied to feathers. They found that both males and females preferred prospective mates that had plumage with UV-light transmission and hence fluorescent signaling. The authors presented this result as evidence that fluorescence serves as a signal in mate choice, but the sun-block that they used in their study eliminated UV wavelengths as well as fluorescent color display. Thus there was no way to distinguish between choice for fluorescent signaling and that for UV signaling. Pearn et al. (2001, 2003) eliminated the problem of confusing UV and fluorescent signaling by using filters that selectively blocked UV-A or UV-B wavelengths. UV-A wavelengths are invisible to birds, but they are the wavelengths that are shifted to visible light in fluorescent displays of parrot plumage. UV-B wavelengths, however, are visible to birds and are part of the color display of Budgerigar plumage. In female mate choice trials with Budgerigars, Pearn et al. (2001, 2003) observed that loss of fluorescence in male plumage had no effect on male attractiveness to females, whereas loss of UV coloration had a large negative effect on male attractiveness. This result suggests that the effect of sun block in the study by Arnold et al. (2002) was due to the removal of the UV plumage signal, not removal of fluorescence. The function of fluorescence in bird plumage, if it has one, remains to be determined, but the studies by Pearn et al. (2001, 2003) suggest that it does not function in mate attraction.

Mate Choice for Psittacofulvins, Porphyrins, and Undescribed Pigments There have been few mate choice studies on color displays that are not at least presumed to be carotenoid, melanin, or structural. In many behavioral studies, however, the source of coloration is untested. The bright orange ear spots of King Penguins (Aptenodytes patagonicus; Plate 17, Volume 1) have recently been shown to result from brown melanins as well as a yet-to-be described yellow pigment similar to pterins (McGraw et al. 2004a). In a field experiment, Jouventin (1984:96) covered the orange ear spots of some male King Penguins and left the spots of others untreated. The female partners of all males in the experiment were held in captivity to force the males to seek new mates. Males lacking orange ear spots took ten times longer to find mates than did males with orange spots. In a more recent study,

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the orange ear spots of unpaired King Penguins either were made smaller or were sham-manipulated with marking pens. Males with reduced ear-patch size were significantly less likely to pair than sham-manipulated males (Jouventin et al. 2005). In a study of Yellow-eyed Penguins (Megadyptes antipodes), Massaro et al. (2003) conducted what they described as a study of assortative mating relative to “carotenoid-derived ornaments.” They found that the hue of the yellow eyes and postocular stripes of paired male and female penguins were correlated independently of age. However, McGraw (2004) showed that the yellow feathers of the postocular stripe of Yellow-eyed Penguins are colored with yet-to-be-described pigments similar to those in King Penguins (Chapter 8, Volume 1). The source of eye color remains untested. So rather than being the only evidence for mate choice for carotenoid-based coloration outside of order Passeriformes, this is one of the few studies of mate choice based on the noncarotenoid penguin pigment. The lack of studies of mate choice relative to plumage coloration that results from mechanisms other than melanins, carotenoids, or microstructure represents a significant gap in our understanding of color displays. Until we know the ubiquity of color displays that result from other sources, there is no way to know how large this gap really is. It has long been known that the brilliant yellow-and-red coloration of parrots (order Psittaciformes) is the result of psittacofulvins (Chapter 8, Volume 1). Despite substantial research on mate choice in parrots, most studies of pairing in parrots have been conducted with Budgerigars and with no consideration of coloration (although studies of fluorescence are an exception, see above). Recently, Masello and Quillfeldt (2003) found assortative mating relative to the size of red belly patches in the Burrowing Parrot (Cyanoliseus patagonus; Plate 16). This is the only evidence for psittacofulvin-based coloration serving as a potential criterion in mate choice. The function of turacin-based coloration in turacos (order Maliphagiformes), which is brilliant green and red in coloration (see Chapter 8, Volume 1; Plate 12, Volume 1), is completely unstudied. Similarly, the signaling function of other porphyrins, which produce reddish-brown coloration in several taxa of nonpasserines (owls, bustards, goatsuckers; Chapter 8, Volume 1), remains to be studied.

Bare-Part Color The bare parts of birds, including combs, wattles, snoods, beaks, and skin, are commonly yellow, orange, or red, and this coloration is thought to be caused by carotenoids deposited in the tissue, by blood under the surface, or by a

Female Mate Choice for Ornamental Coloration

combination of carotenoids and blood (Chapters 5 and 8, Volume 1; Plates 5 and 13, Volume 1). The size of such bare parts has been implicated as a key criterion in female mate choice in several species (Zuk et al. 1990, 1992; Buchholz 1995), but few studies have tested whether females assess the quality of the color of these ornaments. The first and among the most detailed studies on mate choice in relation to the red/orange coloration of bare parts were conducted by Burley and colleagues on leg coloration in Zebra Finches (reviewed earlier in the chapter). Their studies of leg-band color were followed by another mate-choice aviary study on carotenoid-based bill color in Zebra Finches. They manipulated bill color with paint and found that females preferred males with redder bills (Burley and Coopersmith 1987). In a study of natural variation in bill coloration that resulted from different brood sizes, De Kogel and Prijs (1996) also found female mate preference for male Zebra Finches with redder bills, and Blount et al. (2003) presented female Zebra Finches with males reared on high- and low-carotenoid diets and observed that females preferred the brighter-billed males from the high-carotenoid treatment. Males in the latter two studies differed in overall condition as well as bill color, however, so the results are hard to interpret. Other studies have failed to confirm mate choice for bill color in Zebra Finches. Collins et al. (1994) showed that, when they controlled for song rate, there was no significant preference by female Zebra Finches for males with redder bills. In subsequent experiments in which bill color was manipulated with paint, Sullivan (1994) and Weisman et al. (1994) found no female preference for males with redder bills. Collins and ten Cate (1996) discussed why different studies of bill coloration in Zebra Finches have produced such disparate results. They concluded that early rearing environment may affect choice patterns and that there may be a hierarchy of choice criteria, with display behavior (including song) being more important than bill color. The bill-coloration studies that have followed Burley and Coopersmith (1987) show that mate choice can be complicated by context and by assessment of multiple ornaments and behaviors. A few other studies of mate choice and bare-part coloration have been conducted. Omland (1996b) found that male bill color (ranked by human visual assessment of yellowness and amount of black spotting) was a good predictor of pairing success in captive flocks of wild-type Mallards (Plate 15). Male-male interactions could not be controlled in this study. Mateos and Carranza (1995) found no evidence for female choice relative to the color of fleshy wattles in an aviary study of Ring-necked Pheasants, and Faivre et al. (2001) found that male Eurasian Blackbirds (Turdus merula) with oranger bills paired with females

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that were in better condition. However, the bill color of male blackbirds was not significantly related to nest initiation date or number of nesting attempts. Similarly, Dearborn and Ryan (2002) found no relationship between the chroma of the red throat pouches of male Great Frigatebirds (Fregata minor) and nest initiation date. Bare parts can also be blue in coloration; such coloration results from coherently scattering dermal collagen arrays (Chapter 7, Volume 1). In combination with carotenoid pigments, coherent scattering can create a green or bluegreen appearance. Both male and female Blue-footed Boobies (Sula nebouxii) have conspicuous blue-green feet and legs. Torres and Velando (2003) colored the legs of some male Blue-footed Boobies less green (more blue) and less bright, while sham-manipulating others. This treatment made experimental males similar in appearance to males in poor nutritional condition. They found that males with feet and legs colored to be less green were courted less by females and engaged in fewer copulations than did control males. The authors then conducted the same manipulation experiment on females and found that males courted duller females less often than they did control females (Torres and Velando 2005). The authors argued that greener legs signal higher carotenoid content and males showed a mating preference for females signaling this condition. Their study is the most convincing evidence for mate choice for bare-part coloration in a wild population of birds. Bare parts can change coloration in response to environmental conditions faster than can feathers (Chapters 5 and 8, Volume 1), and so bare-part coloration might provide females with fundamentally different information on male condition than does feather coloration. Indeed, only studies of carotenoid coloration of bills (Blount et al. 2003; McGraw and Ardia 2003), not feathers (Navara and Hill 2003), have supported the idea that birds trade off the use of carotenoids for immune response versus ornament display. More studies are needed on mate choice relative to bare-part coloration. Studies simultaneously looking at bare-part and feather coloration in the same individuals would be particularly useful in helping to elucidate the response of females to these different types of color displays.

Polymorphic Traits In the studies described above, the color displays that were under investigation relative to intersexual selection typically showed continuous variation in expression—from small to large patches, from low to high chroma, or from

Female Mate Choice for Ornamental Coloration

yellow to red. In some species of vertebrates, however, variation in color displays jumps between discrete morphs (Chapter 11, Volume 1; Chapter 2). Among the first studies of mate choice relative to plumage coloration in birds was the long-term study by O’Donald of the Parasitic Jaeger (Stercorarius parasiticus; Arctic Skua in Eurasia). Jaegers come in two distinct melanin-based color morphs—light and dark (Chapter 11, Volume 1; Plate 28, Volume 1). O’Donald (1980, 1983) observed that dark-morph males paired significantly faster and had higher reproductive success than did light-morph males. He argued that the mating advantage of dark males was due to female choice for darker males and not due to male-male competition, better resources held by dark males, or some other related factor. He also found evidence for assortative mating by color morph (O’Donald 1983). He proposed that the pale morph is maintained in the population by gene flow from other populations. More recently, in a study of Parasitic Jaegers on an island near O’Donald’s study site, Phillips and Furness (1998) found no fitness advantage for dark-morph males and evidence for assortative mating by morph in some, but not all, years. The conclusions of Phillips and Furness were based on fewer years of observation than were O’Donald’s studies, and they suggested that some of the differences between their findings and those of O’Donald could be due to changes in environmental conditions during the periods that the two studies were conducted. Another well-studied species that has a striking melanin-based plumage polymorphism is the Snow Goose (Chen caerulescens), which comes in a white or dark gray (blue) phase (Plate 28, Volume 1). Cooch and Beardmore (1959) found strong assortative mating for plumage coloration. This pattern of assortative mating was shown to be a result of female mate choice for likeplumaged birds, and the mechanism for such choice was imprinting on one’s parental color morph (Cooke and Cooch 1968; Cooke and McNally 1975; Cooke et al. 1976). In an experiment with captive geese, goslings raised with parents that were colored pink showed a mating preference for pink individuals when they were adults (Cooke et al. 1972). With huge datasets and multiple years of observation, Cooke and colleagues could find no fitness differences among birds of any color morph (Cooke et al. 1995). Sexual imprinting that leads to mating preferences for a parental color type provides an interesting mechanism for the maintenance of plumage color polymorphisms. More study is needed to determine whether such imprinting is more common when a plumage polymorphism is involved and how such imprinting could work if choice is for the most exaggerated expression of a condition-dependent trait (as described in previous sections).

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geoffrey e. hill In the Common Buzzard (Buteo buteo), a large, Eurasian hawk, individuals can display a light, dark, or intermediate plumage morph, the intermediate color morph being the most common in virtually all populations. Kruger et al. (2001) studied mating patterns and reproductive success relative to color morphs in buzzards and found strong assortative mating by color types. Surprisingly, however, they also found a strong fitness advantage for heterozygous individuals with intermediate color morphs, and thus a large fitness advantage for homozygous dark or light morph birds to mate disassortatively. Apparently, imprinting by young on parent’s morph leads to assortative, and maladaptive, mating (Kruger et al. 2001). Imprinting as the cause for assortative mating in this species was deduced rather than experimentally tested. A few other cases of plumage polymorphism in birds have been studied relative to female choice. White-throated Sparrows (Zonotrichia albicollis) either have black or tan crown stripes, and this plumage polymorphism is determined by the chromosomal arrangement they inherit. In both males and females, black-striped individuals are more aggressive than tan-striped ones (Kopachena and Falls 1993), but tan-striped individuals are better parents (Knapton and Falls 1983). There is strong disassortative mating among Whitethroated Sparrows in the wild, with 93–95% of the population paired to individuals of opposite morph (Knapton and Falls 1983). Houtman and Falls (1994) tested whether mate choice was responsible for the disassortative mating. In an aviary, they presented males and females with opposite-sex birds of both morphs. Females of both morphs showed a preference for tan males when they were allowed to interact with the males, but no preference when one-way mirrors prevented interactions. Males of both morphs showed a preference for black-morph females when they could interact with the females, but not when interaction was blocked with one-way mirrors. Houtman and Falls (1994) concluded that, due to their aggressiveness, black-morph females out compete tan-morph females for access to preferred tan-morph males. Tan-morph females are then forced to pair with less preferred white-morph males. If this deduction is correct, then aggressive interactions and not mate choice create the patterns of disassociation of color types seen among pairs of sparrows. Gouldian Finches (Chloebia gouldiae; Plate 18) come in three discrete cheekcolor morphs: red, gold, and black. There are no data regarding assortative mating by cheek color in the wild, but in aviaries, Gouldian Finches mate assortatively (Fox et al. 2002). To test whether this assortative mating was due to mate selection, Fox et al. (2002) conducted aviary mate choice experiments and found no evidence for female preference based on cheek-color morph.

Female Mate Choice for Ornamental Coloration

They also found no evidence for female mate choice for rare male phenotypes. The mechanisms for assortative mating and the maintenance of the color polymorphism in Gouldian Finches remain unexplained. Overall, the evidence is mixed that color morphs within populations are maintained by female mate choice. The most exhaustive studies have been conducted on Snow Geese, in which females imprint on parental color type and imprinting determines the color type that they select as mates. More studies are needed to determine if a similar imprinting mechanism works in other species, but these sorts of studies are difficult to conduct with wild birds.

Color Symmetry and Mate Choice Møller (1990a) and Thornhill (1992) first brought to the attention of behavioral ecologists the idea that precision of bilateral symmetry for traits that are genetically and developmentally programmed to be symmetrical can reflect the phenotypic condition of an individual. This suggestion set off a flurry of studies looking at female mate choice relative to the symmetry of male ornaments. Most of these studies focused on morphological traits that were easy to measure and manipulate, such as the length of tail feathers or the branching of antlers. Several researchers, however, have looked at color symmetry in relation to female mate choice. One way that researchers have manipulated the color symmetry of males and measured the mate-choice response of females to this trait is by manipulating the position of colored leg bands applied to males. In a carefully controlled aviary study, Swaddle and Cuthill (1994b) showed that females preferred to associate with male Zebra Finches with symmetrical leg bands versus those with asymmetrical bands. This same pattern of preference by female Zebra Finches was also found when leg bands were asymmetrical only in the UV portion of the spectrum (Bennett et al. 1996). In a field study conducted on Bluethroats, females showed an association preference for males with symmetrical as opposed to asymmetrical blue and orange leg bands (Fiske and Amundsen 1997). In other studies, researchers have looked at variation in pigment symmetry in plumage coloration. In most of these studies, natural variation in symmetry was assessed, but, in a study of chest barring in Zebra Finches, barring symmetry was manipulated. Swaddle and Cuthill (1994a) observed that female Zebra Finches displayed more vigorously and for a longer period of time in front of males with more symmetrical barring on their chest plumage. In a

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correlative field study of the Rufous Bush Chat (Cercotrichas galactotes), males with more symmetrical white/black tail spots mated earlier, providing at least indirect support for female preference for symmetry (Alvarez 2000). In another field study, Hill (1998) looked at the symmetry of carotenoid pigmentation in House Finches and found that redder males had more precise left/right symmetry of carotenoid pigmentation. Moreover, the carotenoid pigmentation of paired males was more symmetrical than that of unpaired males, and symmetry actually seemed to be a better predictor of pairing success than redness (Hill et al. 1999a). Finally, in a correlative field study of a Montana population of House Finches, paired males had both more symmetrical patches of coloration and greater pigment symmetry within patches than did unpaired males (Badyaev et al. 2001). Overall, there have been comparatively few studies on the symmetry of color displays, but the few studies that have been conducted suggest that females of some species use pigment symmetry in assessing potential mates. It would be interesting to know how pigment symmetry is weighted by females relative to coloration per se, and whether females gain different information by assessing pigment symmetry versus color quality (Badyaev et al. 2001). A novel aspect of color displays that has been the focus of recent studies is the regularity of the borders of colored patches, or the “immaculateness” of the color display. In Common Shelducks (Tadorna tadorna), there was assortative mating by immaculateness of red-brown (presumably phaeomelanin) chest bands, providing indirect evidence for mate choice (Ferns and Lang 2003). In Great Tits, immaculateness of the black border of white cheek patches predicted social status and reproductive success, but there was no clear evidence that it played a role in mate choice (Ferns and Hinsley 2004). It may be challenging to produce a sharp transition between patches of colored feathers, making the immaculateness of color patches a reliable indicator of individual condition. Patch immaculateness appears to be an interesting area for future research on mate choice.

Summary Over the past two decades, the study of mate choice in relation to coloration in birds has reached a level of maturity. More than a hundred studies have now been conducted. The use of color displays as a common criterion in mate choice is no longer controversial, and it is clear that mate choice has been an important selective agent in shaping the evolution of many color displays.

Female Mate Choice for Ornamental Coloration

Fundamental aspects of female mate choice relative to male coloration, however, remain poorly studied. We can now state with confidence that females of at least some bird species use expression of the carotenoid-based plumage and bare-part coloration in choosing mates. However, there are still relatively few carefully controlled experimental studies, conducted in either the lab or the field, that have looked at female preference relative to male carotenoid display in birds. There are as yet no experimental studies of carotenoid coloration and mate choice outside of passerine birds, and most experimental studies of passerine birds have been conducted with cardueline finches—one subfamily of songbirds. The fish literature on mate choice relative to carotenoid coloration is far more extensive and convincing than that for birds, with a broader range of taxa studied and with many more experimental studies. Many ornithologists seem to have the impression that the story related to carotenoid-based plumage coloration and mate choice has been told, and little remains to be done. To the contrary, only the most preliminary phase of research in this field has been completed. Many more experimental studies on a wider range of avian taxa are needed before we can draw firm conclusions regarding the extent of the use of carotenoid ornaments as criteria in mate selection. The evidence for the use of black eumelanin pigmentation as a criterion in avian mate choice is about as strong as that for choice based on carotenoid coloration. A few studies have shown definitely that females assess potential mates based on the size of patches pigmented with eumelanin, but as with studies of carotenoid coloration, more carefully controlled experimental studies on a wider range of avian taxa are needed before we can really know how widespread and important eumelanin ornaments are as criteria in mate choice. In addition, more studies that consider both badge size and color quality of eumelanin ornaments are needed. At present, no firm conclusions regarding the importance of phaeomelanin pigmentation in female mate choice can be made. Experimental manipulations in the field and carefully controlled mate choice experiments in the lab will have to be conducted before we can make a reasonable assessment of the function of phaeomelanin coloration. One interesting, but entirely unstudied, aspect of rusty phaeomelanin coloration is the frequency with which such coloration occurs in combination with blue structural coloration. In two studies, expression of blue structural coloration and expression of orange phaeomelanin coloration were highly correlated. Whether orange and blue coloration occur together because the combination creates an amplified visual display or whether this combination of color displays

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geoffrey e. hill provides better or more complete information on male condition than either trait in isolation remains to be resolved. Because of a surge in interest in UV plumage coloration, there have been a number of recent studies on female mate choice relative to structurally based plumage coloration. The approach of most researchers has been to remove the UV component of color displays, either by using filters that are placed in the front of a male when he is presented to a female or by applying sun-blocking oils to feathers. Few studies have looked at natural variation in expression of structural coloration relative to female mate choice, and virtually no studies have conducted controlled mate choice experiments in which the coloration of males is manipulated so that it mimics natural variation in coloration. Consequently, we can say with certainty that female birds respond negatively to the total removal of UV wavelengths from a plumage coloration display, just as they would surely respond negatively to the removal of red or blue wavelengths, but we can make no statements about the general importance of structural color displays as signals used in mate choice. I encourage colleagues working in the field to move away from the use of agents that block UV wavelengths and instead to use techniques that alter color displays in a more natural manner. It is interesting that the majority of studies of mate choice for carotenoid and structural coloration have focused on color quality, whereas the most studies of mate choice for melanin coloration have focused on the size of color patches. In choosing mates, females are predicted to respond to male characteristics that provide them with reliable and important information. Eumelanin coloration seems to be a poor predictor of individual health or nutritional condition, but a good predictor of social status and resource-holding ability. In contrast, both carotenoid and structural coloration seem to reflect health and foraging ability. It is interesting to speculate that badge size is the best signal of social status and resource-holding potential and hence the focus of assessment for melanin ornamentation, whereas color quality is a better signal of health and condition and hence the focus of assessment of carotenoid and structural ornaments. Color displays that are not produced by melanins, carotenoids, or microstructures are little studied. Perhaps the paucity of these studies makes sense, because most color displays in birds are due to melanins, carotenoids, and microstructures. However, I think that some of these alternative forms of color are particularly deserving of study, because they allow us to test ideas about general principals of signal function in novel systems. Certainly we need many

Female Mate Choice for Ornamental Coloration

additional studies to refine, verify, and reinforce the general themes that have developed regarding carotenoid, melanin, and structural colors, but it seems time to begin to investigate some of the lesser-known color systems as well.

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Female Mate Choice for Ornamental Coloration Møller, A. P. 1990b. Fluctuating asymmetry in male sexual ornaments may reliably reveal male quality. Anim Behav 40: 1185–1187. Mulder, R. A., and M. J. L. Magrath. 1994. Timing of prenuptial molt as a sexually selected indicator of male quality in Superb Fairy-wrens (Malurus cyaneus). Behav Ecol 5: 393–400. Navara, K. J., and G. E. Hill. 2003. Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration. Behav Ecol 14: 909–916. Nicoletto, P. F. 1993. Female sexual response to condition-dependent ornaments in the Guppy, Poecilia reticulata. Anim Behav 46: 441–450. Nicoletto, P. F., and A. Kodric-Brown. 1999. The use of digitally-modified videos to study the function of ornamentation and courtship in the Guppy, Poecilia reticulata. Environ Biol Fishes 56: 333–341. Noble, G. K., and B. Curtis. 1936. Sexual selection in fishes. Anat Rec 64(Suppl 3): 84. Norris, K. J. 1990a. Female choice and the evolution of the conspicuous plumage coloration of monogamous male Great Tits. Behav Ecol Sociobiol 26: 129–138. Norris, K. J. 1990b. Female choice and the quality of parental care in the Great Tit Parus major. Behav Ecol Sociobiol 27: 275–281. O’Donald, P. 1962. The theory of sexual selection. Heredity 17: 541–552. O’Donald, P. 1980. Sexual selection by female choice in a monogamous bird: Darwin’s theory corroborated. Heredity 45: 201–217. O’Donald, P. 1983. The Artic Skua: A Study of the Ecology and Evolution of a Seabird. Cambridge: Cambridge University Press. Omland, K. E. 1996a. Female Mallard preferences for multiple male ornaments. II. Experimental variation. Behav Ecol Sociobiol 39: 361–366. Omland, K. E. 1996b. Female Mallard preferences for multiple male ornaments: I. Natural variation. Behav Ecol Sociobiol 39: 353–360. Palokangas, P., E. Korpimaki, H. Hakkarainen, E. Huhta, P. Tolonen, and R. V. Alatalo. 1994. Female kestrels gain reproductive success by choosing brightly ornamented males. Anim Behav 47: 443–448. Pearn, S. M., A. T. D. Bennett, and I. C. Cuthill. 2001. Ultraviolet vision, fluorescence and mate choice in a parrot, the Budgerigar Melopsittacus undulatus. Proc R Soc Lond B 268: 2273–2279. Pearn, S. M., A. T. D. Bennett, and I. C. Cuthill. 2003. The role of ultraviolet-A reflectance and ultraviolet-A induced fluorescence in the appearance of Budgerigar plumage: Insights from spectrofluorometry and reflectance spectrophotometry. Proc R Soc Lond B 270: 859–865. Peek, F. W. 1972. An experimental study of the territorial function of vocal and visual display in the male Red-winged Blackbird (Agelaius phoeniceus). Anim Behav 20: 112–118.

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geoffrey e. hill Pelkwijk, J. J., and N. Tinbergen. 1937. Eine reizbiologische Analyse einiger Verhaltenweisen von Gasterosteus aculeatus. L. Zeitschr Tierpsychol 1: 193–200. Perrier, C., F. de Lope, A. P. Møller, and P. Ninni. 2002. Structural coloration and sexual selection in the Barn Swallow Hirundo rustica. Behav Ecol 13: 728–736. Phillips, R. A., and R. W. Furness. 1998. Polymorphisms, mating preferences and sexual selection in the Arctic Skua. J Zool Lond 245: 245–252. Potti, J., and S. Montalvo. 1991. Male arrival and female mate choice in Pied Flycatchers Ficedula hypoleuca in central Spain. Ornis Scand 12: 68–79. Price, T. D. 1984. Sexual selection on body size, territory, and plumage variables in a population of Darwin’s Finches. Evolution 38: 327–341. Pryke, S. R., and S. Andersson. 2003. Carotenoid-based status signalling in Redshouldered Widowbirds (Euplectes axillaris): Epaulet size and redness affect captive and territorial competition. Behav Ecol Sociobiol 53: 393–401. Pryke, S. R., S. Andersson, and M. J. Lawes. 2001a. Sexual selection of multiple handicaps in the Red-collared Widowbird: Female choice of tail length but not carotenoid display. Evolution 55: 1452–1463. Pryke, S. R., M. J. Lawes, and S. Andersson. 2001b. Agonistic carotenoid signalling in male Red-collared Widowbirds: Aggression related to the colour signal of both the territory owner and model intruder. Anim Behav 62: 695–704. Reeves, C. D. 1907. The breeding habits of the Rainbow Darter (Etheostoma coeruleum Storer), a study in sexual selection. Biol Bull 14: 35–59. Riters, L. V., D. P. Teague, and M. B. Schroeder. 2004. Social status interacts with badge size and neuroendocrine physiology to influence sexual behavior in male House Sparrows (Passer domesticus). Brain Behav Evol 63: 141–150. Roulin, A. 1999. Nonrandom pairing by male Barn Owls (Tyto alba) with respect to a female plumage trait. Behav Ecol 10: 688–695. Safran, R. J., and K. J. McGraw. 2004. Plumage coloration, not length or symmetry of tail-streamers, is a sexually selected trait in North American Barn Swallows. Behav Ecol 15: 455–461. Saether, S. A., P. Fiske, J. A. Kalas, and J. M. Gjul. 2000. Females of the lekking Great Snipe do not prefer males with whiter tails. Anim Behav 59: 273–280. Sætre, G. P., S. Dale, and T. Slagsvold. 1994. Female Pied Flycatchers prefer brightly colored males. Anim Behav 48: 1407–1416. Sætre, G. P., T. Moum, S. Bures, M. Kral, M. Adamjan, and J. Moreno. 1997. A sexually selected character displacement reinforces premating isolation. Nature 387: 589–592. Senar, J. C., J. Domenech, and M. Camerino. 2005. Female Siskins choose mates by the size of the yellow wing stripe. Behav Ecol Sociobiol 57: 465–469 Sheldon, B. C., S. Andersson, S. C. Griffith, J. Ornborg, and J. Sendecka. 1999. Ultraviolet colour variation influences Blue Tit sex ratios. Nature 402: 874–877.

Female Mate Choice for Ornamental Coloration Siefferman, L., and G. E. Hill. 2003. Structural and melanin coloration indicate parental effort and reproductive success in male Eastern Bluebirds. Behav Ecol 14: 855–861. Siitari, H., J. Honkavaara, E. Huhta, and J. Viitala. 2002. Ultraviolet reflection and female mate choice in the Pied Flycatcher, Ficedula hypoleuca. Anim Behav 63: 97–102. Slagsvold, T. 1986. Nest site settlement by the Pied Flycatcher: Does a female choose her mate for the quality of his house or himself? Ornis Scand 17: 210–220. Smith, D. G. 1972. The role of the epaulets in the Red-winged Blackbird, (Agelaius phoeniceus) social system. Behaviour 41: 251–268. Sorenson, L. G., and S. R. Derrickson. 1994. Sexual selection in the Northern Pintail (Anas acuta): The importance of female choice versus male-male competition in the evolution of sexually-selected traits. Behav Ecol Sociobiol 35: 389–400. Stutchbury, B. J. 1991. The adaptive significance of male subadult plumage in Purple Martins—Plumage dyeing experiments. Behav Ecol Sociobiol 29: 297–306. Sullivan, M. 1994. Discrimination among males by female Zebra Finches based on past as well as current phenotype. Ethology 96: 97–104. Sundberg, J. 1995. Female Yellowhammers (Emberiza citrinella) prefer yellower males: A laboratory experiment. Behav Ecol Sociobiol 37: 275–282. Sundberg, J., and A. Dixon. 1996. Old, colourful male Yellowhammers, Emberiza citrinella, benefit from extra-pair copulations. Anim Behav 52: 113–122. Swaddle, J. P., and I. C. Cuthill. 1994a. Female Zebra Finches prefer males with symmetric chest plumage. Proc R Soc Lond B 258: 267–271. Swaddle, J. P., and I. C. Cuthill. 1994b. Preferences for symmetric males by female Zebra Finches. Nature 367: 165–166. Thornhill, R. 1992. Fluctuating asymmetry and the mating system of the Japanese Scorpionfly Panorpa japonica. Anim Behav 44: 867–879. Thusius, K. J., K. A. Peterson, P. O. Dunn, and L. A. Whittingham. 2001. Male mask size is correlated with mating success in the Common Yellowthroat. Anim Behav 62: 435–446. Torres, R., and A. Velando. 2003. A dynamic trait affects continuous pair assessment in the Blue-footed Booby, Sula nebouxii. Behav Ecol Sociobiol 55: 65–72. Torres, R., and A. Velando. 2005. Male preference for female foot colour in the socially monogamous Blue-footed Booby, Sula nebouxii. Anim Behav 69: 59–65. Trivers, R. L., and D. E. Willard. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 137: 90–92. Veiga, J. P. 1993. Badge size, phenotypic quality, and reproductive success in the House Sparrow: A study on honest advertisement. Evolution 47: 1161–1170. Völker, O. 1937. Über fluoreszierende, gelbe Federpigmente bei Papageien, eine neue Klasse von Federfarbstoffen. J Ornithol 85: 136–146.

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geoffrey e. hill Weisman, R., S. Shackleton, L. Ratcliffe, D. Weary, and P. T. Boag. 1994. Sexual preferences of female Zebra Finches—Imprinting on beak color. Behaviour 128: 15–24. Whitekiller, R. R., D. F. Westneat, P. L. Schwagmeyer, and D. W. Mock. 2000. Badge size and extra-pair fertilizations in the House Sparrow. Condor 102: 342–348. Wolf, W. L., J. M. Casto, V. J. Nolan, and E. D. Ketterson. 2004. Female ornamentation and male mate choice in Dark-eyed Juncos. Anim Behav 67: 93–102. Wolfenbarger, L. L. 1999a. Female mate choice in Northern Cardinals: Is there a preference for redder males? Wilson Bull 111: 76–83. Wolfenbarger, L. L. 1999b. Red coloration of male Northern Cardinals correlates with mate quality and territory quality. Behav Ecol 10: 80–90. Woodcock, E. A., M. K. Rathburn, and L. Ratcliffe. in press. Achromatic plumage reflectance, social dominance and female mate preference in Black–capped Chickadees (Poecile atricapillus). Ethology (in press). Yezerinac, S. M., and P. J. Weatherhead. 1997. Extra-pair mating, male plumage coloration and sexual selection in Yellow Warblers (Dendroica petechia). Proc R Soc Lond B 264: 527–532. Zuk, M., K. Johnson, R. Thornhill, and J. D. Ligon. 1990. Mechanisms of female choice in Red Jungle Fowl. Evolution 44: 477–485. Zuk, M., J. D. Ligon, and R. Thornhill. 1992. Effects of experimental manipulation of male secondary sex characters on female mate preference in Red Jungle Fowl. Anim Behav 44: 999–1006.

5 Function and Evolution of Color in Young Birds rebecca m. kilner

When flipping through any bird guide, the range and diversity of avian coloring is immediately striking. The Magnificent Frigatebird (Fregata magnificens), Resplendent Quetzal (Pharomacrus mocinno), Superb Pitta (Pitta superba), Gorgeous Bush-shrike (Telophorus quadricolor), Beautiful Sunbird (Nectarinia pulchella), and Marvellous Spatuletail (Loddigesia mirabilis), for example, all owe their superlative names to their rich and spectacular colors. When looking at the chicks of these species, however, it is hard to believe that any deserve such exciting names. The dazzling rainbow of plumage and bare parts is not yet developed in young birds, and instead, we see pink or black skin and tufts of white, gray, black, or brown down. When we do see color in chicks, it is usually either red or yellow and typically displayed only briefly (e.g., in the form of mouth flush) as offspring beg for food. In this chapter, I attempt to explain why young birds look so uniformly drab, and why displays of colorful exuberance are so rare and so lacking in diversity.

Why So Dull? Nearly all birds hatch with some down covering the skin. In precocial birds, such as ducks, grouse, and shorebirds, the chick’s body is densely covered in down, whereas in more altricial birds, such as trogons, swifts, and songbirds,

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rebecca m. kilner the down is confined to a few dorsal tufts. This marked difference is apparently the result of a switch in just one developmental parameter. The feathers of both types of offspring develop from germ cells in the epidermis and follow the same developmental pathway (Starck 1998). In precocial offspring, cell proliferation in the feather tip is continuous, whereas in altricial young, it stops early in development, even though cell differentiation continues (Starck 1998). As a result, altricial embryos produce fully developed but miniaturized feathers, which leave large tracts of skin uncovered (Starck 1998). Skin and Plumage Color in Offspring of Altricial Species In many altricial species, the exposed skin is pink (see Plate 21). Occasionally it may take on a yellowish tinge, especially toward the end of the breeding season (e.g., Eurasian Blackbirds [Turdus merula]; pers. obs). In some species, however, such as the Reed Warbler (Acrocephalus scirpaceus), Calandra Lark (Melanocorypha calandra), Zebra Finch (Taeniopygia guttata), and Common Cuckoo (Cuculus canorus), the skin is much darker, varying from gray to almost black. Dark skin coloring is presumably caused by melanin (Chapter 6, Volume 1). Domesticated Zebra Finches occur in several color varieties, and “fawn” birds have a sex-linked recessive mutation that makes them unable to synthesize melanin (Immelman 1965). Nestlings of this variety have much pinker skin than wild-type offspring (Immelmann 1965). Because of the photoprotective effects of melanin (Chapter 6, Volume 1), it is possible that the darker skin has evolved in some species to minimize damaging exposure to sunlight in excessively exposed nests, but this suggestion cannot account for the gray appearance of wild Zebra Finch nestlings, which are shielded from the sun by their domed nests. A similar mutation may be responsible for the two different morphs of nestling Shining Bronze-cuckoo (Chalcites lucidus). The morphs are indistinguishable before hatching, each developing within a similar olive-brown egg. After hatching, they are easily told apart by their skin color; one morph has pink skin, whereas the other has black skin. Of the eight nestlings described by Langmore et al. (2003), four were pink and four were black. The four pink chicks may have been females, the heterogametic sex and therefore able to express the recessive sex-linked melanin mutation, whereas the remaining offspring might have been homozygous males. Intriguingly, three of the four pink chicks were parasites of the Buff-rumped Thornbill (Acanthiza reguloides), which has a relatively well-lit domed nest, and three of the four black chicks

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were raised in the much darker nest of the Yellow-rumped Thornbill (A. chrysorrhoa). However, the functional significance of the different skin colors and the possible role of skin color in preventing chick rejection by hosts remain to be discovered (see Langmore et al. 2003). The function of European Starling (Sturnus vulgaris) skin has recently been investigated by Jourdie et al. (2004). To our eyes, the skin of young starlings looks pink, but starling skin also reflects ultraviolet (UV) light. The skin of nestlings with stronger immune systems reflects more UV light than that of nestlings with weaker immune systems. When sun-block was smeared over the bodies of starling chicks, reducing the extent of UV reflectance, they gained weight more slowly than did nestlings covered with a control substance that permitted reflectance in the UV. Jourdie et al. (2004) concluded from these data that starling skin functions to advertise the state of a nestling’s health and that parents adjust their provisioning decisions accordingly. Whether other species can also reveal their health through their skin color is unclear. The skin of nestling Eurasian Blackbirds reflects little UV light (Hunt et al. 2003), making UV coloration an unlikely channel of communication between parents and offspring in that species. Although the functional significance of nestling skin color is relatively poorly known, the role of skin in minimizing water loss is better understood. The nestling’s epidermis is packed with lipids, which means that nestlings have a far lower rate of water loss through their skin than do adults (Starck 1998). Perhaps the risk of water loss provides a proximate explanation for the general absence of dark blue, light blue, and green skin coloring in altricial chicks (see, e.g., Baicich and Harrison 1997), coloration that is seen widely in the skin of adult birds (Plate 16). In adults, these colors are produced by a thick layer of parallel collagen fibers in the dermis that scatters light and causes constructive interference (Chapter 7, Volume 1). Perhaps equivalent structural colors are too costly for nestlings to produce because they increase the risk of water loss through the skin. The small tufts of feathers that are present in newly hatched altricial young vary among species from white through gray and brown to black and are presumably pigmented with melanin. Yellow domesticated Common Canaries (Serinus canaria) lack any melanic pigmentation, and their offspring have white patches of down. The nestlings of wild-type Common Canaries, in contrast, have gray downy tufts (Harrison and Castell 1998). The function of these tufts is unknown. Perhaps they are thermoregulatory, because they are distributed only on the parts of the nestling’s body that are left exposed when

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adults are not brooding (Ticehurst 1908). The naked ventral side of the chick is then typically pressed against the nest lining, and its bare flanks are commonly pushed against other nestlings, packed tight in the nest cup. The color of the tufts may improve temperature regulation (see below) or it may promote crypsis, perhaps camouflaging offspring by concealing them (in the case of black tufts) or by simulating an empty lined nest (with white tufts). It would be interesting to test these ideas by examining the associations between nest design, brood size, and tuft coloring across altricial species. The long, white, limp feather shafts that adorn the black skin of Pheasant Coucal (Centropus phasianus) chicks are particularly striking (Plate 23). They may function to influence adult provisioning rates by creating an arresting visual display as the brood gapes for food, revealing orange gapes against a background of black skin and white trails of hairlike feathers. Plumage Color in Precocial Species In most precocial species, and in some altricial species as well (e.g., herons, hawks, eagles, vultures), young chicks are covered in downy feathers at hatching. The plumage may be uniformly black (e.g., rails), white (e.g., swans), yellow (e.g., Domestic Chickens [Gallus gallus]; Plate 17, Volume 1), or brown (e.g., Common Eider [Somateria mollissima]). Ducklings are countershaded to be much darker on their back than their underside, presumably for camouflage (Bradbury and Vehrencamp 1998). Crypsis may be further enhanced by disruptive coloring with yellows and browns. In grebes and gallinaceous birds, the darker dorsal surface of chicks is striped with brown and yellow, whereas in sandpipers, coursers, plovers, terns, and gulls, the downy plumage of chicks is mottled. In some species, chicks are polymorphic in their down color, exhibiting as much variation within and between populations as might be seen between species. Perhaps understanding variation within species can provide clues to explaining variation in plumage color and patterning between species. The terns might be especially useful in this regard (see Table 5.1). One possibility is that the color of down functions to camouflage offspring from predators, and plumage variation within and between species has evolved to match different habitats. For example, Chaniot (1970) described three morphs of Caspian Tern (Sterna caspia) chicks at his study site near San Francisco: a light, intermediate, and dark phase. He suggested these three phases each corresponded with one of the three color zones of his study site, and so

Function and Evolution of Color in Young Birds Table 5.1. Variation in Chick Plumage for Terns of the Western Palearctic Species

Latin name

Chick plumage

Gull-billed Tern Caspian Tern Royal Tern Swift Tern Lesser Crested Tern

Gelochelidon nilotica Sterna caspia S. maxima S. bergii S. bengalensis

Sandwich Tern Roseate Tern Common Tern Arctic Tern White-cheeked Tern Bridled Tern Little Tern Whiskered Tern Black Tern White-winged Tern Brown Noddy

S. sandwichensis S. dougallii S. hirundo S. paradisaea S. repressa S. anaethetus S. albifrons Chilidonias hybridus C. niger C. leucopterus Anous stolidus

Polymorphic (uniform gray buff or ochre) Highly variable Highly variable Variable Polymorphic (pale gray, pale buff, off-white) Highly variable Polymorphic (buff or pale-gray) Not variable (buff ) Polymorphic (pale gray or buff ) Polymorphic (pale gray or buff ) Variable Variable Not variable (buff ) Not variable (cinnamon buff ) Not variable (buff-brown) Polymorphic (white, brownish-black, intermediate)

Source: Descriptions from Cramp et al. (1977–1994).

functioned to camouflage nestlings raised in different environments. The palest morph was similar in coloring to the guano deposits on 5% of the study site; the darkest morph was a bit paler than the dark coloring caused by the chitin exoskeletons of dead brine flies on 15% of the study site. The intermediates matched the mud color on the remaining 80% of the study site. Although the frequencies of the three morphs did not correspond with the availabilities of the different habitats in the San Francisco population, evidence from other populations is more consistent with his suggestion. In the Baltic region, 90% of Caspian Terns nest on flat stone surfaces, which become whitewashed with guano, and the white phase is the most common chick morph is the Baltic population (Chaniot 1970). Brown Noddy (Anous stolidus) chicks also have three color morphs, and there is geographic variation in the frequencies of these morphs (Table 5.2). Dorward and Ashmole (1963) suggested that these differences may be explained by variation in habitat, which, for instance, might render the dark phase most cryptic in the Seychelles but the intermediate phase most cryptic on Christmas Island. They also suggested that habitat differences could impose

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Table 5.2. Geographical Variation in the Frequencies of the Three Plumage Morphs in Brown Noddy Chicks Site Ascension Island Christmas Island Seychelles Goenoeng Api Dry Tortugas (1908) Dry Tortugas (1935)

Pale morph (%)

Dark morph (%)

Intermediate morph (%)

84 10 10 50 35 99

2 90 0 50 0 0

Source: Data from Dorward and Ashmole (1963).

thermoregulatory constraints on plumage color. In exposed habitats, for instance, they argued that dark chicks may quickly overheat, whereas white chicks would succumb less easily following prolonged periods in the sun. Recent experimental work, however, indicates that white chicks are in fact more vulnerable to overheating than are dark chicks. The findings seem counterintuitive at first, but these responses simply result from the way in which differently colored plumage influences the chick’s core temperature. Black plumage may heat up more quickly in the sun, but peripheral temperature changes have relatively little effect on core body temperature (Stoutejesdijk 2002). The key variable is the depth to which solar radiation can penetrate. Thick, fluffy, white plumage lets more solar radiation through and so has a greater effect on the chick’s core temperature. In cooler environments, and especially those with some wind, white downy plumage might provide an effective means of saving metabolic energy that would otherwise be devoted to thermoregulation (Stoutejesdijk 2002). In hotter environments, black might be the optimal plumage color for avoiding overheating (Wolf and Walsberg 2000). In Brown Noddies, the three distinct color phases might be caused by a single mutation in the melanocortin gene (c.f., Mundy et al. 2004; Chapter 11, Volume 1). Disruptive selection, caused by either differential predation on each morph or differential ability to thermoregulate in any particular habitat, could explain why the three morphs persist (Galeotti et al. 2003). But in other tern species, such as Royal Terns (Sterna maxima; Buckley and Buckley 1970), Caspian Terns, and Common Terns (S. hirundo; see also Table 5.1), there is continuous variation in chick appearance. It is possible that habitat differences or thermoregulatory constraints also account for continuous variation in the appearance of these chicks.

Function and Evolution of Color in Young Birds

Alternatively, individual variation in chick plumage color may persist because it allows accurate identification of individual offspring when young are raised in crowded colonies (Chaniot 1970; Buckley and Buckley 1972; Shugart 1990; Palestis and Burger 1999; Chapter 2). Anecdotal and experimental evidence from three species suggest that parents and siblings are able to recognize relatives from an early age and that recognition is based in part on visual cues. For example, Buckley and Buckley (1972) switched two pairs of Royal Tern chicks between nests shortly after hatching and observed that parents quickly found their own offspring, even though they were sitting in the wrong nest. Caspian Tern parents have similar discriminatory abilities, and these are probably based on plumage pattern differences. When presented with pairs of foreign chicks, in which one young bird resembled their own offspring while the other did not, parents were more likely to reject and peck at the odd-looking chick (Shugart 1990). How might individuals use plumage-based signatures to recognize kin? One possibility is that individuals learn the signature of the relative during a critical period, in which kinship can be reliably inferred from a contextual rule-ofthumb (Beecher 1982). For example, parents might learn the appearance of their nestlings immediately after hatching because any offspring in their nest at this point must be their own young. Common Tern nestlings appear to use this system for recognizing their siblings and are adept at distinguishing nest mates from foreigners, at least in the laboratory. They have no innate concept of kin, however, and prefer instead to associate with familiar offspring from the same nest, whom they identify primarily through visual cues. Interestingly, Common Tern chicks not only learn to recognize and associate with their nest mates, they also learn to recognize and avoid near neighbors, the individuals with whom they are most likely to be mixed. When presented with the choice of associating with a nest mate or a completely unfamiliar bird, Common Tern chicks showed no clear preference for either type of nestling. Therefore chicks of this species seem able to discriminate only between known individuals from their immediate neighborhood and are unable to pick out known kin from a crowd of strangers (Palestis and Burger 1999). By contrast, the anecdotal evidence from Royal Terns suggests that parents of this species can spot relatives in a crowd. Perhaps because offspring of this species vary so much between families, and in so many dimensions, such as bill color, the color of their legs and feet, the ground color of their plumage, and the extent of breast spotting (Buckley and Buckley 1970), there is enough information to reliably identify kin, even in a large group (Beecher 1982).

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rebecca m. kilner Kin recognition is not confined to parents raising downy offspring and has been intensively studied in colonial nesting Bank Swallows (Riparia riparia) and Cliff Swallows (Hirundo pyrrhonota; e.g., Beecher et al. 1981a,b; Stoddard and Beecher 1983). The need for kin recognition in Bank Swallows arises only toward the end of the nestling period, because adults never mistakenly visit the wrong burrow to provision chicks. However, when offspring are about 16 or 17 days old, and before they fledge, they start to move between nests. Females commonly evict foreign chicks from their burrows, but males are prone to misfeeding strangers (Beecher et al. 1981a). Cross-fostering experiments suggest that females are able to recognize their own young only when they reach 16 or 17 days of age. At this point, offspring start to make a distinctive two-note call that advertises their identity and enables recognition (Beecher et al. 1981b). Colonially nesting Cliff Swallows are similarly able to recognize their offspring, but in this species, visual cues might be used in addition to vocal signatures in individual identification. Stoddard and Beecher (1983) noticed that the faces of Cliff Swallow nestlings start to become distinctive when they are about 13 days old, mostly as a result of variation in the quantity and distribution of white feathers (Plate 9). Furthermore, there were noticeable family resemblances in facial plumage patterns. Why does this species need two modalities for recognition, when Bank Swallows can get by with vocal signatures alone? Stoddard and Beecher (1983) argued that family-specific calls are localized to individual nests in the Bank Swallow because the sandy banks in which these birds nest absorb sound so effectively that birds are unlikely to hear the calls of a neighboring family. In this species, the risk of error in recognition through vocal signatures seems remote. By contrast, the mudcups in which Cliff Swallows nest are far more reverberant, so nestling calls can easily be overheard by neighbors, which increases the risk of misidentifying kin. Consequently, facial recognition may have evolved in this species to improve the accuracy of kin recognition. If the major selective pressures that govern chick coloring favor crypsis and efficient thermoregulation, then it is not hard to understand why most offspring have dull plumage. Perhaps signatures for kin recognition are also drab because brighter coloring would be too costly, carrying a high risk of attracting predators. Signals that facilitate recognition are more likely to be “conspiratorial whispers,” cheap forms of communication that are to the mutual benefit of sender and receiver alike (Dawkins and Krebs 1979). In addition, information about identity may be more efficiently transmitted when it is

Function and Evolution of Color in Young Birds

encoded in a black-and-white pattern (functioning like a barcode) than when it involves a more colorful display, which might be corrupted either by partial shading or when viewed through the filtered light that typically illuminates nest sites (Chapter 4, Volume 1).

When Does Color Evolve? Despite the preponderance of species with drab natal down, colorful plumage and bare parts on young birds have evolved at least six times in birds: in the terns (Sternidae), the hoopoes (Upupidae), the cuckoos (including the nonparasitic Crotophagidae and Centropodidae), the rails (Rallidae), the grebes (Podicipedidae), and the perching birds (all the families in Passeriformes). Of these taxa, only the offspring of rails display orange or red downy plumage (Plate 22). In the remaining families, bright coloring is confined to bare parts in the head regions of young birds (Plates 21–23). Why should only these families of birds have evolved brighter coloring of young? Each produces altricial young, which must compete for parental attention. I investigated whether the evolution of bright coloration of young is associated with an increased level of sibling competition by using clutch size as a measure of competitive intensity. Clutch size data were taken from Bennett and Owens (2002), and I used a family-level phylogeny based on Sibley and Ahlquist (1990), with the amendments suggested by Barker et al. (2001) for the passerines. To control for the potentially confounding effects of phylogeny, I analyzed the data using the comparative analysis by independent contrasts program (CAIC; Purvis and Rambaut 1995). The analysis revealed that more colorful offspring tended to hatch from larger clutches, but with so few contrasts available for analysis, the trend was not significant (R. M. Kilner, unpubl. data). A similar pattern was found within one family, the rails (Krebs and Putland 2004), whose chicks are among the most ornamented of all avian offspring (see Plate 22). Virtually all young rails have black downy plumage, but some, such as the Eurasian Coot (Fulica atra), display a bright red, bald crown, encircled with orange downy feathers. Their eyelids are shaded blue, and the bill is scarlet. Krebs and Putland (2004) mapped the appearance of rail chicks onto a morphological phylogeny of the Rallidae. Their analyses suggested that the ancestral rail chick was rather drab in appearance, and that ornamentation subsequently evolved between 14 and 20 times. Bright coloration in chicks has been secondarily lost at least once, and perhaps as many as six times. The

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rebecca m. kilner evolution of chick ornamentation in rails was associated with larger clutches and a polygamous mating system (Krebs and Putland 2004). The most obvious interpretation of these results is that offspring coloration must have evolved as the result of competition among siblings for parental resources. The more that chicks are challenged in contests for resources, either by more siblings or by siblings with lower average relatedness, the more competitive offspring must be and the more necessary color signaling might be. However, sibling competition alone cannot explain the evolution of bright nestling color. If color gives offspring a competitive edge, it is because it appeals to some aspect of parental psychology. Several lines of evidence suggest that colorful displays are directed at the adults tending offspring rather than at competing siblings. First, the most viciously combative offspring (e.g., herons, eagles, egrets) do not display bright patches of color when fighting for food. Furthermore, color patches do not appear to give physically dominant offspring a competitive edge. On the contrary, in American Coots (Fulica americana), color improves the provisioning success of only the smaller chicks in the brood (Lyon et al. 1994). Similarly, Nuechterlein (1985) observed that the redness of the bald head patch of a Western Grebe (Aechmophorus occidentalis) chick was not correlated with its dominance status. In addition, patches of color displayed by chicks in broods do not simply determine success in the competition for food (Götmark and Ahlström 1997; Kilner 1997; Heeb et al. 2003); they also determine how often the brood is supplied with food (e.g., Common Canaries: Kilner 1997; Reed Warblers: Kilner et al. 1999; Great Tits [Parus major]: Hinde 2004). Finally, color patches can convey information to parents that might influence their provisioning decisions. For example, frontal shields and bills are more brightly colored in Common Moorhen (Gallinula chloropus) chicks that are larger and fatter (Fenoglio et al. 2002). In most species, the pattern of food distribution within the brood results partly from parental choice and partly from physical interference among offspring, although the relative influence of parental choice and nestling competition probably varies from species to species (Kilner 2002a). Interestingly, the most elaborately ornamented nestlings appear to have evolved in the Rallidae (Plate 22), the Viduidae (Plate 21), and the Estrildidae (Plate 21), families in which parents exercise absolute authority over food distribution, even to the extent of killing surplus offspring (Horsfall 1984; Burley 1986; Payne et al. 2001). I have already discussed rail chick ornaments. Estrildid and viduid nestlings are remarkable for the spottings and swellings that adorn and sur-

Function and Evolution of Color in Young Birds

round their gapes (Plate 21). The palate is typically pinkish white (but can be red, yellow, or blue) and spotted with black or violet, and the number of symmetrically arranged dots varies between species. Sometimes the spots blend together, forming horseshoe patterns (e.g., the Plum-headed Finch [Neochmia modesta]). The tongue may be spotted as well, and is waved from side to side as nestlings demand food (Müller and Smith 1978). On the outside of the gape, there are globular papillae at the proximal corners of the lower and upper mandibles, and these can be white, blue, yellow, red, or purple. Because parents appear to have complete control over food distribution in rails as well as in estrildid and viduid finches, offspring can compete only by attracting parental attention. Perhaps the need to signal to parents accounts for the unusually elaborate ornamentation seen in these chicks. The differences in chick coloration between the rails and estrilid/viduid finches is intriguing as well. Such differences may be explained simply by the very different environments in which young rails and finches must signal for food. But perhaps there has been parental choice for these displays as well, which started as an arbitrary sensory bias but which ran away to extreme ornamentation, in a process analogous to Fisherian sexual selection (West-Eberhard 1983; Lyon et al. 1994).

Nestling Mouth Markings Nestling mouths are decorated with spots in other passerine species as well, although the patterns are less extraordinary than those displayed by gaping estrildid and viduid finches (see the Dunnock [Prunella modularis] gape in Plate 22). In some red-mouthed species, such as cuckoos, the gape may be decorated with a few white spots; this pattern is also found in Bearded Tit (Panurus biarmicus) nestlings, in whom white spots adorn a black mouth (Ingram 1907). Those yellow- or orange-mouthed species that display mouth markings carry just two or three black spots on their tongues or palates (e.g., Reed Warbler, Dunnock, Crested Lark [Galerida cristata]), which sometimes merge to form horseshoe patterns. I mapped the incidence of black mouth spotting onto the phylogeny of passerine tribes devised by Barker et al. (2001) and discovered that spotting has evolved on three independent occasions: in the accentors, viduid, and estrildid finches (Prunellidae, Viduidae, and Estrildidae); the larks and cisticolas (Alaudidae, Cisticolidae); and the warblers (Sylviidae: Acrocephalinae, Megalurinae, and Sylvinii; R. M. Kilner, unpubl. data). Mouth spots are probably melanic in origin, given that they are lacking in leucistic

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rebecca m. kilner Zebra Finches, which display an immaculate white gape as they solicit food (Immelmann et al. 1977). The function of nestling mouth and tongue markings remains largely unresolved, although several hypotheses have been advanced and tested. One possibility is that such markings simply enhance chick conspicuousness. If this is the case, then leucistic Zebra Finches raised alongside wild-type Zebra Finch nestlings (which bear a complete set of mouth marks) should obtain less food. However, the evidence to support this prediction is mixed. When the birds were bred in captivity, with abundant supplies of food, there was no indication that the spot-free offspring thrived less well than their nest mates (Skagen 1988; Reed and Freeman 1991). Once food was restricted, however, the chicks lacking mouth markings were placed at a distinct disadvantage (Skagen 1988). One explanation for these results is that parents always feed the most prominent offspring first, which penalizes the least obvious nestlings, but only when food is in short supply. Another hypothesis is that nestling mouth markings signal information to parents. For example, Payne (1997) proposed that colored mouth spots and gape papillae function to advertise nestling health. He observed that the mouth patterns displayed by young Aurora Finches (Pytilia phoenicoptera) were paler when nestlings were infested with the mite Pellonyssus reedi, and also that the mouth coloration faded rapidly after death. Mouth spots may also function to signal identity. Offspring of the Brown Songlark (Cinclorhamphus cruralis), one of the most sexually size-dimorphic birds in the world (Magrath et al. 2004), display orange-yellow gapes marked with black patterns as they beg for food, and parents supply sons with better quality food than they do daughters (Magrath et al. 2004). Meerloo (2003) investigated whether parents might recognize sons by a sex-specific signal encoded in their gape markings, but found that all the sex differences in mouth pigmentation could be explained simply by the pronounced size dimorphism. Another hypothesis is that mouth spots interact with the coloring of the gape to increase parental responsiveness, not because the markings improve chick conspicuousness or signal nestling quality, but because they present a more potent stimulus to parents when viewed in conjunction a brightly colored mouth (Rowe 1999). Mouth spots could thus provide a powerful psychological tool for offspring attempting to extract more investment than parents wish to supply (Kilner 2002b). Perhaps the white papillae adorning the red mouths of young Great-spotted Cuckoos (Clamator glandarius) function in this way, to take resources from unwitting Black-billed Magpie (Pica pica) hosts. Field

Function and Evolution of Color in Young Birds

experiments found that parasitic young competing with magpie chicks for food were less successful when the papillae were obscured with red food coloring (Soler et al. 1995). In other cuckoo species, nestlings display black gape patches, even though they evict host young from the nest and so are not in need of psychological tricks to further promote their competitive ability. For example, the lower and upper palate of the Little Cuckoo (Cuculus poliocephalus) has a black dot at each distal tip, whereas the Oriental Cuckoo (C. saturatus) has a pair of triangular black patches on each side of its upper palate. However, neither cuckoo species parasitizes hosts that display mouth markings, and the function of these patches remains to be determined (Tojo et al. 2002).

Runaway Competition for Parental Attention The observations by Soler et al. (1995) of the Great-spotted Cuckoo raise an interesting question: why haven’t host magpie chicks evolved the same psychological trickery as the Great-spotted Cuckoo to gain an advantage in sibling competition? The answer to this question may lie in kinship asymmetries between the parasite and host young. Brood parasitic nestlings have a greater incentive than the host young to use new strategies in the competition for food, because their selfishness is unconstrained by kinship. The presence of a young brood parasite in the nest may itself promote more competitive behaviors among the host nestlings, because the parasite reduces the average relatedness of the brood members. Nevertheless, the parasitic chick should be the first to develop novel strategies for exploiting psychological weaknesses in its foster parents, because the average relatedness between the parasite and the host young will always be lower than the average relatedness between an individual host nestling and the chicks with whom it shares the nest. A generalist parasite, such as the Great-spotted Cuckoo, which exploits magpies at a relatively low frequency (Davies 2000), will always be one step ahead of host young in its use of novel psychological means of exploiting host parents (Dawkins and Krebs 1979). A prolonged and specific history of interaction between brood parasites and their hosts, however, may result in the evolution of increasingly elaborate begging displays, as parasitic young attempt to outpace host young in the evolutionary battle to win parental attention. The process might begin when the parasite hits on a novel display that more effectively exploits host parents, thus giving it a competitive edge for gaining parental attention. Under selection to be more competitive themselves, the host chick’s begging strategies then

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rebecca m. kilner converge on the parasite’s, reducing the competitive prowess of the parasite until it comes up with a better visual stimulus. This runaway process could come to a stable conclusion with parasitic and host young using similar begging displays, but only if hosts start to discriminate against odd-looking parasitic nestlings, or if sibling parasites are commonly reared in the same nest, thereby reducing the relatedness asymmetry between parasitic and host young. Can runaway competition account for the evolution of the highly intricate mouth ornaments seen in young parasitic viduid finches? At least one alternative explanation for the evolution of elaborate gape ornamentation has been advanced previously. The hypothesis is that complex ornamentation results from an evolutionary arms race between adult hosts and nestling brood parasites, in which hosts develop ever more elaborate gape signatures for recognizing their own young, and nestling parasites mimic host young to escape detection (Davies 2000). In this scenario, the runaway elaboration of nestling gape ornamentation is initiated by selection on hosts to avoid the costs associated with parasitism, and it escalates as a result of co-evolution between adult hosts and nestling parasites. By contrast, the runaway competition hypothesis suggests that complex gape morphologies initially arose in parasitic nestlings selfishly seeking to exploit host parental attention, and they became progressively more elaborate as a consequence of competition with host young. Both hypotheses predict that species with a history of brood parasitism should display more elaborately ornamented mouths than those without. Furthermore, closely related parasitized species should exhibit greater diversity in their mouth patterns than do closely related species with no record of exploitation by parasites. At first sight, there seems to be little evidence to support either prediction. The Australasian estrildid finches all display elaborate mouth markings, and they are not exploited by brood parasites (Payne 1997). Although the young of most species in this family have pinkish-white palates and vary primarily in the number and density of black mouth markings (Immelmann 1965), at least two species, the Gouldian Finch (Chloebia gouldiae) and Red-throated Parrotfinch (Erythrura psittacea) have colorful gapes and display gape papillae. Therefore brood parasitism alone cannot explain the evolution of elaborate gape patterns. There is some anecdotal evidence, however, that suggests that parasitism might enhance the complexity of mouth patterns. Payne et al. (2002) report a recent switch to a novel host by the Village Indigobird (Vidua chalybeata). Nestlings of the old host, the Red-billed Firefinch (Lagonosticta senegala), and the parasite look very similar, each displaying yellow palates decorated with three black spots and white gape papillae

Function and Evolution of Color in Young Birds

bordered with blue. The new host, the Brown Firefinch (Lagonosticta nitidula), has offspring that look quite different. Their mouths are pinkish white (like the unparasitized Australian finches) and marked with three black spots, but their white gape papillae lack the blue borders seen in the old host (Payne et al. 2002). The runaway competition hypothesis can also explain why the gape ornaments displayed by the parasitic viduid nestlings so closely match the mouth patterns displayed by offspring of their particular hosts (see Plate 21). Again, it is foreshadowed by an earlier explanation. According to this earlier view, parasites change their mouth markings to match those of their hosts, which stay unchanged as a consequence of parasitism (Nicolai 1974). Parasites benefit by mimicking host young, either because it enables them to tune into the usual host offspring-parent communication system or because it prevents recognition and rejection (Payne et al. 2001). Thus the means by which host young communicate with their parents are locked and unperturbed by parasitism. The parasitic nestling must tap into this existing signaling system if it is to obtain care for itself. By contrast, the runaway competition hypothesis suggests that host parents are psychologically vulnerable and can be induced to provide more care if presented with a sufficiently attractive visual stimulus. Under this hypothesis, the parasite’s task is to obtain a competitive edge by finding the host parents’ psychological weakness. In so doing, it changes the usual means of communication between host young and parents. Table 5.3 outlines and tests a number of contrasting predictions generated by these two competing hypotheses. The results suggest that the runaway competition hypothesis provides the better explanation for the similarities in host and parasite gape morphologies. It would be interesting to test this idea further in future work.

What Colors Do Offspring Display? Sexual Dichromatism Much of the extraordinary diversity in adult bird coloration is confined to males and probably results from sexual selection (Andersson 1994; Chapters 3 and 4). Sexual dichromatism is rare among offspring, however, and when it does occur, it is apparent only toward the end of the dependent period. In several species, the particular dichromatism seen in the nest simply anticipates the sex differences in color displayed in adulthood. For example, 14 days after hatching, the tails of male Blue Tits (Parus caeruleus) reflect more

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Table 5.3. Comparison of Two Hypotheses on the Evolution of Mouth Markings in Parasitic Viduid Finches Prediction Parasites mimic host young to obtain care Hosts show neither preference for nor discrimination against odd-looking offspring if their regular parasite is nonmimetic (e.g., Goldbreast [Amandava subflava]), but discriminate against odd-looking young if the parasite and host young look alike (e.g., Red-billed Firefinch [Lagonosticta senegala]) Runaway competition Hosts favor some odd-looking offspring if their regular parasite is nonmimetic (e.g., Goldbreast), but may discriminate against odd-looking young if the parasite and host young look alike (e.g., Red-billed Firefinch) Parasitic offspring should be more attractive to host parents than closely related non-parasites

Evidence Prediction not supported: No significant difference in the likelihood of Goldbreasts and Red-billed Firefinches fledging odd-looking (nonparasitic) offspring (Fisher Exact P = 0.25; Payne et al. 2001)

Prediction supported: Goldbreasts are more likely to raise Village Indigobirds (Vidua chalybeata) than other foreign finch species (Fisher Exact P = 0.02), whereas Red-billed Firefinches discriminate against all odd-looking young Prediction supported: Both Red-billed Firefinches and Goldbreasts are more likely to raise Village Indigobirds than nonparasitic estrildid finch young

Source: Data from Payne et al. (2001).

UV light than those of females, a pattern that persists in later life (Johnsen et al. 2003). Similarly, young Eclectus Parrots (Eclectus roratus) develop their sex-specific plumage as nestlings (R. Heinsohn, pers. comm.; Plate 19), and male Southern Emu-wrens (Stipiturus malachurus) are distinguishable from females in the nest through the display of their sky-blue bibs (G. S. Maguire, pers comm.). Rarely, offspring advertise their sex with a display that is not seen again after maturity. Male Blue Tits have more intensely colored yellow breast plumage than do females as nestlings, but do not differ in this regard as adults (Johnsen et al. 2003). Female nestling European Bee-eaters (Merops apiaster) bear a dark greenish patch on their chestnut crown patch, which disappears on maturity (C. M. Lessells, pers. comm.). It is interesting that many sexually dichromatic species choose not to reveal their sex as offspring. Perhaps sexual selection in these species is so strong that one sex would consistently receive less parental investment and so chooses to

Function and Evolution of Color in Young Birds

conceal that information for as long as possible. Why, then, do nestling beeeaters and Blue Tits advertise their sex with plumage specifically designed for that purpose alone? Analyses by Lessells (2002) identify a condition in which sexual advertisement can evolve, even though daughters who declare their sex as offspring are penalized as a result. She showed that, when the marginal returns of investing in sons are high, daughters gain so much inclusive fitness through their brothers that this offsets the fitness they lose as a result of their parents’ favoritism toward sons. Hence there is no incentive for daughters to conceal their sex. Seeing Red The blues and greens seen in sexually dichromatic young birds are rare in other nestlings. The colors more typically displayed by offspring range from yellow to red (Plate 22), at least when viewed by human eyes. Some also involve reflectance in the UV (Figure 5.1), yielding nonspectral colors analogous to purple as seen by humans (Hunt et al. 2003). Only rail chicks display brightly colored feathers on hatching (see Plate 22). They have yellow, orange, or red coloration on their heads and necks that extends down the back and across the wings (Taylor and van Perlo 1998). The coloration may be due to carotenoids, but this supposition has not been tested in chicks from this family (Chapter 5, Volume 1). The colored feathers are lost before chicks reach maturity, suggesting that their principle function is served during the period in which offspring are cared for by their parents (Lyon et al. 1994; Krebs and Putland 2004). Lyon et al. (1994) tested the function of bright feather coloration in American Coot chicks by cutting the colored portion off their head plumes. Chicks thus deprived of orange head ornamentation obtained less food than did control nestlings and grew more slowly as a result (Figure 5.2). Bare Skin Patches Colored by Differential Blood Flow In some families, color is displayed through bare patches of skin, which quickly change color as a result of differential blood flow. The bald heads of young rails, for example, are redder in hungrier chicks (Boyd and Alley 1948). Similar color changes are seen in grebes. Newly hatched Pied-billed Grebes (Podilymbus podiceps) possess a bare loral patch that changes from flesh ochre to crimson red as chicks beg for or receive food from their parents (Forbes and Ankney 1987). At least eight of the 20 or so grebe species also have a triangular

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Figure 5.1. Spectral reflectance of the mouths and surrounding flanges of nestling European Blackbirds and the background of their nest. Adapted from Hunt et al. (2003).

bare patch on the crown, which also becomes redder when the chick is begging for food. Young Great-crested Grebes (Podiceps cristatus) and Silvery Grebes (P. occipitalis) can vary the color of the crown and loral patches independently for reasons that are unknown (Nuechterlein 1985). Podilymbus and Poliocephalus species generally lack the bare crown and have a contrasting patch of rufous plumage on the crown instead. In the Pied-billed Grebe, the bare crown spot disappears within a few days of hatching and is replaced by rufous down (Storer 1967). It would be interesting to know which is the ancestral condition in this family, the bare patch or the rufous crown. Perhaps rufous crown feathers represent an attempt by chicks to cheat the signal from the bare patch by displaying a permanently reddish head. Conversely, perhaps the bare crown patch evolved to exploit a pre-existing parental sensory bias for red crowns (see also Lyon et al. 1994). The mouth colors of species from at least four passerine families, Corvidae (E. Gwinner, pers. comm., cited in Kilner and Davies 1998), Pycnonotidae (Swynnerton 1916), Passeridae (Clotfelter et al. 2003) and Fringillidae (Kilner 1997; Kilner and Davies 1998), can also change in redness, presumably as a result of becoming suffused with blood. In Dark-eyed Juncos ( Junco hye-

Feeding rate (feeds•chick–1•min–1)

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Figure 5.2. The rate at which American Coot chicks with and without their orange head plumes received food. In “orange control” broods, all chicks were left intact, whereas in “black control” broods, all chicks were trimmed of their orange head feathers. In experimental broods, half the brood was left intact (orange) and the other half was trimmed (black). Note that parental preference for the orange head plumage is relative rather than absolute. Box plots show medians, interquartile ranges, and tenth to ninetieth percentiles. Redrawn from Lyon et al. (1994).

malis), mouth color changes gradually (on an hourly time scale), becoming paler if chicks lose heat (Clotfelter et al. 2003). In the remaining species, the color change is more immediately obvious, as the mouth rapidly flushes from pink to crimson following the onset of begging. Such rapid change in mouth coloration was probably first noticed by Swynnerton (1916:285), who describes a young bulbul begging for food: “The mouth is . . . sometimes brighter than at others, even nearly carmine. I found, in fact, that when I opened the mouth myself it was dull brownish in coloration, the bright color . . . being evidently due not to pigment but to a rush of blood to the mouth under the stimulus of eagerness.” In the cardueline finches (Fringillidae), the flush reddens the gape to a greater extent when nestlings are hungrier, at least in the days immediately following hatching (Kilner 1997; Kilner and Davies 1998). Older Common Canary chicks display intensely colored pink mouths as they solicit food, and the flush in redness is much less noticeable than in chicks a few days past hatching.

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A simple trade-off in blood use may allow parents to accurately infer the hunger of young nestlings from their mouth color. Perhaps in very young birds, blood is diverted to the gut soon after eating, which means that offspring cannot misrepresent their true hunger by displaying a red mouth if they have recently received food (Kilner 1997). It may be easier for older nestlings to escape this physiological bind on reliable signaling, perhaps because they have acquired enough carotenoid pigments to permanently color their mouths or because they can more easily afford to satisfy the blood flow demands of both the gut and the gape. The use of regulated blood flow through bare patches as a signal to parents has evolved at least five times in birds (in Podicepidae, Rallidae, Corvidae, Pycnonotidae, and Passeroidea). The species that exhibit these displays have in common a high degree of parental control over food allocation within the brood, although parental authority arises in different ways. In the rails and grebes, chicks that seek a different pattern of food distribution to the one preferred by parents are punished (Horsfall 1984; Forbes and Ankney 1987), with parents roughly tousling chicks that demand food out of turn. Common Ravens (Corvus corax) and the cardueline finches make it difficult for a competitively dominant chick to monopolize food, because parents regurgitate food for their young and can therefore divide resources among several nestlings at each nest visit. In these species, parents spend longer at the nest provisioning young and so have the time to assess finely graded signals of need. Furthermore, their response can be just as fine-tuned as the signal, because food items can be readily subdivided among chicks (Kilner and Davies 1998). Perhaps when chicks have greater physical control over the distribution of food, they have less to gain from signaling to parents. And if parents routinely dole out large, single items of food, nestlings will benefit even less from advertising subtle, fine-scale information about their hunger. Nestling Mouth Color The offspring of all other passerine species also display brightly colored mouths as they beg for food, as do young hoopoes, cuckoos and terns. Mouth colors range from red through pink and orange to yellow (Plate 22). According to Wetherbee (1961), the color of the mouth can arise in one of three ways: (1) vascularization of the mouth lining, (2) pigmentation that can produce red (e.g., Reed Bunting [Emberiza schoeniclus]) or orange (e.g., Dunnock) coloration, or (3) a horny sheathing that covers the bones of the bill and pro-

Function and Evolution of Color in Young Birds

duces a brilliant yellow coloration in starlings, wrens, and titmice. The pigments responsible for coloration in the second group mentioned above may be carotenoids, but this is just conjecture (Chapter 5, Volume 1). Whatever their origin, the vibrant colors displayed by offspring have usually faded by adulthood, which suggests that they serve their major function during the nestling period. One function of the brightly colored gape is to advertise the number of hungry nestlings in the brood. Provisioning parents adjust their rate of food delivery at the nest in response to the amount of brightly colored flesh their brood reveals as it demands food (Kilner 1997; Kilner et al. 1999; Hinde 2004). In Reed Warblers, European Robins (Erithacus rubecula), and Dunnocks, the precise color of the mouth does not appear to affect provisioning rates (Kilner et al. 1999; Noble et al. 1999), although redder mouths evoke more frequent provisioning by canary parents (Kilner 1997). A clearer function for the specific color of the gape has been suggested by Saino et al. (2000, 2003). Because mouth color may contain carotenoid pigments (Wetherbee 1961), and carotenoids play a key role in mounting an immune response, Saino et al. suggested that nestlings must trade off investment in maintaining their immune system with investment in displaying a brightly colored gape. According to this view, unhealthy nestlings devote more of their carotenoids to fighting infection and so cannot afford to display a brightly pigmented mouth. Mouth color thus indicates to parents the sickly members of their brood, the offspring offering least returns on parental investment in times of limited resources. In support of their hypothesis, Saino et al. (2000) demonstrated that parent Barn Swallows (Hirundo rustica) prefer to feed nestlings whose naturally yellow mouths have been artificially reddened (although it is unclear whether manipulated gape color falls within the range observed naturally). They also reported that swallow nestlings injected with sheep red-blood cells have mouths that are less intensely colored (Saino et al. 2000, 2003). Rictal Flange Color The color of the mouth is not the only component of the visual begging display of passerines. The rictal flanges surrounding the gape are commonly thickened and colored as well (Plate 21). Species whose offspring solicit food in dark nest cavities possess relatively thicker flanges that are whiter and less densely colored in relation to their mouth color than those displayed by species whose

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Figure 5.3. Changes in mean (± standard error) Great Tit nestling mass as a function of the color of the gape and that of the surrounding flange (each manipulated with food coloring) under different lighting conditions (luminosity) in the nestbox. The dotted line at 0 indicates no change in nestling mass during a treatment. Redrawn from Heeb et al. (2003).

offspring beg in better illuminated nests (Ingram 1920; Kilner and Davies 1998). Perhaps at nests with low illumination, the broad pale rictal flanges act as beacons, enhancing chick detectability by guiding parents to their nestling’s mouths. Experiments on Great Tits show that paler flanges improve a chick’s foraging success, but only in dark nests and more or less regardless of nestling mouth color. Nestlings whose naturally pale yellow rictal flanges and mouths were reddened with food coloring gained less weight in the subsequent hour than nestlings whose mouths alone were painted red (Heeb et al. 2003; Figure 5.3).

Why So Much Red and Yellow? Grabbing Parental Attention The preponderance of red and yellow in displays of color by young birds is striking and demands an explanation. One possibility is that these colors are deployed by offspring to get the attention of parents. Perhaps they function to improve a young bird’s conspicuousness by maximizing the color contrast

Function and Evolution of Color in Young Birds

with its backdrop (Götmark and Olsson 1997; but see Krebs and Putland 2004). For example, the UV component of the nonspectral reds and yellows revealed by gaping passerines contrasts sharply with the nest background, which typically reflects very little UV light (Hunt et al. 2003; see Figure 5.1). The longer wavelengths at which the gape reflects light varies between species (see above). The specific wavelengths used may have been selected to maximize color contrast with the nest background in the particular light microenvironment in which the gapes are typically viewed by parents (c.f., Endler and Théry 1996). Red gapes, for example, are commonly associated with green ambient light and so will appear black to parents. They are most typically displayed against a pale-colored nest background (S. Hunt, R. M. Kilner, N. E. Langmore, and A. T. D. Bennett, unpubl. data). Offspring that display in well-illuminated environments may use orange or red because it appeals to a sensory bias in parents (Lyon et al. 1994), but a predilection for red is not universal. Götmark and Ahlström (1997) discovered that Great Tit parents favored individual nestlings whose ordinarily yellow mouths had been painted red with food coloring, at least when the cavity nest was illuminated by means of a small window cut into the nestbox (but see Heeb et al. 2003; Figure 5.3). However, neither Reed Warbler, European Robin, nor Dunnock parents preferred to feed nestlings with artificially reddened gapes (Noble et al. 1999). Sending the Right Message As well as improving the efficacy of communication with parents, red and yellow displays may have been selected because these colors are intimately connected with the message of the signal. In other words, red and yellow coloring may have resulted both from selection on the offspring, keen to communicate efficiently with parents, and from selection on parents (or other receivers) intent on responding only to credible signals. Red or yellow might reveal the specific content of the message in a number of ways. I have already discussed how physiological trade-offs mean that the concentration of any carotenoids in the gape might advertise the health of a nestling, or the extent of blood flow through a bare patch of skin can indicate offspring hunger. The redness of a bare patch might similarly advertise offspring temperature, if blood is diverted away from peripheral tissues to maintain the core body temperature when a young bird becomes chilled (e.g., Clotfelter et al. 2003).

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Swynnerton (1916) was the first to suggest that bright nestling mouth coloring might serve an aposematic function—the sudden flash of red or yellow surprising and deterring a would-be predator. His idea now seems most likely to explain the brilliant red and orange mouths displayed by young cuckoos (Noble et al. 1999; Tojo et al. 2002), because nestlings of other species typically crouch in the nest at the first sign of danger, with their gapes firmly closed. Cuckoo nestlings are unusual in possessing a warning display that develops roughly a week after hatching that can be evoked with the slightest touch to the nest rim. For instance, when disturbed, nestlings of the Common Cuckoo puff out their pin feathers, rise quivering in the nest with the bright orange-red gape wide open, and then quickly sink down again, repeating the process several times (Wyllie 1981; Kilner and Davies 1999). Oriental Cuckoos similarly display their orange mouths when threatened (Tojo et al. 2002). Developmental Constraints Finally, there remains the possibility that reds and yellows are used simply because these bright colors are the simplest to produce, and offspring are constrained in their ability to display other hues (see above). Red displays, for example, can be engineered simply by revealing a vascularized bare patch, and yellow carotenoid pigments are packed in the egg to protect chicks during early development (e.g., Blount et al. 2003). In passerines, there is a marked phylogenetic component to nestling mouth color (Ficken 1965), which suggests that the specific color selected for display by young birds may have no function in itself. I mapped the distribution of nestling mouth color onto the Barker et al. (2001) phylogeny of passerine tribes, summarizing descriptions of nestling mouth color from Birds of the Western Palearctic (Cramp et al. 1977–1994) and Birds of Africa (Fry et al. 1982–2004) into four categories: white, yellow, orange, and red. I found that orange and red are the most recently evolved gape colors, and yellow is the ancestral character (Figure 5.4). This pattern is unlikely to be explained by nest type, because nestlings with yellow mouths are typically associated with safer nest sites (Ficken 1965; Kilner 1999), yet the ancestral passerines probably favored riskier nest locations (Bennett and Owens 2002). It would be interesting to map the use of yellow to red in adult plumage onto a phylogeny, to test whether such plumage colors are similarly more recently derived traits. Across rail species, there is a positive correlation between the degree of elaboration in offspring

Function and Evolution of Color in Young Birds

Nestling mouth color

red orange yellow creamy white

225 Pittidae Tyranninae Menuridae Climacteridae Ptilorhynchidae Maluridae Meliphagidae Pardalotidae Pomatostomidae Corvini Laniidae Monarchini Dicrurini Oriolini Vireonidae Vangini Malaconotini Petroicidae Picathartidae Cisticolidae Alaudidae Aegithalidae Pycnonotidae Timaliini Sylviini Megalurinae Acrocephalinae Zosteropidae Hirundininae Remizinae Parinae Ptilogonati Bombycillini Regulidae Turdinae Saxicolini Muscicapini Mimini Sturnini Cinclidae Troglodytinae Certhiini Polioptilinae Tichodraminae Sittinae Nectariniini Estrildidae Prunellinae Passerinae Motacillinae Fringillini Carduelini Peucedraminae Thraupini Emberizini Parulini Icterini Cardinalini

Figure 5.4. Nestling mouth color in relation to phylogeny within the passerines.

ornamentation and the extent of ornamentation later displayed by adults, which may have arisen as a byproduct of selection on adult phenotypes alone (Krebs and Putland 2004). Similarly, it could be that the orange and red mouths displayed by more recently evolved passerine taxa are simply a byproduct of the selective forces that caused the evolution of redder adult plumage.

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Why Are Adult Birds More Diversely Colorful Than Their Young Offspring? When compared with their parents, and especially when viewed alongside their fathers, young birds are dull. Immature offspring tend to be shades of white, brown, or black, with a few taxa evolving yellow or red coloration in response to sibling competition. I conclude by considering why the expression of bright color in birds is usually confined to adults. One explanation, which I have already explored, is that offspring are constrained in their ability to produce a more gaudy appearance. Perhaps there are developmental constraints, which prohibit the display of bright ornamentation in the newly hatched. Or there may be physiological constraints because a chick’s skin or feathers are designed for thermoregulation or for crypsis and cannot simultaneously be brightly colored. There might also be phylogenetic constraints, which appear at least to limit the display of bright red. Adult males may display a greater abundance of color than offspring because of differences they experience in the relative costs and benefits of signaling, and differences in the nature of the information they advertise with color. For example, a male displaying to a potential mate has the greater incentive to be flamboyant, because he will encounter more resistance than a chick soliciting food from its parents: the potential for a conflict of interest between prospective partners is greater than between parent and offspring (Queller 1994). Furthermore, males have more to lose from a feeble display, because they run the risk of outright rejection by the female. By contrast, parents might neglect offspring that solicit food weakly during one bout of provisioning, but they rarely reject offspring entirely. In this regard, it is telling that the most elaborate offspring displays are associated with the highest risk of abandonment by parents. Males may also advertise their color from a greater variety of display sites than used by offspring, which might also lead to increased diversity in adult plumage color (see Endler and Théry 1996). The information that males convey visually is likely to vary much more between species than the information revealed by displays of offspring color, which might also account for the greater interspecific variation in male ornamental coloration. For example, a female carefully assessing whether a displaying male would make a good partner is interested in long-term indicators of his quality—his health, condition, ability to provide paternal care, and genetic background, characteristics that take some time to develop and that might vary according to the message they convey. By contrast, a parent choosing an off-

Function and Evolution of Color in Young Birds

spring to feed is interested simply in the hunger of her young, a trait that fluctuates rapidly in the short term and that can be readily advertised by the temporary display of a single color patch. In short, offspring are duller than adult males because they have one message for their parents. It is a message that parents are inclined to receive, and offspring have repeated opportunities to deliver it. By contrast, adults are interested in multiple aspects of the quality of prospective mates. Their greater inclination toward skepticism when sizing up mates than when assessing their young, and the opportunity of females to reject dull partners completely has contributed to the evolution of more brilliantly colorful adult males.

Summary Why are adult birds almost universally more brilliantly and diversely colorful than their immature offspring? I suggest that young birds owe their dull coloring to selection for crypsis or thermoregulation; they might also be constrained in their ability to signal with bright coloration. Badges of identity that are used in kin recognition are also drab, usually involving black, brown, or white plumage, perhaps because signals with these colors are less vulnerable to corruption when viewed in the shade or with light filtered through vegetation. The most diversely colorful displays are associated with the advertisement of offspring sex and can involve greens, blues, reds, and yellows. Perhaps some of this diversity is simply a byproduct of sexual selection on the adult phenotype. Otherwise, offspring displays of color are typically confined to reds and yellows and are associated with increased levels of sibling competition for parental care. Red or yellow coloration may have resulted both from selection on the offspring, keen to communicate efficiently with parents, and from selection on parents (or other receivers), intent on responding only to credible signals. Perhaps because parents are interested simply in the neediness of their young, whereas females want information about a range of qualities in a prospective mate, offspring displays of color are far less diverse than those exhibited by male birds.

References Andersson, M. 1994. Sexual Selection. Princeton, NJ: Princeton University Press. Baicich, P. J., and C. J. O. Harrison. 1997. A Guide to the Nests, Eggs, and Nestlings of North American Birds. London: Academic Press.

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rebecca m. kilner Barker, F. K., G. F. Barrowclough, and J. G. Groth. 2001. A phylogenetic hypothesis for passerine birds: Taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data. Proc R Soc Lond B 269: 295–308. Beecher, M. D. 1982. Signature systems and kin recognition. Am Zool 22: 477–490. Beecher, M. D., I. M. Beecher, and S. Lumpkin. 1981a. Parent-offspring recognition in Bank Swallows (Riparia riparia): I. Natural history. Anim Behav 29: 86–94. Beecher, M. D., I. M. Beecher, and S. H. Nichols. 1981b. Parent-offspring recognition in Bank Swallows (Riparia riparia): II. Development and acoustic basis. Anim Behav 29: 95–101. Bennett, P. M, and I. P. F. Owens. 2002. Evolutionary Ecology of Birds: Life Histories, Mating Systems and Extinction. Oxford: Oxford University Press. Blount, J. D., N. B. Metcalfe, K. E. Arnold, P. F. Surai, G. L. Devevey, and P. Monaghan. 2003. Neonatal nutrition, adult oxidant defences and sexual attractiveness in the Zebra Finch. Proc R Soc Lond B 270: 1691–1696. Boyd, H. J., and R. Alley. 1948. The function of the head-coloration of the nestling coot and other nestling Rallidae. Ibis 90: 582–593. Bradbury, J. W., and S. Vehrencamp. 1998. Principles of Animal Communication. Sunderland, MA: Sinauer Associates. Buckley, P. A., and F. G. Buckley. 1970. Color variation in the soft parts and down of Royal Tern chicks. Auk 87: 1–13. Buckley, P. A., and F. G. Buckley. 1972. Individual egg and chick recognition by adult Royal Terns (Sterna maxima maxima). Anim Behav 20: 457–462. Burley, N. 1986. Sex ratio manipulation in color banded populations of Zebra Finches. Evolution 40: 1191–1206. Chaniot, G. E. 1970. Notes on color variation in downy Caspian Terns. Condor 72: 460–465. Clotfelter, E. D., K. A. Schubert, V. Nolan, and E. D. Ketterson. 2003. Mouth color signals thermal state of nestling Dark-eyed Juncos (Junco hyemalis). Ethology 109: 171–182. Cramp, S., C. M. Perrins, and K. E. L. Simmons, ed. 1977–1994. Birds of the Western Palearctic. Oxford: Oxford University Press. Davies, N. B. 2000. Cuckoos, Cowbirds and Other Cheats. London: T. & A. D. Poyser. Dawkins, R., and J. R. Krebs. 1979. Arms races within and between species. Proc R Soc Lond B 205: 489–511. Dorward, D. F., and N. P. Ashmole. 1963. Notes on the biology of the Brown Noddy Anous stolidus on Ascension Island. Ibis 103b: 447–457. Endler, J. A., and M. Théry. 1996. Interacting effects of lek placement, display behavior, ambient light and color patterns in three Neotropical forest-dwelling birds. Am Nat 148: 421–452. Fenoglio, S., M. Cucco, and G. Malacarne. 2002. Bill colour and body condition in the Moorhen Gallinula chloropsis. Bird Study 49: 89–92.

Function and Evolution of Color in Young Birds Ficken, M. S. 1965. Mouth color of nestling passerines and its use in taxonomy. Wilson Bull 77: 71–75. Forbes, M. R. L., and C. D. Ankney. 1987. Hatching asynchrony and food allocation within broods of Pied-billed Grebes Podilymbus podiceps. Can J Zool 65: 2872– 2877. Fry, C. H., S. Keith, and K. Urban, ed. 1982–2004. Birds of Africa. London: Academic Press and Christopher Helm. Galeotti, P., D. Rubolini, P. O. Dunn, and M. Fasola. 2003. Colour polymorphisms in birds: Causes and functions. J Evol Biol 16: 635–646. Götmark, F., and M. Ahlström. 1997. Parental preference for red mouth of chicks in a songbird. Proc R Soc Lond B 264: 959–962. Götmark, F., and J. Olsson. 1997. Artifical colour mutation: Do red-painted Great Tits experience increased or decreased predation? Anim Behav 53: 83–91. Harrison, C. J. O., and P. Castell. 1998. Bird Nests, Eggs and Nestlings of Britain and Europe. London: Harper Collins. Heeb, P., T. Schwander, and S. Faoro. 2003. Nestling detectability affects parental feeding preferences in a cavity-nesting bird. Anim Behav 66: 637–642. Hinde, C. A. 2004. Reproductive Strategies in the Great Tit (Parus major). Ph.D. thesis, University of Cambridge, Cambridge, UK. Horsfall, J. 1984. Brood reduction and brood division in coots. Anim Behav 32: 216–225. Hunt, S., R. M. Kilner, N. E. Langmore, and A. T. D. Bennett. 2003. Conspicuous, ultraviolet-rich mouth colours in begging chicks. Proc R Soc Lond B 270: S25– S28. Immelmann, K. von. 1965. Australian Finches. Sydney: Angus and Robertson. Immelmann, K. von, A. Piltz, and R. Sossinka. 1977. Experimentelle Untersuchungen zur Bedeutung der Rachenzeichnung junger Zebrafinken. Z Tierpsychol 45: 210–218. Ingram, C. 1907. On tongue-marks in young birds. Ibis 1: 574–578. Ingram, C. 1920. A contribution to the study of nestling birds. Ibis 2: 856–880. Johnsen, A., K. Delhey, S. Andersson, and B. Kempenaers. 2003. Plumage colour in nestling Blue Tits: Sexual dichromatism, condition dependence and genetic effects. Proc R Soc Lond B 270: 1263–1270. Jourdie, V., B. Moureau, A. T. D. Bennett, and P. Heeb. 2004. Ultraviolet reflectance by the skin of nestlings. Nature 431: 262. Kilner, R. 1997. Mouth colour is a reliable signal of need in begging canary nestlings. Proc R Soc Lond B 264: 963–968. Kilner, R. M. 1999. Family conflicts and the evolution of nestling mouth colour. Behaviour 136: 779–804. Kilner, R. M. 2002a. Sex differences in Canary (Serinus canaria) provisioning rules. Behav Ecol Sociobiol 52: 400–407.

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rebecca m. kilner Kilner, R. M. 2002b. The evolution of complex begging displays. In J. Wright and M. L. Leonard, ed., The Evolution of Begging: Competition, Cooperation and Communication, 87–106. Dordrecht: Kluwer Academic. Kilner, R., and N. B. Davies. 1998. Nestling mouth colour: Ecological correlates of a begging signal. Anim Behav 56: 705–712. Kilner, R. M., and N. B. Davies. 1999. How selfish is a cuckoo chick? Anim Behav 58: 797–808. Kilner, R. M., D. G. Noble, and N. B. Davies. 1999. Signals of need in parentoffspring communication and their exploitation by the cuckoo. Nature 397: 667–772. Krebs, E. A., and D. A. Putland, 2004. Chic chicks: The evolution of chick ornamentation in rails. Behav Ecol 15: 946–951. Langmore, N. E., S. Hunt, and R. M. Kilner. 2003. Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422: 157–160. Lessells, C. M. 2002. Parental investment in relation to offspring sex. In J. Wright and M. L. Leonard, ed., The Evolution of Begging: Competition, Cooperation and Communication, 65–86. Dordrecht: Kluwer Academic. Lyon, B. E., J. M. Eadie, and L. D. Hamilton. 1994. Parental choice selects for ornamental plumage in American Coot chicks. Nature 371: 240–243. Magrath, M. J. L, E. van Lieshout, G. H. Visser, and J. Komdeur. 2004. Nutritional bias as a new mode of adjusting sex allocation. Proc R Soc Lond B 271: S347– S349. Meerloo, M. van. 2003. Function of Gape Colouration in the Brown Songlark Chick (Cinclorhamphus cruralis). Ph.D. thesis, University of Gröningen, Gröningen, The Netherlands. Müller, R. E., and D. G. Smith. 1978. Parent-offspring interactions in Zebra Finches. Auk 95: 485–495. Mundy, N. I., N. S. Badcock, T. Hart, K. Scribner, K. Janssen, and N. J. Nadeau. 2004. Conserved genetic basis of a quantitative plumage trait involved in mate choice. Science 303: 1870–1873. Nicolai, J. 1974. Mimicry in parasitic birds. Sci Am 231: 93–99. Noble, D. G., N. B. Davies, I. R. Hartley, and S. B. McRae. 1999. The red gape of the Nestlings Cuckoo (Cuculus canorus) is not a supernormal stimulus for three common cuckoo hosts. Behaviour 136: 759–777. Nuechterlein, G. L. 1985. Experiments on the functions of the bare crown patch of downy Western Grebe Chicks. Can J Zool 63: 464–467. Palestis, B. G., and J. Burger. 1999. Individual sibling recognition in experimental broods of Common Tern chicks. Anim Behav 58: 375–381. Payne, R. B. 1997. Avian brood parasitism. In D. H. Clayton and J. Moore, ed., HostParasite Evolution: General Principles and Avian Models, 338–369. Oxford: Oxford University Press.

Function and Evolution of Color in Young Birds Payne, R. B., J. L. Woods, and L. L. Payne. 2001. Parental care in estrildid finches: Experimental tests of a model of Vidua brood parasitism. Anim Behav 62: 473–483. Payne, R. B., K. Hustler, R. Stjernstedt, K. M. Sefc, and M. D. Sorenson. 2002. Behavioural and genetic evidence of a recent population switch to a novel host species in brood-parasitic Indigobirds Vidua chalybeata. Ibis 144: 373–383. Purvis. A., and A. Rambaut. 1995. Comparative analysis by independent contrasts (CAIC): An Apple Macintosh application for analysing comparative data. Comp Appl Biosci 11: 247–251. Queller, D. C. 1994. Male-female conflict and parent-offspring conflict. Am Nat 144: S84–S99. Reed, H. J., and N. H. Freeman. 1991. Does an absence of gape markings affect survival of leucistic young in the Zebra Finch? Bird Behav 9: 58–63. Rowe, C. 1999. Receiver psychology and the evolution of multicomponent signals. Anim Behav 58: 921–931. Saino, N., P. Ninni, S. Calza, R. Martinelli, F. de Bernardi, and A. P. Møller. 2000. Better red than dead: Carotenoid-based mouth coloration reveals infection in Barn Swallow nestlings. Proc R Soc Lond B 267: 57–61. Saino, N., R. Ambrosini, R. Martinelli, P. Ninni, and A. P. Møller. 2003. Gape coloration reliably reflects immunocompetence of Barn Swallow (Hirundo rustica) nestlings. Behav Ecol 14: 16–22. Shugart, G. W. 1990. A cue-isolation experiment to determine if Caspian Tern parents learn their offspring’s down color. Ethology 84: 155–161. Sibley, C. G., and J. E. Ahlquist. 1990. Phylogeny and Classification of Birds. London: Yale University Press. Skagen, S. K. 1988. Asynchronous hatching and food limitation: A test of Lack’s hypothesis. Auk 105: 78–88. Soler, M., J. G. Martinez, J. J. Soler, and A. P. Møller. 1995. Preferential allocation of food by Magpies Pica pica to Great Spotted Cuckoo Clamator glandarius chicks. Behav Ecol Sociobiol 37: 7–13. Starck, J. M. 1998. Structural invariants and invariants in avian embryonic and postnatal development. In J. M. Starck and R. E. Ricklefs, ed., Avian Growth and Development, 59–88. Oxford: Oxford University Press. Stoddard, P. K., and M. D. Beecher. 1983. Parental recognition of offspring in the Cliff Swallow. Auk 100: 795–799. Storer, R. W. 1967. The patterns of downy grebes. Condor 69: 469–478. Stoutejesdijk, F. 2002. The ugly duckling: A thermal viewpoint. J Therm Biol 27: 413–422. Swynnerton, C. F. M. 1916. On the coloration of the mouths and eggs of birds. I. The mouths of birds. Ibis 4: 264–294. Taylor, B., and B. van Perlo. 1998. Rails: A Guide to the Rails, Crakes, Gallinules and Coots of the World. Sussex, UK: Pica Press.

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6 Benefits to Females of Assessing Color Displays simon c. griffith and sarah r. pryke

Early in the mating season, as a female bird casts her eyes over the group of males in a bush or strung out along a fence, she will subconsciously pay attention to small variations in the plumage of the different males. Is one male slightly brighter than the others, or does one perhaps have a colored patch slightly larger in size than his fellows? This subtle variation between the males will direct her in choosing a mate for the coming breeding season, or possibly even for the rest of her life. That a female bases such an important decision purely upon the appearance of a potential partner may at first seem quite arbitrary. In fact, variation in the expression of color in birds can signal a wide range of different benefits to a discerning receiver, many of which will have significant effects on the immediate reproductive success and subsequent lifehistory of that individual. In birds, the benefits signaled through color variation form a large component of the reproductive variance among individuals within a population, driving the process of sexual selection and the evolution of sexually selected ornamental traits. As the empirical study of sexual selection has accelerated over the past decades, studies of avian systems have been at the forefront, and it is now possible to discuss nearly all aspects of sexual selection using only avian examples. In fact, there is an overwhelming number of studies, and although in the first part of this chapter we use many empirical examples to

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introduce the various benefits that may be signaled through color, it is by no means an exhaustive review. We also briefly discuss the idea that different forms of color and pattern variations may be better than others at signaling the various types of benefits. For example, are carotenoid-based colors better at signaling the ability of an individual to gather food and provision nestlings than melanin-based signals? This remains an attractive idea, and we very briefly outline reasons why this may be the case, but also highlight some of the problems associated with generalizing about the relative function and evolution of different color mechanisms across different species.

Color Displays in Birds Although color is prevalent and has evolved under many different forms of selection in birds, it is important to delimit the color displays that are the focus of this chapter. We have limited this discussion purely to color displays that are related to mate choice—ornamental color. Typically, ornamental traits are characterized by high levels of variance across a population, with the most attractive individuals displaying the highest levels of trait expression (Andersson 1994). Color-based ornamental traits in birds may vary either in the size of a particular patch of colored plumage or in the qualitative nature of the color itself. For example, the black throat patch of the male House Sparrow (Passer domesticus; Plate 23, Volume 1) does not vary much in its blackness, but shows extensive variation in its size. By contrast, the red plumage of the House Finch (Carpodacus mexicanus; Plate 14) varies most significantly in the quality of the color, from straw yellow to deep scarlet. Typically, individuals with the richest color or largest patch are seen to have the highest level of ornamental expression. As birds generally express a number of different discrete plumages throughout their lives (produced during periodic molts), many species also exhibit agedependent color displays. This phenomenon varies from species with delayed plumage maturation of the majority of their contour feathers (e.g., Bullock’s Oriole [Icterus bullockii]; Richardson and Burke 1999) to species such as the Blue Tit (Parus caeruleus; Plate 18), in which a relatively subtle color difference in the primary coverts alone distinguishes a yearling from an older bird (Perrins 1979). Even in species that display no specific age-dependent difference in plumage or color, there are often quite distinct age-related differences in the expression of sexual ornaments, with yearlings usually displaying a smaller or less intense variation of the trait (Figure 6.1).

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Badge length (mm)

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Age of male

Figure 6.1. Size of throat badges in yearling and adult male House Sparrows on the Island of Lundy, England. Box plots show the median inside a box bounded by the 25th and 75th percentiles (IQD), with whiskers either 1.5×IQD above and below the box or to the maximum and minimum data points, whichever is less; all data above and below the whiskers are plotted, and sample sizes are shown above each box. Drawn from data in Griffith et al. (1999a,b).

There are obvious advantages to females in assessing the age of a male, given that older individuals will often have more breeding experience and presumably also have good genes because they have survived longer (Kokko and Lindström 1996). However, in this chapter, we focus on more standard sexual ornaments, expressed with continuous variation across the population, such as that of the House Sparrow, rather than on plumages showing fixed agedependence, such as that of Bullock’s Oriole (see Chapters 2 and 3 for further discussion of age-specific plumages). Finally, we have adopted the convention of using the male as the ornamental sex, signaling to the female as the receiver, or choosy sex. Obviously there are species in which both sexes are ornamental and mutual mate choice

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occurs, just as there are a few species in which there is a complete reversal of roles. However, the general pattern observed in birds is for males to be showy and females choosy (Bennett and Owens 2002), and we feel it is preferable to adopt those stereotypes throughout rather than the verbose and clumsy alternative of removing gender altogether and referring to individuals as choosers, receivers, and signalers. There is great variety in the breeding systems of birds, from highly polyandrous systems in which the male and female come together very briefly to copulate through to life-long social and reproductive partnerships (Bennett and Owens 2002). Consequently, the range of potential benefits that females can expect from mate choice on the basis of color is extensive, and naturally, in some breeding systems females may gain a multitude of different benefits. Females can gain benefits pre- or post-fertilization, and directly (for themselves) or indirectly (through their offspring). Although we have divided the different benefits for the sake of providing some structure in the chapter, females can simultaneously gain many different benefits. Benefits are often strongly correlated with one another, and thus despite our organization of this chapter, we are not suggesting that these benefits are mutually exclusive.

Direct Benefits Signaled by Color Displays Dominance-Related Benefits The prevalence of social monogamy in birds (Lack 1968; Ligon 1999) means that males and females will generally have prolonged associations (temporally and spatially). Consequently, females can gain considerable benefits from their partners that will affect their own fitness directly, in terms of the number of offspring they can rear in their life, either through the current reproductive event or through life-history trade-offs to future reproduction (Stearns 1989). Even in highly polygynous mating systems, in which pair associations are limited to brief copulations, males can provide very basic direct benefits to females in the form of territories in which females can breed, feed, and escape harassment by other males (e.g., Pryke and Lawes 2004). Because high-quality resources or territories are typically limiting, male contests often determine access to valuable resources; males that are unable to successfully defend a territory are usually forced to leave the breeding habitat, occupy low-quality or marginal areas, or become nonterritorial floaters with limited opportunity for successful reproduction (although this may be counter-

Benefits to Females of Assessing Color Displays

acted by extra-pair paternity). Females assessing male color are likely to gain good territories and nest sites, because male ornaments are often related directly to male dominance (Chapter 3). This may, at least in part, be explained by the relationship between the expression of ornamental color and the level of circulating testosterone (e.g., Owens and Short 1995; Evans et al. 2000; Peters et al. 2000; Chapter 10, Volume 1), which, in turn, is related to aggression (Ketterson and Nolan 1992). Male dominance has typically been associated with the variation in melaninbased “badges of status” (Rohwer 1975), which allows individuals to assess one another’s competitive ability (through variable plumage cues) and thus avoid costly interactions and injuries when establishing dominance relationships (Rohwer 1975, 1982; Chapter 3). Traditionally, status signal costs and honesty have been attributed to social mediation (Rohwer 1982; Chapter 3). However, more recently, some striking examples of life-history trade-offs (e.g., Gustafsson et al. 1995; Griffith 2000; Badyaev and Qvarnström 2002) have broadened our understanding of colored-badge honesty. Although most studies investigating dominance interactions have focused on melanin-based coloration, agonistic signals are not limited to this particular form of color. For example, the variation in carotenoid (e.g., Røskaft and Rohwer 1987; Evans and Hatchwell 1992; Pryke et al. 2002; Pryke and Andersson 2003a,b) and structural coloration (e.g., Keyser and Hill 2000; Alonso-Alvarez et al. 2004) may also be maintained by intense male competition for territories. Females may gain a number of direct benefits from choosing highly ornamented males who also defend the best resources for breeding (Table 6.1). An initial requirement for most females is selecting territories with high-quality nesting sites or habitat, such as those containing the most suitable nesting vegetation (Searcy 1979; Yasukawa 1981; Wolfenbarger 1999) or the best or most numerous nesting cavities (Møller 1988; Veiga 1993). Highly ornamented males may also offer predator protection to both the female and her offspring by providing nesting habitats with fewer predators (Hill 1988) or by actively defending her brood (Norris 1990; Reyer et al. 1998). Food resources, especially high-quality foods, are also crucial for raising a larger number of healthy offspring (see below), and males defending such resources may be particularly appealing to prospective females. For example, male Red-winged Blackbirds (Agelaius phoeniceus; Plate 11) become highly attractive when they are given extra food on their territories (Ewald and Rohwer 1982; Wimberger 1988). More colorful males may defend important resources, such as the nectar flowers (inflorescences) used by Scarlet-tufted Malachite Sunbirds (Nectarinia johnstoni;

237

Blue Grosbeak (Passerina caerulea) Scarlet-tufted Malachite Sunbird (Nectarinia johnstoni) Great Tit (Parus major) House Sparrow (Passer domesticus) C M M M M

Red pectoral tufts

Black badge size Black badge size

Black badge size

Black badge size

C C C C M M M M M

Red collar size and color Red collar size and color Red epaulet size and color Red epaulet size and color White forehead patch White forehead patch Black patch color Black patch color Black patch color S

M

Rusty breast streaks

Blue plumage color

C

C C

Color

Red plumage color

Red epaulet size Red epaulet size

Resource quality Red-winged Blackbird (Agelaius phoeniceus)

Northern Cardinal (Cardinalis cardinalis) Yellow Warbler (Dendroica petechia) Red-collared Widowbird (Euplectes ardens) Red-shouldered Widowbird (E. axillaris) Collared Flycatcher (Fidecula albicollis) Pied Flycatcher (F. hypoleuca)

Ornament measure

Species

Cor

Exp

Cor Cor

Exp

Cor

Cor Exp Cor Exp Cor Exp Exp Cor Exp

Cor

Cor

Cor Exp

Study

Territory acquisition and size Territory acquisition and size Territory acquisition and size Territory acquisition and size Territory size Territory size Territory quality Territory quality Nest site quality (number of nest boxes) Territory size and quality (prey abundance) Territory size and quality (inflorescences) Territory quality Nest site quality (containing multiple cavities) Nest site quality (number of nest boxes) Nest site quality (number of nest boxes)

Territory quality (vegetation density) Territory quality

Territory acquisition and quality Territory acquisition and quality

Territory or nest measure

–

+

+ +

+

+

+ + + + + + + + +

+

+

+ +

Outcome

Kimball (1997)

Veiga (1993)

Evans and Hatchwell (1992); Evans (1996) Norris (1990) Møller (1988)

Keyser and Hill (2000)

Pryke et al. (2001b) Pryke et al. (2002) Pryke and Andersson (2003a, b) Pryke and Andersson (2003b) Pärt and Qvarnström (1992) Qvarnström (1997) Alatalo et al. (1986) Slagsvold (1986) Slagsvold and Lifjeld (1988)

Studd and Robertson (1985)

Peek (1972); Smith (1972) Hansen and Rohwer (1986); Røskaft and Rohwer (1987) Wolfenbarger (1999)

Reference

Table 6.1. Studies of Resource (Territory and Nest) Quality and Defense in Relation to the Expression of Male Color Variation (Size and/or Intensity)

M C C C S M M M M M

Black plumage color

Yellow patch size Yellow patch size

Red plumage color

Blue plumage color

Black badge size Black badge size

Black plumage color

Black body patch size

Black badge size

Cor

Cor

Cor

Cor Cor

Cor

Cor

Cor Exp

Cor

Territory size

Territory placement

Territory with fewer predators

Male brood defense Male nest defense

Probability of nest predation

Male nest defense

Territory quality (heterogenous habitat) Territory size Territory size

–

+

+

+ +

–

0

+ +

+

Ralph and Pearson (1971)

Edwards (1982)

Hill (1988)

Norris (1990) Reyer et al. (1998)

Keyser and Hill (2000)

Jawor and Breitwisch (2004)

Marchetti (1998) Marchetti (1998)

Hill (1988)

Notes: 0, no relationship; –, negative relationship; +, positive relationship; C, carotenoid pigmentation; Cor, correlational study; Exp, Experimental study; M, melanin pigmentation; S, structural coloration.

Black–headed Grosbeak (Pheucticus melanocephalus) Yellow-browed Leaf Warbler (Phylloscopus inornatus) Resource defense Northern Cardinal (Cardinalis cardinalis) Blue Grosbeak (Passerina caerulea) Great Tit (Parus major) House Sparrow (Passer domesticus) Black–headed Grosbeak (Pheucticus melanocephalus) Greater Golden Plover (Pluvialis apricaria) White-crowned Sparrow (Zonotrichia leucophrys)

240

simon c. griffith & sarah r. pryke Evans and Hatchwell 1992; Evans 1996) or the arthropods important in nestling feeding by Blue Grosbeaks (Passerina caerulea; Plate 7, Volume 1; Keyser and Hill 2000). However, considering that many territorial birds forage, at least partly, on the nesting territories, relatively few studies have attempted to quantify food resources as a separate component of territory quality used in mate choice. In species actively defending territories or resources, the relationship between variation in the ornamental trait and territory quality (e.g., food, shelter, nest sites for females) is often maintained by intense male competition, as males compete to monopolize precisely the benefits that females are seeking. However, this pattern does not imply that females necessarily evaluate male color expression. If highly ornamented males establish and defend high-quality territories through male contests, then females may not assess male color directly but instead simply exercise choice based on aspects of his territory. Therefore females may not exhibit a preference for a particular color-based trait that relates to pairing success, but may simply be settling on the best territories, which are held by the most competitive and ornamented males. This complicating issue was first demonstrated in the socially monogamous Pied Flycatcher (Ficedula hypoleuca), a species in which the female can expect to gain far more from the male than simply a small breeding territory and genes for her offspring. Alatalo et al. (1986) realized that the correlation between male ornamentation and territory and nest site quality could confound female mate choice, as the males arrive from migration and establish territories several weeks before the females arrive and choose a partner. Dominance interactions among male Pied Flycatchers are strongly related to the expression of the melanin-based plumage (Plate 27, Volume 1), and the darkest males gain and hold the best territories and nest holes (Alatalo et al. 1986; Lundberg and Alatalo 1992). Given that females can simultaneously assess both the color of a male and the quality of territory or nest site, it was very difficult to determine whether they were actually assessing color or simply basing their choice of mates on the resources held by males (and correlated with his color). In their classic study, Alatalo et al. (1986) dissociated the two variables by experimentally allocating males to territories as they arrived on the breeding ground from migration, and found that females simply settled on the best territory, irrespective of the quality of the male holding that territory. It seems rather surprising, given the implications of this study (Alatalo et al. 1986), that no other study has attempted to explore this possibility experimentally, and it is quite possible that many examples of female mate choice based

Benefits to Females of Assessing Color Displays

on ornamentation may, in fact, also be choice for resources that are associated with male coloration. Similarly, the relationship between ornament variation, territory quality, and female mate choice may be complicated or concealed by additional ornaments and the interaction of different selection pressures. For example, in the highly polygynous and strikingly ornamented Red-collared Widowbirds (Euplectes ardens), males display two classic sexually selected plumage traits—long tails and carotenoid coloration. Although selection analyses (Pryke et al. 2001a) and experiments (Pryke and Andersson 2005) have shown that females strongly target territorial males with longer tails (Figure 6.2), surprisingly, especially given the findings from a number of recent studies (Hill 1999; Chapter 4), they completely ignore the prominent and highly variable red collar patch in mate choice decisions. In the field, the redness of a male is unrelated to the number of females he attracts to nest on his territory (Figure 6.2; Pryke et al. 2001a), and there is no evidence from experiments manipulating male color patches that females exhibit a preference for variation in the color (Pryke and Andersson 2003b). Instead, the red collar functions as a signal in male competition to gain access to a territory (only about 30% of males establish territories) and settle male conflicts (Pryke et al. 2002; Pryke and Andersson 2003a,b). Because males use their territories to display to and attract choosy females (targeting tails), a male’s mating success critically depends on his success in obtaining and defending a territory. These experimental studies on flycatchers and widowbirds suggest that caution should be used when interpreting apparent relationships between male color and direct territorial benefits that females can gain by assessing them. Even though male coloration may seem very striking, females may pay little attention to it and simply express preferences for a nest site or territory directly. Nonetheless, it is generally found that where there is variation in the quality of resources, the most ornamented males hold the best territories and nest sites (e.g., Hansen and Rohwer 1986), both of which will improve a female’s chance of breeding successfully. Courtship Feeding Beyond the resources that colorful males can monopolize, there are a number of other benefits that males can provide in a more direct sense to females and their offspring. In many species, males provide food to females during courtship or incubation (e.g., in the Blue Tit; Perrins 1979). In the extreme case of the Monteiro’s Hornbill (Tockus monteiri), the female is completely dependent

241

simon c. griffith & sarah r. pryke

242

Number of active nests

10

a

8

6

4

2

0 100

150

200

250

300

Tail length (mm)

Number of active nests

10

b

8

6

4

2

0 560

570

580

590

600

610

Collar hue (nm)

Figure 6.2. Male Red-collared Widowbird reproductive success (number of actively nesting females) in relation to (a) tail length (n = 43) and (b) the redness (hue) of the collar patch (n = 41). Hue is measured as the wavelength at the point on the reflectance curve halfway between the maximum and minimum reflectance (λR50). Females showed a strong, significant preference for males with longer tails but no preference for males with redder plumage. Redrawn from data in Pryke et al. (2001).

on the male to feed her for the extended period during which she is imprisoned in the sealed nest chamber (e.g., Stanback et al. 2002). Feeding during courtship and incubation should improve the ability of a female to allocate resources to the eggs. A number of studies has demonstrated that females experimentally supplemented with food before and during egg laying may increase clutch size (e.g., Nager et al. 1997). Given that colorful males tend

Benefits to Females of Assessing Color Displays

to be on better territories (often with a high abundance of food) and, in many cases, feed nestlings at a higher rate (see below), it seems reasonable to expect a relationship between ornamental color in males and the level of courtship feeding. To our knowledge, the relationship between courtship feeding and color expression has only been directly assessed in a single study. Hill (1991) found a relationship between the plumage redness of a male House Finch and the amount of food he provided to the female during the early part of the reproductive cycle. The extent to which variation in courtship feeding benefited the female or increased the number of eggs laid is unknown in that species or any other, another rather surprising gap in the knowledge base. Fertilization and Incubation Perhaps of all the direct benefits that males can provide to females, the most important is the fertilization of eggs, into which females will have invested a significant amount of resources by the time they are laid. If eggs fail to develop as a result of insufficient or poor quality sperm, the female will have lost a significant part of her reproductive potential. It is very difficult to determine the extent to which natural egg failure may be dependent on male sperm (and consequently related to male ornamentation). A number of studies has demonstrated that eggs that fail to develop even the smallest visible embryo generally have large numbers of sperm on the inner perivitelline membrane, particularly around the germinal disc, which is the site of fertilization (e.g., Birkhead et al. 1994). The reason these eggs fail to develop is unclear. It could be that, although sperm have arrived at the site of fertilization, they are still in some way defective, or it could be that egg development failure has nothing to do with the variation in sperm and is therefore unlikely to be related to male color. Nonetheless, recent work on Domestic Chickens (Gallus gallus) has demonstrated a clear relationship between ornamentation and some aspects of sperm quality, such as mobility (Froman et al. 2002), and in some species, there is also a relationship between the expression of ornamental color and ejaculate size (e.g., Zebra Finches [Taeniopygia guttata]; Plate 18; Birkhead 1998). This is clearly an area worthy of further investigation, and at the present time, it still seems reasonable to expect a relationship between color and fertility (Sheldon 1994; Blount et al. 2001). Future studies addressing the relationship between male color and infertility will need to adopt a molecular approach because any deficiency in the male partner’s fertility is generally obscured by extra-pair copulations (any eggs not

243

simon c. griffith & sarah r. pryke

244

fertilized by the partner may be fertilized by extra-pair sperm). As extra-pair copulations tend to be cryptic in nature and are difficult to observe, we still do not know the proportion of females that actually participate in extra-pair copulations (Griffith et al. 2002). Levels of extra-pair paternity (observed post-hoc through molecular work) may systematically underestimate female participation in extra-pair copulations. As yet, we simply do not know the proportion of extra-pair copulations that result in offspring. A recent study of the Collared Flycatcher (Ficedula albicollis; Plate 18) indicates that many more females may participate in extra-pair copulations than was previously thought (Michl et al. 2002), suggesting that multiple mating is very widespread but generally masked by success of the pair male in sperm competition. Paternal Care of Offspring Perhaps not surprisingly, the direct benefit that has received the most attention is the extent to which males provide care to their offspring. Parents are most visible when they are feeding nestlings and fledglings, and this nesting period often provides the best opportunity to capture the parents and quantify the expression of ornamental traits in relation to the frequency of provisioning visits made to their offspring. In all sexually reproducing taxa except birds, bi-parental care is the exception rather than the rule (Clutton-Brock 1991), suggesting that in birds, the extended contribution of both partners is almost fundamental to successful reproduction. A number of studies has revealed the dire consequences on reproductive output when either the male or female is removed from a reproductive effort (Gowaty 1996). Although not as extreme as losing a partner altogether, it is obvious that having a partner who is not a very good parent will decrease reproductive output, either immediately or in the future, as the quality of the offspring suffer. Furthermore, given the dynamic nature of bi-parental care, with each parent compensating for the effort invested by the other (Wright and Cuthill 1989), if one partner is a poor parent and the other has to compensate, the better parent’s lifeexpectancy and future reproductive potential are likely to be dramatically reduced (Stearns 1989). By contrast, if one partner does a large share of the provisioning of young, not only will the other be able to increase both the number and quality of offspring reared, but potentially can invest less. Given that parenting in birds is so important and generally a joint effort, it seems clear that there should be strong selection on both males and females to choose partners that will be good parents. Above all other factors, ornamental color in

Benefits to Females of Assessing Color Displays

birds may be a particularly relevant signal of an individual’s ability to provide parental care (Hoelzer 1989). There are several lines of evidence supporting the idea that assessment of color variation provides direct benefits to the choosy sex in the form of improved parental care (Table 6.2). Offspring provisioning obviously takes place long after mate choice, and in most cases, females will never have directly observed a male’s provisioning abilities (many males will not have provisioned chicks before). Therefore females are generally unable to use direct cues of parental ability and may instead base their choice on the variation in color, even if it is only quite weakly related to parental care. Again there are some complications in assigning a causal relationship. First, if color is related to territory quality, it may be that the amount of food delivered to the nest by a male reflects the ease with which he can find it in a good territory, rather than any innate ability to hunt or gather food. One way in which this potential problem has been dealt with is by examining the rate of male provisioning relative to the female, who is presumably foraging in the same territory (e.g., Sheldon and Ellegren 1999). Although it is important to distinguish between the source of variation in the male’s ability to deliver food to the nest—hunting ability or good territory—the female is only really interested in the end result, the amount of food delivered to her offspring. A second, more significant complication, which may underlie observed correlations between male color and chick provisioning (e.g., Linville et al. 1998), is that parental care is generally provided by both parents simultaneously and the care provided by each parent is therefore largely dependent on that provided by the other (Wright and Cuthill 1989). For example, when parents are feeding chicks at a nest, the visiting rate of each parent is generally mediated by the hunger and begging behavior of the chicks. If one parent feeds more, the other parent will feed less. This behavior poses a problem for examining the relationship between color expression and parental care because of the possibility of differential allocation (Burley 1988). Differential allocation is the phenomenon in which an individual will allocate more resources to a particular reproductive attempt if they deem it to be of higher than average value. If a female pairs with a particularly attractive male, it might be adaptive to produce more offspring (Petrie and Williams 1993) or provision the offspring at a higher rate (Burley 1988; Møller and de Lope 1995) to maximize the potential of offspring fathered by an attractive sire and to increase the possibility of keeping the attractive male (Burley 1988). The problem is that, if a female alters her investment in parental care in response to her

245

Blue Grosbeak (Passerina caerulea)

Yellowhammer (Emberiza citrinella) European Kestrel (Falco tinnunculus) Collared Flycatcher (Fidecula albicollis) Pied Flycatcher (F. hypoleuca) M M M M M

Black patch color Black patch color

Black patch color Black patch size White forehead patch size S

M M M

Gray-brown tail color Gray-brown tail color White forehead patch

Blue plumage color

C

Yellow patch color

M M

Rusty breast streaking Rusty breast streaking

House Finch (Carpodacus mexicanus) Yellow Warbler (Dendroica petechia)

C C C C M C

Red plumage color Red plumage color Red bill color Red plumage color Black mask size Red plumage color

Northern Cardinal (Cardinalis cardinalis)

Color

Ornament measure

Species

Cor

Cor Cor Exp

Cor Cor

Cor Cor Exp

Cor

Cor Exp

Cor Cor Cor Cor Cor Exp

Study

Male hunting effort Male hunting effort Male nestling provisioning (manipulated forehead size) Male nestling provisioning Male nestling provisioning (energy expenditure) Male nestling provisioning Male nestling provisioning Male nestling provisioning (manipulated forehead size) Male nestling provisioning

Male nestling provisioning Parental nestling provisioning (manipulated via weights) Male nestling provisioning

Male nestling provisioning Male nestling provisioning Male nestling provisioning Female nestling provisioning Female nestling provisioning Male courtship feeding

Territory or nest measure

+

0 0 –

+ 0

+ – –

–

– 0

+ + 0 0 + +

Outcome

Table 6.2. Studies of Brood Provisioning in Relation to the Expression of Male Color Variation (Size and/or Intensity)

Keyser and Hill (2000)

Rinden et al. (2000) Dale et al. (1999) Sanz (2001)

Sætre et al. (1995) Sætre et al. (1997)

Palokangas et al. (1994) Tolonen and Korpimaki (1994) Qvarnström (1997)

Sundberg and Larsson (1994)

Studd and Robertson (1985) Lozano and Lemon (1996)

Linville et al. (1998) Jawor and Breitwisch (2004) Jawor and Breitwisch (2004) Jawor et al. (2004) Jawor et al. (2004) Hill (1991)

Reference

M M S

Chestnut throat patch size Chestnut throat patch color Blue plumage color Red leg bands M

M S M

Chestnut throat patch color Blue plumage color Black badge size

Plumage color

M

Leg bands Chestnut throat patch size

Cor

Cor Cor Cor Cor

Cor Cor Cor

Exp Exp

Male nestling provisioning

Male nestling provisioning Male nestling provisioning Male nestling provisioning Parental nestling provisioning

Male nestling provisioning Female nestling provisioning (manipulated via male removal) Male nesting provisioning Male nestling provisioning Male nestling provisioning

+

+ + + 0

0 0 +

0 0

Roulin (2001)

Siefferman and Hill (2003) Siefferman and Hill (2003) Siefferman and Hill (2003) Burley (1988)

Smiseth et al. (2001) Smiseth et al. (2001) Møller (1988); Voltura et al. (2002)

Rohde et al. (1999) Smiseth and Amundsen (2000)

Notes: 0, no relationship; –, negative relationship; +, positive relationship; C, carotenoid pigmentation; Cor, correlational study; Exp, experimental study; M, melanin pigmentation; S, structural coloration.

Zebra Finch (Taeniopygia guttata) Barn Owl (Tyto alba)

House Sparrow (Passer domesticus) Eastern Bluebird (Sialia sialis)

Bluethroat (Luscinia svecica)

simon c. griffith & sarah r. pryke

248

perception of a partner’s attractiveness, then that female’s response will obscure any relationship between the expression of a male ornament and his ability or willingness to provision chicks. For example, the most colorful males may be the best foragers and potentially the best fathers, but if a female increases her effort in response to pairing with a colorful mate, then whenever the male arrives at the nest, the chicks will be less hungry and he will decrease the amount of food he delivers. This is a very difficult problem to address, and in species with biparental care, we should certainly be very wary of natural correlations between the expression of ornamental traits and the relative amount of provisioning provided to chicks. The best way of exploring the underlying relationship between male color and provisioning ability or willingness will be to remove females during part of the chick rearing period, and then measure the performance of the male alone. Additionally, it will be necessary to control for the differing number and quality of chicks that males are provisioning. Not surprisingly, such a complicated experiment has yet to be done, and there is very little unequivocal evidence that females assess male ornaments to gain direct benefits in the form of a higher quality of parental care (Table 6.2). However, this observation almost certainly reflects a lack of adequate tests and does not necessarily suggest that the direct benefits of pairing with a colorful male are unimportant. Nest Defense The young of birds, particularly passerines, hatch at a very early stage of development and are particularly vulnerable to predation throughout the prefledging period. Although in many cases there is probably relatively little that a bird can do to prevent predation by a large reptile or mammal, there are a number of antipredator strategies that males can adopt that in turn have been related to male ornamental color (see Table 6.1). For example, males can defend territories with fewer predators (e.g., Hill 1988; Keyser and Hill 2000) or even actively defend (e.g., by mobbing) the nest against predators (e.g., Norris 1990; Reyer et al. 1998). Overall, few studies appear to have investigated the importance of antipredator behavior in relation to male coloration or its importance to female fitness. Parasite Avoidance The co-evolutionary race between parasites and their hosts plays a major role in evolutionary processes, and there are few, if any, avian species that are not

Benefits to Females of Assessing Color Displays

host to a multitude of different parasites. The potential link between parasites and color in birds was made clearly in the classic paper by Hamilton and Zuk (1982), in which they suggested that parasites mediated the process of sexual selection in birds because females choosing bright males would be gaining partners who signaled resistance to parasites. Although they specifically dealt with resistance genes that could be passed onto offspring (an indirect benefit), a female who pairs with a male who is resistant to parasites will also gain a number of direct benefits. First, males that are resistant to parasites are unlikely to carry a high load, reducing the risk that the female will be infected during copulation or through other behavioral interactions (Hamilton 1990). Similarly, a parasite-free male will not contaminate the nest and transfer parasites to the offspring. Finally, regardless of his parasite load, a male who has a high level of resistance to parasites will be in better overall condition than one who is susceptible and will therefore be in a better position to provide other direct benefits. There are good theoretical reasons to presume that the expression of color is related to immunocompetence. The two most commonly used pigments in avian coloration are carotenoids and melanins (Chapters 5 and 6, Volume 1). The relationship between immune function and carotenoids has been readily accepted (e.g., Zuk 1991; Olson and Owens 1998; von Schantz et al. 1999; Walther et al. 1999), and it is equally plausible in the case of melanin (Owens and Wilson 1999). In addition, current physiological evidence points to equivalent roles of melanins, carotenoids, and several of their precursors and derivatives, in the functioning of the immune system (e.g., Rock 1997; Vershinin 1999; Konashi et al. 2000; Lu et al. 2002). Variation in the expression of melanin or carotenoid pigmentation could therefore indicate variability in the ability to mount antiinflammatory responses and fight both intracellular and extracellular parasites, as well as signaling aspects of past parasite exposure. Nonetheless, it appears that no one has directly tested to see whether females explicitly gain these direct parasite-related benefits from assessing the ornamental color of males. Numerous studies, however, have focused on the relationship between the expression of color and natural or experimentally elevated parasite infection (summarized in Table 6.3). Although both the approaches and findings of these studies are highly variable, overall, high levels of parasite infections appear to depress color expression (Chapter 12, Volume 1). An alternative approach is to investigate the relationship between color expression and a measure of the efficiency or strength of the immune system.

249

American Goldfinch (Carduelis tristis) M C C

Orange bill color

Yellow patch color

C

Red plumage color

Black patch color and size

C C

Yellow color (2–4 feathers) Red plumage color

C

C

Yellow color (2–4 feathers)

Yellow patch color

C

Number of yellow feathers

House Finch (Carpodacus mexicanus)

C

Yellow patch color

Eurasian Greenfinch (Carduelis chloris)

C

Yellow bill color

M

Black body color

Mallard (Anas platyrhynchos)

C

Red epaulet size

Red-winged Blackbird (Agelaius phoeniceus)

Color

Ornament measure

Species

Exp

Cor

Exp

Exp

Exp

Cor Cor

Exp

Exp

Cor

Exp

Exp

Exp

Study Response to diptheria-tetanus innoculation Response to diptheria-tetanus innoculation Immune investment after immunization with sheep red blood cells (SRBC) Intensity of Haematoproteus infection in three populations Extent and duration of infection with Sindbis virus Antibody production after immunisation with SRBC Number of heterophils Levels of infection of feather mite and avian pox lesions Infection with Isospora spp. or Mycoplasma sp. Endoparaistic infection with Isospora sp. Endoparaistic infection with Isospora sp. Endoparaistic infection with Isospora sp. Immune response after immunisation with SRBC

Immunocompetence measure

Table 6.3. Studies of Immunocompetence in Relation to the Expression of Color Variation (Size and/or Intensity)

0

–

0

–

–

– –

+

–

–

–

0

0

Outcome

McGraw and Hill (2000) McGraw and Hill (2000) McGraw and Hill (2000) Navara and Hill (2003)

Brawner et al. (2000)

Saks et al. (2003) Thompson et al. (1997)

Lindström and Lundström (2000) Saks et al. (2003)

Merilä et al. (1999)

Peters et al. (2004a,b)

Westneat et al. (2003)

Westneat et al. (2003)

Reference

M M C

White patch color

White patch color

Yellow color (2 feathers)

Great Tit (Parus major)

M

C

Yellow patch color

White forehead patch size

C C C M M M M M M M M C

Yellow patch color Yellow patch size Yellow patch size and color Black patch color Black patch size Black patch color Black patch size Gray patch color Gray patch size Gray patch color Gray patch size Yellow patch size

C

Yellow patch color

Pied Flycatcher (Ficedula hypoleuca)

Yellowhammer (E. citrinella)

Cirl Bunting (Emberiza cirlus)

C

Yellow patch color

Cor

Cor

Cor

Exp

Cor

Cor Cor Cor Cor Cor Cor Cor Cor Cor Cor Cor Cor

Exp

Exp

Immune response using PHA assay Immune response after infection with Mycoplasma gallisepticum Lymphocycte count Lymphocycte count Heterophil count Lymphocycte count Lymphocycte count Heterophil count Heterophil count Lymphocycte count Lymphocycte count Heterophil count Heterophil count Prevalence of infection with Haemoproteus coatneyi Prevalence of infection with Haemoproteus coatneyi Mating effort manipulation and diptheria–tetanus innoculation Prevalence of Haemoproteus sp. infection Blood cell counts of heterophils and leukocytes Prevalence of Haemoproteus sp. infection old males +

+

0

+

0

– 0 + + 0 – 0 0 + 0 – –

0

0

continued

Dufva and Allander (1995) Dufva and Allander (1995) Hõrak et al. (2001)

Kilpimaa et al. (2004)

Sundberg (1995)

Figuerola et al. (1999) Figuerola et al. (1999) Figuerola et al. (1999) Figuerola et al. (1999) Figuerola et al. (1999) Figuerola et al. (1999) Figuerola et al. (1999) Figuerola et al. (1999) Figuerola et al. (1999) Figuerola et al. (1999) Figuerola et al. (1999) Sundberg (1995)

Navara and Hill (2003)

Navara and Hill (2003)

C C

Yellow bill color

C

Red beak color

Yellow bill color

C

S

Blue plumage color

Red beak color

M S

Black badge size Blue plumage color

C

M

Black badge size

Yellow plumage color

M

Black badge size

Exp

Exp

Exp

Exp

Exp

Cor

Cor Cor

Exp

Exp

Exp

Exp

Exp

Cor

Study

Prevalence of Haemoproteus sp. infection Manipulation of feather mite load Immune response to food manipulation and exercise level Carotenoid diet manipulation and PHA response Antibody production after immunization with SRBC PHA response

Prevalence of Haemoproteus sp. infection in yearling males Manipulated flea infestation levels Manipulated flea infestation levels Manipulation of diet and infection with Haemoproteus sp. Immune response to PHA assay (in November) Immune response to PHA assay (in April) Size of bursa of Fabricius Ectoparasite load

Immunocompetence measure

+

–

+

0

–

–

0

–

+

0

–

0

–

Outcome

Faivre et al. (2003)

Faivre et al. (2003)

Blount et al. (2003)

Birkhead et al. (1998)

Møller et al. (1996) Doucet and Montgomerie (2003) Doucet and Montgomerie (2003) Figuerola et al. (2003)

Gonzalez et al. (1999b)

Gonzalez et al. (1999b)

Fitze and Richner (2002) Fitze and Richner (2002) Gonzalez et al. (1999a)

Hõrak et al. (2001)

Reference

Notes: 0, no relationship; –, negative relationship; +, positive relationship; C, carotenoid pigmentation; Cor, correlational study; Exp, experimental study; M, melanin pigmentation; S, structural coloration.

Eurasian Blackbird (Turdus merula)

European Serin (Serinus serinus) Zebra Finch (Taeniopygia guttata)

Satin Bowerbirds (Ptilonorhynchus violaceus)

M

M

Black stripe size

Black badge size

M

White patch color

House Sparrow (Passer domesticus)

C

Yellow color (2 feathers)

Great Tit

Color

Ornament measure

Species

Table 6.3. (continued)

Benefits to Females of Assessing Color Displays

For example, a number of studies has found positive or negative correlations between counts of different types of blood cell and plumage coloration in a variety of species (Table 6.3). These relationships have been more clearly demonstrated by experimental challenges of the immune system, although once more, such studies have produced highly variable results, both within and between species (Table 6.3). Part of this inconsistency may be due to the unknown immune histories of individuals taking part in the experiments. Therefore, to assess a generalized immune response, some studies have used pathogens or antigens that, from an evolutionary context, are completely unfamiliar to the species. In these studies, individuals are commonly inoculated with sheep red blood cells, phytohaemagglutinin, diptheria-tetanus, or the Sindbis virus, and the response is measured directly. Yet again, the results of these experimental studies are relatively inconsistent (Table 6.3). Some studies have found negative relationships between the immune response and the expression of ornaments (e.g., Mallard [Anas platyrhynchos; Plate 15], Peters et al. 2004a,b; European Greenfinch [Carduelis chloris], Lindström and Lundström 2000; House Sparrow [in spring], Gonzalez et al. 1999b; European Blackbird [Turdus merula], Faivre et al. 2003), some positive relationships (European Greenfinch, Saks et al. 2003; Pied Flycatcher, Kilpimaa et al. 2004; House Sparrow [in winter], Gonzalez et al. 1999b; Zebra Finch, Blount et al. 2003; McGraw and Ardia 2003), and some found no relationship (Red-winged Blackbird, Westneat et al. 2003; American Goldfinch [Carduelis tristis; Plate 30, Volume 1], Navara and Hill 2003). Despite the heterogeneity in the approach and findings of these studies, on the whole, it seems that the expression of coloration (plumage and bills) can be related to the functioning of the signaler’s immune system. However, it is often not clear whether colorful males have higher levels of resistance to parasites or have simply escaped exposure to them, although with regard to providing direct benefits to females, it may not matter. What is important is that a female choosing a colorful male selects a partner who is unlikely to harbor a large, potentially contagious parasite load and is in generally good health. Therefore, although the actual direct benefits to females listed above have not been specifically demonstrated, given the apparently clear relationship between parasites and the expression of ornamental color in males and the relatively straightforward nature of the potential direct benefits, it seems likely that such benefits are available to females.

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Indirect Benefits Signaled by Color The indirect benefits of mate choice to a female are those that improve the quality of her offspring rather than directly benefiting the female herself (Andersson 1994). It is often surprisingly difficult to separate direct and indirect benefits, as well as to determine the relative importance of the two forms of benefits. Consider the benefits of choosing a parasite-free partner. There are clearly direct benefits to the female, in the form of avoiding the parasite herself and having a healthy partner who can contribute to offspring care, and there may also be indirect benefits, in the form of resistance genes for offspring that could be inherited from their father. Generally, indirect benefits include all the additive genetic components of variation that females can gain from males. Assuming that variation in color expression is heritable (see Chapter 11, Volume 1), perhaps the most obvious indirect benefit that a female can potentially gain by choosing to mate with a brightly colored male is production of brightly colored sons. In both the House Finch (Hill 1991) and Great Tit (Parus major; Plate 11; Norris 1993), sons did indeed resemble their fathers with respect to ornamental coloration. However, this resemblance is not always as straightforward as it seems, and a key issue that remains to be satisfactorily answered is the relative contribution from environmental sources. The genes inherited from the father are responsible for a certain amount of the resemblance, but as indicated by the number of direct benefits cataloged above, there are clearly many other ways in which a father can influence the expression of color in his offspring. When Griffith et al. (1999a) cross-fostered young male House Sparrows between different nests, they found that the expression of the melanin-based throat patch of young males resembled the male who reared them (the foster father) rather than the genetic father (Figure 6.3), a result consistent with an earlier and widely neglected study of the Great Tit by Lemel (1993). So male birds, particularly in socially monogamous species in which they contribute a significant amount of care to their offspring, can affect the quality and appearance of their offspring through both environmental and genetic routes (direct and indirect effects, respectively). A major problem in empirical studies of indirect effects has been separating these two major sources of variation, a problem that is exacerbated in birds by the high levels of paternal care provided by many species. Traditionally, in the study of sexual selection, a dichotomy has arisen between the different theoretical models explaining indirect benefits, such that the Fisherian process (Fisher 1930) is often viewed as being a somewhat sep-

Benefits to Females of Assessing Color Displays

255

Mean badge size of surviving sons (mm)

40

35

30

25 25

30

35

40

45

Badge size of foster father (mm)

Figure 6.3. Relation between the badge size of male House Sparrows and that of their foster fathers (r = 0.62, n = 19, p = 0.005). There was no significant relation between the badge sizes of these males and their genetic fathers (r = 0.03, n = 18, p > 0.5; not shown), demonstrating the environmental determination of badge size in this species. Redrawn from Griffith et al. (1999a).

arate process to the viability models of sexual selection, such as the handicap model that was later proposed by Zahavi (1975). It is not clear how, or why, this dichotomy arose, but it seems to have come from misinterpretations of the original theoretical work rather than being intrinsic to the models themselves. Here the relevant question is to what extent females gain indirect benefits for their offspring by assessing the colored ornaments of males, and we do not try to differentiate among the indirect benefits models any further. The key indirect benefits (genetic components) that have been specifically investigated in birds are genes for attractiveness and viability. Given that sexually selected traits are thought to have evolved to capture and signal the condition of individuals (through heightened condition-dependent sensitivity in their expression; Rowe and Houle 1996), it is believed that an individual with good viability genes will also be phenotypically attractive (Andersson 1986). Therefore it is difficult to disassociate viability from attractiveness per se, and we do not attempt to do so here. Instead we refer to all indirect benefits as “good-genes” benefits, as this term encompasses all theoretical models of sexual selection (for indirect benefits) and both types of genetic benefits (attractiveness and viability) that might be available to a choosy female’s offspring.

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simon c. griffith & sarah r. pryke Good-Genes Benefits of Assessing Color Studies of extra-pair paternity in birds have provided good opportunities for investigators seeking to demonstrate the good-genes benefits to females of assessing male color. In more than 90% of avian species, social monogamy is observed, with a male and female pairing together for at least the duration of a reproductive cycle (Lack 1968). However, genetic polyandry is widespread and occurs, for example, in more than 85% of passerine species that have been surveyed using molecular markers (Griffith et al. 2002). Given that females apparently receive very little from the extra-pair sire except sperm, it is conventionally believed that the prime benefits to females indulging in extra-pair behavior are good genes for at least some of their offspring (in socially monogamous birds, just over 11% of all offspring are extra-pair; Griffith et al. 2002). This belief is overly simplistic, because there are other benefits that females may receive from extra-pair matings with colorful males. For example, females may seek extra-pair copulations to gain direct benefits, such as fertility assurance (Wetton and Parkin 1991) by using phenotypic clues from males to gauge their likely fertility (Sheldon 1994), or possibly to gain access to the superior territories of the most colorful males (Gray 1997). However, irrespective of whether direct or indirect benefits are the primary motivation for females seeking extra-pair copulations, any resulting extra-pair paternity certainly has the potential to provide indirect benefits to the female, and it is worth briefly summarizing the studies in this area. In many species, females appear to be selecting extra-pair mates nonrandomly with respect to male coloration (Table 6.4). In four of the species investigated so far, a positive relationship has been reported between male coloration and the number or proportion of extra-pair offspring fathered (Collared Flycatcher, Sheldon and Ellegren 1999; Yellow Warbler [Dendroica petechia], Yezerinac and Weatherhead 1997; Yellowhammer [Emberiza citrinella; Plate 15], Sundberg and Dixon 1996; Common Yellowthroat [Geothlypis trichas], Thusius et al. 2001). In a further eight species, a link has been found between male age and either gains in paternity in other nests or losses of paternity in their own nest. Most, if not all, of these species express age-dependent plumage to some degree (as in the House Sparrow; see Figure 6.1), and it is likely that either females are assessing male age using plumage characteristics or perhaps are not even assessing age directly but merely distributing extra-pair copulations with respect to plumage (and therefore the age dependence reported by the investigators is merely correlative). In many of these studies, plumage coloration was not scored directly.

Benefits to Females of Assessing Color Displays

257

Table 6.4. Phenotypic Correlates of Variation among Males in the Number of Extra-Pair Offspring in Their Own Brood and the Number of Extra-Pair Offspring They Sire in Other Broods Which males lose paternity? Ornamental color Collared Flycatcher (Fidecula albicollis) Common Yellowthoat (Geothlypis trichas)

Bluethroat (Luscinia s. svecica) Age American Redstart (Setophaga ruticilla) Bobolink (Dolichonyx oryzivorus) Bullock’s Oriole Eastern Bluebird

Indigo Bunting (Passerina cyanea) Purple Martin (Progne subis)

White-crowned Sparrow (Zonotrichia leucophrys)

Which males gain paternity?

Reference

Collared Flycatcher

Sheldon and Ellegren (1999)

Common Yellowthroat Yellowhammer (Emberiza citrinella) Yellow Warbler (Dendroica petechia)

Thusius et al. (2001) Sundberg and Dixon (1996)

American Redstart

Perreault et al. (1998)

Yezerinac and Weatherhead (1997) Johnsen et al. (2001)

Bollinger and Gavin (1991) Bullock’s Oriole (Icterus bullockii) Eastern Bluebird (Sialia sialis) House Sparrow (Passer domesticus)

Richardson and Burke (1999) Gowaty and Bridges (1991) Wetton et al. (1995) Westneat (1990)

Purple Martin

Wagner et al. (1996)

Red-winged Blackbird (Agelaius phoeniceus) White-crowned Sparrow

Weatherhead and Boag (1995) Sherman and Morton (1988)

Note: The table includes species in which a significant association has been demonstrated for each phenotypic variable in turn.

More incisively, extra-pair paternity allows direct assessment of the goodgenes benefits that females can gain from highly ornamented extra-pair males. This is because naturally occurring extra-pair paternity resembles a breeding experiment in which two males sire offspring with a single female and all the offspring are reared simultaneously in a shared environment, thereby removing the majority of confounding effects that would otherwise cloud an investigation of sire effects. This comparison of within- and extra-pair maternal half

simon c. griffith & sarah r. pryke

258

Difference in fledgling condition of half-sibs

2

1

0

–1

–2 –30

–20

–10

0

10

20

Difference in forehead patch area of sires (mm2)

Figure 6.4. The difference in condition between half-sibling Collared Flycatchers is related to the difference in the size of the white crown patches of their (within- and extra-pair) fathers in a cross-fostering experiment. Female flycatchers thus improve the condition of their offspring by producing offspring sired by large-patched males. Redrawn from Sheldon et al. (1997).

siblings, in relation to the color expressed by their respective fathers, has given the clearest insight into the indirect benefits available to females discriminating between males on the basis of their color. In their study of the Collared Flycatcher, Sheldon et al. (1997) revealed that extra-pair offspring fledge in better condition than their maternal half siblings, with the difference in quality being related to the difference in their father’s expression of a sexually selected trait (Figure 6.4). Therefore the indirect benefit that a female can gain is directly proportional to the difference in the expression of color in the potential fathers. Sadly, such data are relatively difficult to obtain, and the Sheldon et al. (1997) paper remains the only demonstration of its kind. Once again, the lack of other clear examples providing support for the indirect effects of assessing color almost certainly reflects the absence of adequate experimental studies rather than the lack of a biological relationship. Good-genes effects are notoriously weak, and in their meta-analysis of numerous good-genes studies, Møller and Alatalo (1999) found that on average, good-genes effects explained only 2% of the variation in viability among individuals. To reliably demonstrate such a weak effect requires a combination of large sample sizes, welldesigned experiments, and a thorough molecular analysis.

Benefits to Females of Assessing Color Displays

Genetic Compatibility Through the study of extra-pair paternity, a slightly different version of goodgenes mate choice has been proposed—mate choice for compatible genes (Tregenza and Wedell 2000). In birds, as in many other taxa, the level of genetic similarity between two parents can be an important source of offspring fitness (Tregenza and Wedell 2000). If parents are too closely related, then fitness may be reduced through the deleterious effects of inbreeding (e.g., Bensch et al. 1994; Kruuk et al. 2002). Although recent evidence in other taxa suggests that outbred individuals are more vigorous (Amos et al. 2001), there is an optimum level of outbreeding, because extreme outbreeding leads to hybridization, with its associated deleterious effects on offspring fitness and fertility (Haldane 1922). The genetic compatibility hypothesis deals with the selection on females to optimize the level of outbreeding by mating with genetically compatible mates. To date, very few studies have investigated the genetic compatibility hypothesis in birds, and none have specifically included color as a potential cue that females could use to assess genetic compatibility. The first avian study finding molecular evidence somewhat consistent with female extra-pair choice for compatible genes found that in two species of shorebird, extra-pair partners were less genetically similar to the female/male than the within-pair partner (Blomqvist et al. 2002). This result was interpreted as evidence that the male/ female recognized that their partner was genetically similar and sought extrapair paternity with less genetically similar individuals (Blomqvist et al. 2002). However, this conclusion is unlikely to be as straightforward as it appears (e.g., Griffith and Montgomerie 2003). A primary concern is that most of the mismatched offspring in the study were apparently the result of quasi-parasitism (extra-pair maternity). This phenomena has no logical adaptive explanation and has yet to be properly documented in birds, with the exception of two passerine species in which it probably occurs as a very rare stochastic byproduct of regular extra-pair paternity and intra-specific brood parasitism (Griffith et al. 2004). Furthermore, the interpretation by Blomqvist et al. (2002) of the difference between the level of genetic similarity between the pair individual and the within- and extra-pair partners relies on an unprecedented ability to behaviorally recognize the level of genetic similarity (see Griffith and Montgomerie 2003). In fact, one of the main problems posed by the genetic compatibility hypothesis is to explain the ability of a female to assess the genetic compatibility of potential mates. In the conventional good-genes models, good

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simon c. griffith & sarah r. pryke genes are an intrinsic trait, such that the best individuals are best for everyone in a population. For example, relative to a yellow male House Finch, the reddest male in the population will look reddest to all other individuals, and will also reliably signal a number of associated benefits (e.g., parasite resistance, courtship feeding). By contrast, genetic compatibility is an extrinsic trait, such that a single male may be very compatible with one female but completely incompatible with another. Therefore, in a normal population, there is unlikely to be a set of individuals who are optimally compatible with every female. For this reason, it is very difficult to imagine a trait that could signal compatibility, particularly through an ornament, such as color (Mays and Hill 2004). A recent study of the highly polyandrous lekking Ruff (Philomachus pugnax; Plate 7) has shed some light on how selection for genetic compatibility may occur in birds. In their study, Thuman and Griffith (2005) demonstrated that sperm competition within the reproductive tract of the female virtually always (in 12 of 13 cases) favored the least genetically similar male (relative to the female), despite the low levels of genetic similarity among the individuals. Therefore, even in a situation in which it is extremely unlikely that the females had any cues by which to prefer one male over another, in a conventional behavioral manner, paternity was distributed in a nonrandom fashion (Thuman and Griffith 2005). This finding suggests that although paternity may be distributed nonrandomly with respect to genetic compatibility, this may not be due to female mate choice in the conventional sense (following phenotypic signals or cues from males); instead female “choice” may be entirely cryptic, occurring at a cellular or physiological level. If female “choice” is occurring at this cryptic level, based on genetic compatibility, it is very unlikely that color plays any role in determining the outcome of this form of selection generally. Perhaps the only scenario in which color may be used by females to select compatible genes is in the relatively unusual situation in which two very closely related species occur in sympatry. In their study of sympatrically breeding Collared and Pied Flycatchers, Veen et al. (2001) found that, when females were paired with a male of the wrong species, they were far more likely to produce extra-pair offspring in their nest, who had been sired by a male of the correct species. Given that ornamental color is both a sexually selected trait and has diverged to reinforce pre-mating isolation in these species (Sætre et al. 1997), females could be using male color to adaptively find compatible genes in the local area (although the results of Veen et al. 2001 may also be explained by cryptic female choice, as described earlier in the Ruff; Thuman and Griffith 2005).

Benefits to Females of Assessing Color Displays

Immunocompetence Although similar to other forms of good-genes models, which are likely linked to both viability and the expression of ornamental traits through condition dependence, one subset of good genes worthy of additional discussion are genes for immunocompetence. As mentioned earlier, Hamilton and Zuk’s (1982) paper on parasite-mediated sexual selection sought to explain variation in avian color expression in relation to the parasites of those species. They specifically drew attention to the additive genetic variation underlying an individual’s ability to cope with parasite infections (i.e., good immunocompetence genes), although Hamilton did later point out that the direct benefits to females of avoiding contagion were also likely to play a significant role in mate choice (Hamilton 1990). The Hamilton and Zuk (1982) hypothesis, linking color, genes, and immunocompetence, has been one of the most fashionable in the field of behavioral ecology through the 1990s, and over a thousand studies have cited the paper. Despite this popularity, there is no clear evidence that by mating with colorful males, females gain indirect fitness benefits for their offspring. To date, only one study has directly investigated the indirect benefits of mate choice on immunocompetence. In their study of the Bluethroat (Luscinia svecica; Plate 19), Johnsen et al. (2000) showed that females enhanced their offspring’s immunocompetence through extra-pair copulations. Nestlings sired by extra-pair males had a higher T-cell–mediated immune response than did their maternal half siblings raised in the same nest (Figure 6.5). The comparison of maternal half siblings is particularly compelling because it controls for many of the nongenetic components of variation, which could otherwise contribute to the variation in immunocompetence. Although Johnsen et al. (2000) demonstrated that females can gain immunocompetence-related indirect benefits by discriminating among males, they were unable to find evidence that females choose males with which to have extra-pair copulations on the basis of color variation (Johnsen et al. 2000, 2001), and therefore only half of the story is complete in this species. As briefly reviewed in the direct benefits section of this chapter (and summarized in Table 6.3), most studies investigating immunocompetence have focused on the relationship between the expression of color and naturally or experimentally elevated parasite infection. Although both the approach and findings of these studies are often inconsistent, generally, high levels of parasite infections appear to depress color expression, and therefore a female may gain information about the state of an individual’s current health from his color. However, this information will not necessarily reflect indirect benefits

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262

Residual immune response of EPY (mm)

1

0.5

0

–0.5

–1 –1.2

–0.8

–0.4

0

0.4

0.8

Residual immune response of WPY (mm)

Figure 6.5. Relation between the residual immune response of within- (WPY; full siblings) and extra-pair young (EPY; half siblings) Bluethroats reared in the same nest (n = 32 broods). Equal response of WPY and EPY is indicated by the thick dashed line; extra-pair young more often had a higher response. Thus females improved the immunocompetence of some of their offspring by producing offspring sired outside the pair bond. Redrawn from Johnsen et al. (2000).

to offspring in the form of parasite-resistant genes because an individual’s current health (or parasite status) is also dependent on a wide range of environmental factors. At best, the relationship between parasite infection and color expression is a very indirect line of evidence for this indirect benefit and reveals little or nothing about the genes important for parasite resistance. At the moment, the biggest gap in our knowledge is that no study has conclusively shown that by choosing a brightly colored male, a female produces offspring that are more immunocompetent. In fact, no empirical study has yet clearly demonstrated that color is linked to more immunocompetent or parasite-resistant genes. Ironically (and despite its popularity) this link is the essence of the “good immunocompetence genes” theory initially proposed by Hamilton and Zuk (1982). Hopefully, given recent advancements in gene mapping for disease resistance, such studies will now be possible, and this important gap closed. Nevertheless, as individual fitness is likely related to the ability of individuals to resist pathogens, it would certainly benefit females to base mate choice decisions on ornamental variation, which is a cue of immunocompetence. Assuming that at least some components of immunocompetence are heritable, she will then gain indirect fitness benefits for her offspring. At the very least, she will gain the direct benefits of a mate who is in better health and less likely to infect her and her offspring (see above).

Benefits to Females of Assessing Color Displays

Future Challenges Perhaps more so than in other taxa, in birds, females can potentially gain a variety of direct and indirect benefits from males that will influence not only their own fitness, but also the fitness of their offspring. A diverse range of male traits and characters can be signaled by the color expressed in ornaments, and consequently, assessment of ornaments can lead to direct and indirect benefits to females. However, a key finding in our review is that, despite a general feeling that females are likely to gain a multitude of benefits from assessing color displays in males, there is very little good direct evidence to support this notion, and there are a number of big gaps in our knowledge. How much fitter is a female that chooses her mate compared to a female that mates randomly? To what extent are females able to discriminate natural variation in ornamental color? Are the direct or indirect components more important to females, and does that vary with female condition or age? Do the benefits gained from males affect daughters in the same way as sons? Do females use the same criteria when choosing a social and extra-pair mate? From the female perspective, these are quite basic questions and yet none have been tackled empirically.

Condition Dependence—A Unifying Direct and Indirect Benefit In trying to write a structured review of the different direct and indirect benefits that females can gain by assessing color, we have set quite artificial divisions between traits and benefits. In reality, of course, traits and benefits interact with one another in complex and interesting ways. Many benefits may be highly correlated, whereas others may trade off against one another, temporally (males obviously cannot incubate eggs and protect a territory at the same time), or perhaps physiologically (there is a well established trade-off between mating and parental effort; Ketterson and Nolan 1992). Nonetheless, through a potentially complicated tangle of different traits, there does seem to be one general unifying theme—condition. In every sense, for every direct or indirect benefit we have discussed (with the singular exception of genetic compatibility), females benefit most by selecting males in the best condition, and in fact, it is hard to imagine a trait for which a female would be better off by choosing a male in inferior condition. If females are always better off choosing a male in good condition over one in poor condition, and if all direct and indirect benefits are generally correlated in a predictable way to condition, then in effect, it would make sense for females to simply choose males on the basis of condition rather than parenting ability, territory acqui-

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simon c. griffith & sarah r. pryke sition ability, immunocompetence, and so on. In fact, although most studies have separated out these singular indices and we have confounded it by dividing this chapter into bite-size chunks based on these divisions, this makes little biological sense. A female House Sparrow is unlikely to choose a largebadged male simply because she is concerned about nest predators. In reality, a large-badged male is nearly always best (but see Griffith et al. 1999b) because he is dominant over other males (Møller 1988), will provide one of the best nest sites (Møller 1988), feed her offspring proficiently (Møller 1988), help her produce large-badged sons (Griffith et al. 1999a), have a good level of general immunity (Møller et al. 1996; Gonzalez et al. 1999a), and of course, help to defend her offspring (Reyer et al. 1998). All of these direct and indirect benefits are signaled by male badge size. What else does male badge size in the house sparrow signal? Condition. Following an earlier demonstration in the Collared Flycatcher (Gustafsson et al. 1995), Griffith (2000) manipulated condition in male House Sparrows in the wild by experimentally increasing or decreasing the number of chicks that males reared (chick rearing is obviously a costly activity and will affect future condition) and then comparing the badge expressed in the molt 3 months after the experiment with that expressed previously. Just as in the flycatchers, there was a clear relationship between the manipulation of reproductive effort and a proportional change in ornament expression; the more chicks a male reared, the smaller his ornament became and vice versa (Gustafsson et al. 1995; Griffith 2000; Figure 6.6). From an evolutionary perspective, it makes far more sense that ornamental traits have evolved to signal condition, a unifying trait that interacts with all aspects of genetic quality, health, good fortune, and life-history, rather than that such traits have evolved simply to communicate with a female about simple, individual and often inconsequential indices. Condition-dependent sexual selection (Fisher 1930; Andersson 1986; Rowe and Houle 1996) is striking because it is such a simple and potentially efficient process, enabling females to always select the individuals that will maximize the benefits they can gain. An individual’s condition is potentially affected by every part of its genome and every intrinsic or extrinsic factor that affects its development, growth, and health, including completely stochastic factors. For example, did a male hatch in a cold, rainy spell, during which time its parents could not feed it properly, or did it have the good fortune to hatch during the peak of a seasonal crop of food in a particularly favorable year? Was the individual lucky enough to avoid contagion with any of a myriad of potential par-

Residual change in patch size (mm2)

Proportional change in badge size

Benefits to Females of Assessing Color Displays

265

a 0.2

3

6 0

7

4

1

17

26

15

–0.2

b 17

10

35 0

–10

–1 0 2 1 Experimental change in number of nestlings

–2

Figure 6.6. Relation between a manipulation of reproductive investment in spring (number of offspring added or removed from a brood) and the change (after the next nuptial molt) in expression of the subsequent ornament in (a) House Sparrows and (b) Collared Flycatchers, 4 or 10 months later, respectively. The plumage display of House Sparrows is melanin-based, whereas the white crown patches of Collared Flycatchers results from incoherent scattering by microstructures. Graphs show means ± standard errors with sample sizes above each bar. Redrawn from Griffith (2000) and Gustafsson et al. (1995).

asites (some of which it may not have had any genetic resistance to)? Individuals are genetically unique, and by the time they come to express even their first sexually selected ornament, every individual will have followed a unique, detailed life-history (based on hundreds of little scenarios like those mentioned above). Ultimately, these interactions determine the overall condition of that individual at the time at which they express their first color ornament (Box 6.1).

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Box 6.1. Condition-Dependent Expression of Variation in Ornament Expression Figure B6.1 shows a simplistic graphical representation of conditiondependent models of sexual selection (Andersson 1986; Rowe and Houle 1996) in which the expression of variation in ornamental traits is generally mediated through condition. Few natural factors directly affect expression (solid arrows). Generally, factors will affect condition (broken arrows) and, subsequently, condition as a whole will influence ornament expression. For simplicity, only a very few of the hundreds of biotic and abiotic sources of variation in condition have been shown. For example, parasites, good genes, and the investment their parents made during their development all contribute toward the variation in condition among individuals. It is unlikely that these factors directly influence ornament expression, which explains the persistent effects of factors on ornament expression. For example, the manipulation of brood size in the Collared Flycatcher (Gustafsson et al. 1995) affects the expression of a trait that is not even produced until 10 months later (see Figure 6.6). Some factors have both a direct and indirect effect on ornament expression. One obvious example is nutrition. Overall levels of nutrition help determine condition (with an indirect effect on ornament expression, as mentioned above), but specifically, the level of carotenoids in the diet will influence an individual’s ability to express a carotenoid-based ornament. In the extreme case in which carotenoids are removed from the diet, individuals will not be able to express carotenoid-based color. Similarly, genetic elements can have direct and indirect effects. Some genes contribute directly to the expression of the trait, and thousands of other genes influence individual condition and so affect the ornament indirectly. Finally, although for simplicity, only one is shown in the figure, there are many interactions among factors, condition, and ornament expression. For instance, social dominance is an intermediary in a feedback loop between condition (dominant individuals have good access to resources) and the expression of ornaments. If we manipulate any one of those things, other factors will probably be affected as well. For example, when we manipulate color in an individual, we also affect its dominance interactions and therefore—through its access to resources and its stress levels—the individual’s condition.

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Nutrition

Good genes Condition

Variation in ornament expression

Condition Reproductive investment

Parasites Social dominance

Figure B6.1.

On average, a female will always benefit most by pairing with a male in good condition. To her, it does not matter why he is in good condition. It could be because he has been exceptionally lucky, or alternatively, he has been unlucky but possesses exceptionally good genes that have counteracted his bad luck. What is important to her is that he is fit, healthy, and in an ideal position to provide all the direct benefits that are obviously so important to many birds. Good genes are also important and the chances are high that he will have a pretty good set of genes for coping with that particular environment. What adds efficiency to the process is that if environmental circumstances change quite dramatically and perhaps favor a new suite of genes, then a highly condition-dependent signal will very quickly allow individuals with those new “good genes” to be identified by females. Imagine, for example, that a new pathogenic parasite is introduced into a population. Even if only 10% of the population has specific resistance genes, the next time individuals express an ornamental trait (e.g., after a molt), we would expect those individuals with the resistance genes to display the highest expression of the condition-dependent trait. Without having to make any changes to their existing mate-preference functions, females would be able to select and reproduce with those males, quickly spreading their genes through the population. Imagine, by contrast, the situation in which ornaments are mechanistically linked to single traits (e.g., resistance to a specific parasite, ability to feed nestlings, nest defense).

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simon c. griffith & sarah r. pryke How long, in comparison, would it take for a population to link the expression of color variation with each new trait and for females to learn a new preference function? In summary, there should be intense selection for females to choose males for all of the benefits reviewed above. However, selection is likely to favor males in good overall condition, which, in turn, has favored the evolution of male signals that capture condition in the broadest sense. Logically, it makes no biological sense to split female choice into distinct components, like the subdivisions of this chapter. Furthermore, given the interrelationships among the different traits (particularly through condition), it is impossible to determine the real motivation behind any subsequently observed female choice. For example, an experiment that manipulates diet will also affect condition, dominance, ornamentation, health, and a range of other variables. In the future, we need not only to understand the complexities of the models of conditiondependent signaling, but also to study signals with a more holistic approach. Instead of concentrating on the individual components of male signals, a key challenge is to measure the extent of selection on females to choose males, as well as the efficiency of the overall evolutionary process.

Benefits to Females of Assessing Color and Variation in Avian Color One of the main questions that this book addresses is: what causes the tremendous diversity of color across birds? In the context of this chapter, we can think about that question by imagining two small birds, high above the street on a telephone wire, a male House Finch and a male House Sparrow. One has a bright red streak of carotenoid-based plumage on its breast, the other, a large melanin-based black patch stretching from its bill halfway down its chest. Both males are in their prime. From their extravagant plumage displays, both are the most attractive males on the block (in their respective cohorts). As we look at them, and in particular at the size or color of their ornaments, what else can we really tell about the underlying qualities of the two males? More importantly, does the red carotenoid color of the House Finch tell a different story than that of the black melanin-containing patch of the House Sparrow? Do females of the two species learn something specifically different about male qualities from either the carotenoid or melanin plumage? Or do they both gain the same information that is simply signaled by a different pigment in each species?

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Should there be any difference in the ability of variously colored ornaments (melanins, carotenoids, or structural colors) to signal condition generally? There is no logical reason why there should be. On average, the selective force on females to be able to discriminate among males and pick the partners in best condition should be equal across different species of birds. Likewise, the selection on males to honestly advertise their condition should, on average, be equal across different species. Presumably, the colors of condition-dependent ornaments used by species today are those that were available to those lineages in their evolutionary past and that have now been captured as useful signals. For example, parrots use psittacofulvins in their bright red color signals (Chapter 8, Volume 1), rather than carotenoids, simply because synthesis of those pigments evolved in parrots. Currently there is no evidence that, at some stage in the evolutionary history of a particular group, different pigments were “tried out” and “rejected” by the evolutionary process. Did an ancestral cardueline finch use melanin as a sexual ornament before replacing it with carotenoids? Obviously, we will never know. However, if we do not believe this was the case, then is there any reason to believe that some classes of color are inferior sexual signals compared to others? If selective pressures to produce a good signal are roughly equal across all classes of color, then we can assume that evolution has probably brought them all to a relatively equal standard, in much the same way that insect and bird wings have all been turned into equally good mechanisms for flight.

Summary Female birds gain a wide variety of benefits from their male partners, enhancing their own fitness and the fitness of their offspring. Direct benefits help to explain the high level of bi-parental care in birds. This widespread social monogamy led (almost inevitably) to widespread infidelity and genetic polyandry, which is at least partly maintained by the indirect benefits to females from extra-pair males. Given the importance of both types of benefit (and also because females can simultaneously maximize the capture of both), we expect strong selection on females to assess males and it would be surprising if they did not use ornamental color to help them in their mate-choice decisions. Ornamental color in males is expressed with a high degree of conditiondependence, making it an ideal signal for females, given that males in good condition will invariably be the best social mates.

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Although the empirical work in this area supports the very general summary above, definitive support for most types of benefits of mate choice are lacking. The vast majority of studies we have reviewed are descriptive in nature and completely unable to untangle the complex interactions among the traits involved in the potential benefits of choice for color. Even the more experimental work in this field is generally quite limited in its scope and has tackled a very small part of a complex system. A surprising number of quite basic questions have yet to be addressed at all in this area. When all the studies are considered, we are left still to wonder whether females benefit by assessing color displays.

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Benefits to Females of Assessing Color Displays Rohwer, S. 1975. The social significance of avian winter plumage variability. Evolution 29: 593–610. Rohwer, S. 1982. The evolution of reliable and unreliable badges of fighting ability. Am Zool 22: 531–546. Røskaft, E., and S. Rohwer. 1987. An experimental study of the function of the red epaulettes and black body colour of male Red-winged Blackbirds. Anim Behav 35: 1070–1077. Roulin, A. 2001. Food supply differentially affects sibling negotiation and competition in the Barn Owl (Tyto alba). Behav Ecol Sociobiol 49: 514–519. Rowe, L., and D. Houle. 1996. The lek paradox and the capture of genetic variance by condition-dependent traits. Proc R Soc Lond B 263: 1415–1421. Sætre, G. P., T. Fossnes, and T. Slagsvold. 1995. Food provisioning in the Pied Flycatcher—Do females gain direct benefits from choosing bright colored males? J Anim Ecol 64: 21–30. Sætre, G. P., T. Slagsvold, A. Kruszewicz, and H. Viljugrein. 1997. Paternal care in Pied Flycatchers Ficedula hypoleuca: Energy expenditure in relation to plumage colour and mating status. Ardea 85: 233–242. Saks, L., I. Ots, and P. Hõrak. 2003. Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence. Oecologia 134: 301–307. Sanz, J. J. 2001. Experimentally reduced male attractiveness increases parental care in the Pied Flycatcher Ficedula hypoleuca. Behav Ecol 12: 171–176. Searcy, W. A. 1979. Male characteristics and pairing success in Red-winged Blackbirds. Auk 96: 353–363. Sheldon, B. C. 1994. Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proc R Soc Lond B 257: 25–30. Sheldon, B. C., and H. Ellegren. 1999. Sexual selection resulting from extra-pair paternity in Collared Flycatchers. Anim Behav 57: 285–298. Sheldon, B. C., J. Merilä, A. Qvarnström, L. Gustafsson, and H. Ellegren. 1997. Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character. Proc R Soc Lond B 264: 297–302. Sherman, P., and M. Morton. 1988. Extra-pair fertilizations in mountain Whitecrowned Sparrows. Behav Ecol Sociobiol 22: 413–420. Siefferman, L., and G. E. Hill. 2003. Structural and melanin coloration indicate parental effort and reproductive success in male Eastern Bluebirds. Behav Ecol 14: 855–861. Slagsvold, T. 1986. Nest site settlement by the Pied Flycatcher: Does the female choose her mate for the quality of his house or himself? Ornis Scand 17: 210–220. Slagsvold, T., and J. T. Lifjeld. 1988. Plumage colour and sexual selection in the Pied Flycatcher (Ficedula hypoleuca). Anim Behav 36: 395–407. Smiseth, P. T., and T. Amundsen. 2000. Does female plumage coloration signal parental quality? A male removal experiment with the Bluethroat (Luscinia s. svecica). Behav Ecol Sociobiol 47: 205–212.

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simon c. griffith & sarah r. pryke Smiseth, P. T., J. Ornborg, S. Andersson, and T. Amundsen. 2001. Is male plumage reflectance correlated with paternal care in Bluethroats? Behav Ecol 12:164–170. Smith, D. G. 1972. The role of the epaulettes in the Red-winged Blackbirds (Agelaius phoeniceus) social system. Behavior 41: 251–268. Stanback, M., D. S. Richardson, C. Boix-Hinzen, and J. Mendelsohn. 2002. Genetic monogamy in Monteiro’s Hornbill, Tockus monteiri. Anim Behav 63: 787–793. Stearns, S. C. 1989. Trade-offs in life-history evolution. Funct Ecol 3: 259–268. Studd, M. V., and R. J. Robertson. 1985. Evidence for reliable badges of status in territorial Yellow Warblers (Dendroica petechia). Anim Behav 33: 1102–1113. Sundberg, J. 1995. Parasites, plumage coloration and reproductive success in the Yellowhammer, Emberiza citrinella. Oikos 74: 331–339. Sundberg, J., and A. Dixon. 1996. Old, colourful male Yellowhammers, Emberiza citrinella, benefit from extra-pair copulations. Anim Behav 52: 113–122. Sundberg, J., and C. Larsson. 1994. Male coloration as an indicator of parental quality in the Yellowhammer, Emberiza citrinella. Anim Behav 48: 885–892. Thompson, C. W., N. Hillgarth, M. Leu, and H. E. McClure. 1997. High parasite load in House Finches (Carpodacus mexicanus) is correlated with reduced expression of a sexually selected trait. Am Nat 149: 270–294. Thuman, K. A. and S. C. Griffith. 2005. Genetic similarity and the nonrandom distribution of paternity in a genetically highly polyandrous shorebird. Anim Behav 69: 765–770. Thusius, K. J., K. A. Petersen, P. O. Dunn, and L. A. Whittingham. 2001. Male mask size is correlated with mating success in the Common Yellowthroat. Anim Behav 62: 435–446. Tolonen, P., and E. Korpimaki. 1994. Determinants of parental effort—A behavioral study in the Eurasian Kestrel, Falco tinnunculus. Behav Ecol Sociobiol 35: 355– 362. Tregenza, T., and N. Wedell. 2000. Genetic compatibility, mate choice and patterns of parentage: Invited review. Mol Ecol 9: 1013–1027. Veen, T., T. Borge, S. C. Griffith, G. P. Sætre, S. Bures, L. Gustafsson, and B. C. Sheldon. 2001. Hybridization and adaptive mate choice in flycatchers. Nature 411: 45–50. Veiga, J. P. 1993. Badge size, phenotypic quality, and reproductive success in the House Sparrow: A study on honest advertisement. Evolution 47: 1161–1170. Vershinin, A. 1999. Biological functions of carotenoids: Diversity and evolution. Biofactors 10: 99–104. Voltura, K. M., P. L. Schwagmeyer, and D. W. Mock. 2002. Parental feeding rates in the House Sparrow, Passer domesticus: Are larger-badged males better fathers? Ethology 108: 1011–1022.

Benefits to Females of Assessing Color Displays von Schantz, T., S. Bensch, M. Grahn, D. Hasselquist, and H. Wittzell. 1999. Goodgenes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B 266: 1–12. Wagner, R. H., M. D. Schug, and E. S. Morton. 1996. Confidence of paternity, actual paternity and parental effort by Purple Martins. Anim Behav 52: 123–132. Walther, B. A., D. H. Clayton, and R. D. Gregory. 1999. Showiness of Neotropical birds in relation to ectoparasite abundance and foraging stratum. Oikos 87: 157–165. Weatherhead, P. J., and P. T. Boag. 1995. Pair and extra-pair mating mating success relative to male quality in Red-winged Blackbirds. Behav Ecol Sociobiol 37: 81–91. Westneat, D. F. 1990. Genetic parentage in the Indigo Bunting: A study using DNA fingerprinting. Behav Ecol Sociobiol 27: 67–76. Westneat, D. F., D. Hasselquist, and J. C. Wingfield. 2003. Tests of association between the humoral immune response of Red-winged Blackbirds (Agelaius phoeniceus) and male plumage, testosterone, or reproductive success. Behav Ecol Sociobiol 53: 315–323. Wetton, J. H., and D. T. Parkin. 1991. An association between fertility and cuckoldry in the House Sparrow, Passer domesticus. Proc R Soc Lond B 245: 227–233. Wetton, J. H., T. Burke, D. T. Parkin, and E. Cairns. 1995. Single-locus DNA fingerprinting reveals that male reproductive success increases with age through extra-pair paternity in the House Sparrow (Passer domesticus). Proc R Soc Lond B 260: 91–98. Wimberger, H. 1988. Food supplement effects on breeding time and harem size in the Red-winged Blackbird (Agelaius phoeniceus). Auk 105: 799–802. Wolfenbarger, L. L. 1999. Red coloration of male Northern Cardinals correlates with mate quality and territory quality. Behav Ecol 10: 80–90. Wright, J., and I. Cuthill. 1989. Manipulation of sex differences in parental care. Behav Ecol Sociobiol 25: 171–181. Yasukawa, K. 1981. Male quality and female choice of mate in the Red-winged Blackbird (Agelaius phoeniceus). Ecology 62: 922–929. Yezerinac, S. M., and P. J. Weatherhead. 1997. Extra-pair mating, male plumage coloration and sexual selection in Yellow Warblers (Dendroica petechia). Proc R Soc Lond B 264: 527–532. Zahavi, A. 1975. Mate selection—A selection for a handicap. J Theor Biol 53: 205–214. Zuk, M. 1991. Sexual ornaments as animal signals. Trends Ecol Evol 6: 228–231.

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7 Female Coloration: Review of Functional and Nonfunctional Hypotheses trond amundsen and henrik pärn

Historically, the vast majority of bird coloration studies have focused on showiness in males and the phenomenon of female coloration has been largely ignored (Amundsen 2000a,b). However, conspicuous female coloration is far from rare in birds. On the contrary, in many avian species both males and females are spectacularly colorful. Conspicuous female coloration has a wide distribution taxonomically, with examples in many avian families (e.g., see Table 7.1). The phenomenon is common both among nonpasserine and passerine birds. The aim of this chapter is to summarize current ideas and evidence regarding the evolution of female colors and to provide a platform for future studies that could eventually lead to a better understanding of female beauty among birds. The taxonomy and nomenclature of this chapter follows Clements (2000). We adopt a simplistic, human-vision-based approach to conspicuousness in the following survey. Our review includes all kinds of conspicuous female coloration in birds, ranging from subtle to brilliantly spectacular. We have attempted to be comprehensive in coverage both taxonomically and with respect to types of coloration. Although it may sometimes be difficult to judge whether a color is conspicuous or cryptic in the species’ natural environment (Endler 1990; Chapter 4, Volume 1), we have, for pragmatic reasons, consid-

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ered the color of a female bird to be conspicuous if, to the human eye, the color seems more likely to make the bird stand out from, rather than blend in with, its surroundings. This wide definition would encompass everything from rather subtly colored grebes and auks to such spectacularly colorful birds as rollers and tanagers. Much of the literature on the evolution of avian color patterns (e.g., Bleiweiss 1997; Owens and Hartley 1998; Badyaev and Hill 2000, 2003; Dunn et al. 2001) has focused on the degree to which males and females differ in coloration, which likely reflects differences in selection pressures acting on the two sexes. Here, our main focus is not so much on the contrast between the two sexes but rather on the females themselves: are they in any sense conspicuous in coloration or not? If they are, the mere fact calls for an evolutionary explanation, in functional (adaptive) or nonfunctional (neutral or maladaptive) terms. As previously pointed out (Amundsen 2000a), studies aiming to understand the evolution of female traits should focus on the traits themselves rather than comparing them with male traits (Box 7.1). This is not to say that comparisons with males are less valuable; they are instead suitable for formulating and answering different questions. Several functional and nonfunctional explanations of female coloration in birds have been suggested (Figure 7.1). Our aim in the present chapter is to assess the merit of each hypothesis based on the current evidence. Historically, the main nonfunctional explanation has been that female colors are mere byproducts of sexual selection acting on male coloration (Figure 7.1). Female coloration has also been suggested to proximately reflect sex hormone levels, especially in species in which only a minority of females is colorful. The main adaptive hypotheses to explain female colors are that they either signal dominance status or are attractive to potential partners (Figure 7.1)—the same functional explanations often applied to male color displays. Finally, female colors could play a role in species recognition or in concealment of sexual identity.

Categorizing Female Coloration Heuristically it is helpful to categorize the diversity of female colors in birds based on both the female colors themselves and on the degree to which male and female colors of the same species differ. Such a categorization is useful as a first description of the phenomenon and as a background for understanding the historical and conceptual development of the field. The result is five main

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Box 7.1. Does Monomorphism Signify No Sexual Selection? It is remarkable that species in which both sexes are conspicuously colorful or otherwise decorated have rarely been subject to study in relation to sexual signaling. According to conventional thinking, such cases are explained by selective processes other than sexual signaling that favor a conspicuous appearance in females, including species recognition. In comparative work, sexual dimorphism (including dichromatism) has often been used as proxy for sexual selection (e.g., Owens and Hartley 1998; Dunn et al. 2001). Undeniably, this approach has often proven successful (see Badyaev and Hill 2003). The relative success of such studies lends some support to the traditional view that sexual selection is mainly acting on males. However, one fundamental limitation to this approach is the confusion of two very different phenomena—drab monomorphism and conspicuous monomorphism. Both of these types of monomorphism are implicitly or explicitly assumed to reflect an absence of sexual selection. The two states are so different, however, that they can be considered the extremes of a continuum with dimorphism in the middle. Treating these two situations as fundamentally the same is in conflict with the idea that coloration and other forms of ornamentation carry a cost, which for males has been taken to imply that conspicuousness must have a function to be maintained over the course of evolution. It is hard to see why costs should not also apply to conspicuous female ornaments. Although drab monomorphism begs the question why neither sex carries extravagant ornamentation, cases in which both sexes are conspicuously colored call for explanations of the decorations of both sexes. Obviously, these functions can be nonsexual, as traditionally assumed, but there is no a priori reason to assume that sexual selection is unimportant when both sexes are colorful. Instead, it is quite possible that sexual selection may act on both sexes, not only on males. We suggest that, in the future, researchers should not consider dichromatism or monochromatism as character states, but rather focus on the appearance of the two sexes. Each sex (or individual) may be very drab, highly conspicuous, or something in between (because colors come in degrees). Quantification of the actual coloration of each sex, ideally in relation to the natural environment of the species, is an essential prerequisite for careful investigation of color functions in the two sexes.

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283 Ultimate function

Status signaling (female-female competition)

Mate attraction (male mate choice)

Species recognition

Concealment of sexual identity

Female coloration

Genetic correlation

Hormones

Proximate mechanism Figure 7.1. Flowchart showing proximate and ultimate factors that can determine expression of coloration in female birds.

classes of bird color patterns: (1) females and males equally colorful, (2) both sexes colorful but males more so, (3) both sexes colorful but females more so, (4) both sexes colorful but differently so, and (5) only females colorful. Both Sexes Equally Colorful The typical condition for birds is often thought to be bright males and drab females, but in many avian families, both males and females are conspicuously colored. Families with mostly monomorphically bright species include cassowaries, penguins, grebes, cranes, gannets and boobies, ibises, auks, jacanas, toucans, barbets, pittas, kingfishers, motmots, bee-eaters, rollers, jays, shrikes, waxwings, and tanagers. Often, species displaying monochromatically conspicuous plumages also have extensive mutual displays, as illustrated by Greatcrested Grebes (Podiceps cristatus; Huxley 1914). Most families dominated by monochromatically bright species have been subject to little research on sexual or signal selection. Several, but far from all, of these families have their main distribution in tropical or subtropical regions. Species in which both males and females are colorful span the full range of mating systems. Whereas penguins, puffins, and kingfishers are typically monogamous, jacanas are largely polyandrous, some tanagers are polygynous, and many bee-eaters and some toucans are cooperative breeders. For several of the families in question, in particular those inhabiting the tropics, little is currently known about the breeding biology. That birds can see parts of the spectrum invisible to humans (e.g., Bennett et al. 1994) implies that species that appear monochromatic to humans can

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trond amundsen & henrik pärn be dichromatic in the eyes of the birds (Andersson et al. 1998; Mahler and Kempenaers 2002; Eaton and Lanyon 2003). This circumstance calls for caution in classifications of monochromatic versus dichromatic species. However, when males and females are identically and conspicuously colored in the visible parts of the spectrum, a human-vision-based initial classification may be justified, ideally to be verified or corrected by subsequent spectral analyses. Both Sexes Colorful but Males More So The number of species in which both sexes display some degree of conspicuous coloration but the male is clearly the more extravagant is vast. To our knowledge, no survey has established whether this condition is more or less common than the “classical” case in which males only are conspicuous and females entirely drab (not discussed here). However, in several bird families (e.g., parrots, hummingbirds, woodpeckers, trogons, leafbirds, many other passerine families) females are typically similar to males in coloration but paler. It is a highly variable class, with female colors ranging from conspicuous and almost as gaudy as the males (e.g., many hornbills) to only rudimentary traces of “malelike” coloration (e.g., many passerines). We would not be surprised if a proper species-level survey found more than a thousand cases of this pattern. Wellstudied examples include House Finches (Carpodacus mexicanus; Plate 14; Hill 1993a,b, 2002) and Bluethroats (Luscinia svecica; Plate 19; Amundsen et al. 1997; Rohde et al. 1999; Smiseth and Amundsen 2000). These may represent the extremes among temperate passerines: “colorful” House Finch females have only traces of male-like coloration, whereas the most colorful female Bluethroats are almost identical to males. The Bluethroat case may be instructive with regard to the risk of neglect of colorful female variants. Until recently, the general view of females of the species was that they were entirely drab in appearance (as illustrated in most field guides). In contrast, our studies have revealed that the average Bluethroat female has marked, although not very conspicuous, blue and chestnut coloration (e.g., Amundsen et al. 1997). “Rudimentary” coloration in females, as seen in Bluethroats and even more typically in House Finches, Northern Cardinals (Cardinalis cardinalis; Plate 25), and several other passerines, has traditionally been considered to have no adaptive value. Instead, the fact that females sport “pale reflections” of male extravaganza has constituted the empirical basis for the correlated response hypothesis: such female colors have been considered byproducts of selection on males (Darwin 1871; Lande 1980). Evidence from studies on Bluethroats

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(Amundsen et al. 1997), House Finches (Hill 2002), and Northern Cardinals ( Jawor and Breitwisch 2003b; Jawor et al. 2003), however, suggest that this hypothesis is not the sole explanation of female colors. Both Sexes Colorful but Females More So This is a relatively rare phenomenon among birds, occurring, to our knowledge, only among polyandrous species in which sex roles are supposedly reversed. These include Greater Painted-snipes (Rostratula benghalensis), three phalarope species, and Eurasian Dotterels (Charadrius morinellus; Plate 20). Notably, however, the many jacanas with polyandrous mating systems are mainly monochromatic, so brighter females are not a necessary consequence of polyandry. Although painted-snipe males are very drab compared to females, phalarope and dotterel males are normally only slightly less colorful than the females (del Hoyo et al. 1992–2005). Darwin (1871) was well aware of the color patterns of these species and attributed drab male and bright female coloration mainly to their unusual pattern of parental care, with the males performing most of the incubation duties while the females mated again with other males. To our knowledge, among these species, only the Eurasian Dotterel (Owens et al. 1994) and the Red-necked Phalarope (Phalaropus lobatus; Reynolds 1987) have been subject to research on the functions of female plumage. Both Sexes Colorful but with Different Colors Species in which males and females have different conspicuous colors or other ornaments are particularly interesting, because such cases can hardly be correlated byproducts of selection on males but must somehow be due to selection acting directly on the females (Amundsen 2000a; Amundsen and Forsgren 2001). Such different male and female colors seem more common among fishes (e.g., wrasses, family Labridae; Amundsen 2000a, 2003) than birds, but no systematic survey exists, to our knowledge, for birds. Such species can be found, however, in several avian families. Perhaps the best known example is the Eclectus Parrot (Eclectus roratus; Plate 19), in which males are largely green with some red and blue and with bright reddish beaks, whereas females are conspicuously red and blue, with black beaks (Heinsohn et al. 2005). In the Torrent Duck (Merganetta armata), a riverine duck from the high Andes, the males have conspicuous white/black patterns that are lacking in females. Females instead have a rufous-red underside, quite conspicuous in the barren

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high Andes landscape (del Hoyo et al. 1992–2005). Another remarkable example is the hummingbird Juan Fernandez Firecrown (Sephanoides fernandesis), in which males are bright orange but females iridescent blue-green with a white belly; until the mid-nineteenth century, the sexes were thought to be different species. Further examples include Fairy-bluebirds (Irena spp.), in which females of many species are glittering blue-green, unlike the males, and typical antbirds (Thamnophilidae), in which females of certain species have a conspicuous red cap not present in males (del Hoyo et al. 1992–2005). To our knowledge, no avian species with differently bright males and females has yet been subject to sexual selection research. Only Females Colorful We are not aware of any species in which females are conspicuously colorful but males entirely drab. The closest example we can think of is the Greater Painted-snipe, but even in this species, the males have traces of female-like patterns. Another close candidate might be the Eclectus Parrot, in which females are red and blue but the males green with bright bills and smaller red and turquoise color patches (Heinsohn and Legge 2003; Heinsohn et al. 2005; Plate 19). The absence of species in which only the females are colorful is in striking contrast to the probably thousands of species in which only the males are colorful, and this pattern makes the relative neglect of the study of female coloration somewhat understandable historically.

The Many Kinds of Beauty Female coloration, like male coloration, can occur in an extraordinary variety among birds (see the other chapters of this volume and the color plates). The search for general explanations of broad classes of phenomena that share principal similarities has often led researchers to collapse the vast color diversity into “bright” versus “drab” or “dichromatic” versus “monochromatic.” Although such generalizations are useful in certain contexts, it may also be useful to keep in mind how variable avian coloration is. Variability can be briefly described along a number of axes, as detailed in this section. Simple versus Complex The simplest forms of coloration are well-defined patches of uniform color (e.g., breast patches in Rock Petronias [Petronia petronia]); the more complex in-

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clude a combination of several pigment-based and structural colors covering most body parts, sometimes overlapping one another (e.g., parrots, tanagers). Notably, most research on female colors so far has been carried out on species with rather simple and often not very conspicuous coloration (e.g., see Tables 7.1–7.3). Colors versus Appendages Birds not only have gaudy colors, they often possess more (e.g., birds of paradise) or less (e.g., Northern Cardinals) extravagant modifications of plumage (e.g., tails, crests, plumes) or skin (e.g., combs, wattles). Like gaudy coloration, such extravagant structures are less common in females than in males, but crests (e.g., in European Shags [Phalacrocorax aristotelis], Crested Auklets [Aethia cristatella]), plumes (e.g., in Least Auklets [A. pusilla; Plate 12]), and long tails (e.g., in motmots) can sometimes be equally developed in females and males. Colors and plumage modifications are not independent traits; instead, all appendages have color, frequently quite conspicuous. By and large, sexual selection theory has treated colors and other plumage extravaganza as fundamentally the same (“costly ornaments”). Although this may be true in a broad sense, the evolution of colors and appendages may be functionally related instead of merely being two ways to achieve the same goal. For instance, it is conceivable that appendages can evolve as amplifiers of informative colors (sensu Hasson 1990), or even that colors can amplify informative plumage modifications (appendages). Cases in which such amplifier functions may be worth considering include the elongated bright red tail feathers of Red-tailed Tropicbirds (Phaethon rubricauda) and the white head plumes of Inca Terns (Larosterna inca) that contrast their dark head. Thus some traits discussed in the present chapter are both colorful and ornamentally structured. In certain cases, the sizes of such appendages but not their colors have been subject to investigation. Indeed, measuring the size of a colored feather appendage provides information very similar to that obtained by measuring the size of a colored patch located on otherwise nonornamental body parts. Bearing in mind that, in males, color signals used both in status signaling (Chapter 3) and for mate attraction (Chapter 4) need not be very flashy (e.g., breast patches of House Sparrows [Passer domesticus; Plate 23, Volume 1], head patterns of Zonotrichia sparrows), we have included female appendages even when these are not strikingly colorful (e.g., the head plumes of auks; Tables 7.1–7.3).

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Position of Color on the Body The female plumage colors that have been studied in a number of species have been variably positioned on the body: head, throat, breast, rump, back, tail, wings, for example. From a naive perspective, one might consider certain positions of conspicuous coloration less viable candidates for a signaling function. One remarkable example is female under-wing color in Northern Cardinals, apparently positioned so as not to be displayed. However, it has recently been reported that female Northern Cardinals have evolved a particular display to show off this coloration, involving waving of the wings (Jawor and Breitwisch 2003b). The lesson to be learned is that the function of a color is not easily interpreted from its color and position alone; display behaviors could often better reveal cues to function (Andersson 1994). Although it is possible that the position of colors on the female body may relate to signal function, this idea will not be dealt with further in this chapter. Pigment-Based versus Structural Colors As is the case for studies of male coloration, most tests of female coloration in relation to quality, competition, or mate choice have not properly investigated the pigment or structural basis of the color(s) in question. Therefore, statements regarding these issues in the present analyses (e.g., see Tables 7.1–7.3) are mostly made by judging the pigments by their colors, an approach with obvious limitations (McGraw et al. 2004). Despite these limitations, it appears clear that conspicuous female colors span the full range of pigments (e.g., eumelanins, phaeomelanins, carotenoids, pterins, psittacofulvins) as well as structural colors. However, studies on the function of each kind of color (pigment or structure) in females are too few to reveal any clear pattern with regard to function. Therefore most of our discussion focuses on colors in a general sense. Visible versus Invisible Colors With a few exceptions (e.g., Andersson et al. 1998; Safran and McGraw 2004; Heinsohn et al. 2005, Komdeur et al. 2005; Siefferman and Hill 2005), studies of female colors have been based solely on techniques for quantification that rest on human vision. Thus most studies do not take into account reflectance in the ultraviolet (UV) part of the spectrum or fluorescence, both of which

Female Coloration

have proven important in mate choice (Andersson and Amundsen 1997; Johnsen et al. 1998; Arnold et al. 2002). Relatively few studies have focused on structural coloration in females (e.g., see Tables 7.1–7.3). This paucity may be because such colors can be difficult to quantify reliably, especially when they extend into the UV and include varying degrees of glossiness.

A History of Neglect Until about 1990, female coloration was subject to very little scientific interest. By and large, the fact that females could be conspicuously colorful was either not realized, or considered a byproduct of selection on males and thus not very exciting. Although Darwin (1859, 1871) provided excellent guidance for later research on most issues, he may have unwittingly misled twentiethcentury scientists on female ornamentation. Having formulated the theory of sexual selection, Darwin (1871) argued that such selection would typically act on the males, apart from the special case of sex-role reversal. Being the greatest naturalist of all times, Darwin was of course aware that females of both birds and other animals could be brightly colored or otherwise ornamented— sometimes equally gaudy as the males, at other times less so. However, he attributed such cases to “the modes of inheritance.” Selection was on males, Darwin (1871) argued, with the selected male traits being transferred to the females despite having no function in that sex. The fact that male traits were “transferred” to the females in highly variable degrees was—atypically for Darwin—explained by proximate constraints; the laws of inheritance would, for unknown reasons, result in greater or lesser transmission in various species (e.g., see Cronin 1991). Darwin’s view on this issue is essentially the genetic correlation hypothesis of today. After Darwin (1871), research on sexual selection was almost entirely absent for the next century (Cronin 1991). The most notable exception was Fisher (1930), who largely reiterated Darwin’s argument of correlated evolution of female characters in his theoretical models. When sexual selection was “rediscovered” around 1960 (Maynard Smith 1958; O’Donald 1962) and grew into a major focus of evolutionary biology during the following decades, the emphasis was on understanding male appearance (Andersson 1994). It remains an open question whether the neglect of female ornamentation in studies of sexual selection in the 1970s and 1980s can be explained by internal scientific dynamics (the “big issue” of male showiness needed an answer before the “small issue” of female beauty could be tackled), or by the sociology of the scientific

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enterprise (e.g., there being more male than female scientists). The lack of interest in female ornaments, however, was somewhat legitimized by Lande’s (1980, 1987) influential models of genetic correlations in the evolution of sexual dimorphism. As is all too often the case, the nuances in the theoretical works were largely overlooked by empirical scientists, and Lande’s papers were misinterpreted to claim that female ornaments would typically, perhaps always, occur for reasons of genetic correlation. Thus a line of great theoreticians, from Darwin via Fisher to Lande, had in different ways given rise to a general opinion that female showiness served no function. Such conventional thinking may have been facilitated by a human tendency for stereotypic simplifications (Houde 2001), leading to a focus on the “main issue” (male ornamentation) and neglect of the “detail” (female ornamentation). It was not until about 1990, and particularly during the past 10 years, that science took a significant interest in the evolution of female ornamentation. Consequently, the current understanding of the phenomenon remains limited. Patterns and suggestions emerging from the present chapter should thus be treated as tentative rather than conclusive.

Merely a Genetic Correlation? Traditionally, the hypothesis most often invoked to explain female coloration, especially when female coloration is similar to that of the male but less flashy, is that female coloration is the product of a genetic correlation (Lande 1980, 1987; Lande and Arnold 1985; Figure 7.1). Although this hypothesis is true in the narrow sense that the same traits in males and females share a genetic basis, it is an empirical question whether it is also true in the wider sense of explaining intra- and interspecific variation in female conspicuousness. Indeed, it seems likely that the degree to which females of a certain species possess extravagant colors is also affected by selection pressures that either favor a cryptic or a conspicuous appearance (Figure 7.2). Antagonistic selection can occur in the same species, the end result (i.e., expressed coloration) reflecting the balance among various selection pressures. These selection pressures act on a genome in which traits in males and females are, due to their shared genetic basis, often tightly correlated unless some mechanism has evolved to decouple male and female appearance. Although Lande (1980) originally argued that such mechanisms would require a very long time to evolve, recent comparative evidence suggests that changes in the similarity between males and females have occurred frequently in several phylogenetic lineages.

Female Coloration

291

conspicuous

Males

cryptic

Females

a

b

c

d

e

f Figure 7.2. Schematic illustration of possible evolutionary changes in conspicuousness of males and females: (a) sexual selection for conspicuousness in males; (b) predation-generated natural selection for crypsis in males; (c) sexual selection for conspicuousness in females; (d) predation-generated natural selection for crypsis in females; (e) sexual selection for conspicuousness in males and correlated evolution in females, or sexual selection for conspicuousness in both sexes; (f ) predation-generated natural selection for crypsis in females and correlated evolution of males, or predation-generated natural selection for crypsis in both sexes. Modified after Amundsen (2000b).

Price and Birch (1996) provided one of the first studies to suggest that the link between male and female trait expression, including coloration, was evolutionarily quite flexible. They showed that transitions between monomorphism and dimorphism had occurred very frequently among passerines and that dichromatism had been lost more often than it had evolved. Similar patterns

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Euphagus carolinus

E. cyanocephalus

Dives dives Male plumage evolution

Quiscalus mexicanus

Female plumage evolution

Q. niger

Q. quiscula

Iridescent black Non-iridescent black Brown

Figure 7.3. Example of evolutionary changes in female coloration without parallel changes in males. In a clade including shiny blackbirds (Euphagus and Dives) and grackles (Quiscalus), females have twice evolved from a cryptic to a conspicuous plumage. The males of all clades have been conspicuous and have not undergone evolutionary color change during the same period. Redrawn from Irwin (1994).

of more frequent gains than losses of dichromatism have been reported by Peterson (1996) and Omland (1997). Taken together, these studies question the evolutionary inertia caused by genetic correlation (Lande 1980, 1987). Price and Birch (1996) did not quantify trait expression in the two sexes separately and thus could not tell whether changes in dimorphism were due to evolutionary changes in males or in females. Such quantification has been done, however, in phylogenetically based comparative work on New World blackbirds (Irwin 1994; Figure 7.3), tanagers (Burns 1998; see Figure 10.9 in Chapter 10); Plate 20), and Anseriformes (Figuerola and Green 2000). The patterns arising from these studies are remarkably similar: during evolution, male and female coloration has changed largely independently of changes in the opposite sex. Moreover, evolutionary change in coloration has happened more frequently in females than in males, and the majority of changes has been in the direction of more colorful female plumages (e.g. Irwin 1994; Burns 1998; see also Chapter 10). Taken together, the current evidence suggests that selection has acted on male and female traits quite independently. Notably, there is no conflict between genetic correlation and functional female coloration. On the contrary, genetically correlated female colors may serve as the starting

Female Coloration

point for functional female coloration, be it for competition, mate attraction, or other functions. Moreover, because of genetic correlations, male mate choice for colorful females will not only produce colorful daughters, but also colorful, “sexy” sons. Therefore, provided that color is attractive in both sexes, a genetic correlation can actually promote the evolution of functional coloration in both males and females (Amundsen 2000b). The correlated-response idea cannot be tested directly on single species; instead, indirect support for this hypothesis can be obtained if all relevant functional hypotheses are tested and refuted. Although refuting all alternative hypotheses is impossible in a strict Popperian sense, inferences based on such indirect evidence can be informative, provided sufficient effort has been spent on testing alternative, functional explanations. The genetic correlation idea has most frequently been advocated in cases in which females are similar to males but paler in color. This practice makes some sense, because transitional forms would be expected if current selection favors a drab female appearance but the ancestral state is conspicuous. At the same time, a similar-to-male but weaker female coloration can result, for instance, from equally strong sexual selection on the two sexes but stronger predation-induced selection for crypsis in females (e.g., see Wallace 1889, 1891; Martin and Badyaev 1996). Thus the mere fact that females are less colorful than males in many species is not evidence against a selective advantage of female coloration. If selection favors different trait expression in the two sexes, antagonistic selection may constrain evolution in both sexes. In Zebra Finches (Taeniopygia guttata; Plate 18), in which females prefer red bills in males but males prefer orange bills in females, the genetic correlation for bill color (Price and Burley 1993) constrains the evolution of red male bills (and orange female bills; Price and Burley 1994). When males and females carry different colors, or coloration on different body parts, the explanation can hardly be genetic correlation (e.g., see Amundsen and Forsgren 2001; Heinsohn et al. 2005). Species displaying conspicuous but different coloration in the two sexes are therefore particularly interesting candidates for selection on females. At the same time, such species are few among birds, and their study cannot provide the evidence needed to broadly understand color evolution among female birds. Ultimately, the understanding of female colors as they occur in numerous bird species will rest on the degree to which researchers understand how genetic correlations and selection on females interact to shape their appearance.

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Indicators of Quality? Quality is a rather vague and nonoperational term (Pirsig 1974), yet the concepts of phenotypic and genetic quality are crucial to evolutionary theory. Operationally, quality is perhaps best approximated by condition in the very general sense of having a high capacity, as determined by genes and environment (Rowe and Houle 1996; Tomkins et al. 2004; see Chapter 6). During recent decades, studies of male birds (and other animals) have revealed that colors often act as indicators, telling about some quality of the bearer (e.g., Andersson 1994; Sheldon 2000b; Chapter 12, Volume 1; Chapter 6). Potentially, female colors or other ornaments could be similarly related to individual quality (Amundsen 2000b; Figure 7.4), either because they have been selected as signals in themselves or because condition dependence itself may be subject to intersexual genetic correlation (e.g., see Bonduriansky and Rowe 2005). Thus a link between female color and quality does not provide proof of selection acting directly on the female trait (Amundsen 2000c). Even if the initial correlation between color and quality was a byproduct of selection on males, however, it could serve as a starting point for selection on female coloration that could help maintain, strengthen, and possibly modify the indicator value of female coloration in competition and mate attraction (Amundsen 2000b). It has been suggested that signals should be designed to somehow reflect the information they convey. Because essential qualities may differ between males and females, one might expect the color signals of the sexes to be different (e.g., see Roulin et al. 2001a). Such a difference in coloration appears to be rare (see above). Whether the rarity of cases in which both sexes are colorful but differently so implies that color signals reflect very general qualities (condition in a wide sense) or rather reflect constraints imposed by genetic correlation (Roulin et al. 2001a) remains to be determined. Different colors have been suggested to reflect different qualities (see McGraw et al. 2002; Senar et al. 2003; Chapter 12, Volume 1). For instance, carotenoids have been assumed to be costly and therefore good candidates for honest signaling in mate choice (e.g., Olson and Owens 1998; Hill 2000). By contrast, melanin pigments have been thought to be energetically cheap to produce. Maynard Smith and Harper (1988, 2003) and McGraw and Hill (2000) have suggested that melanins should therefore be used in badges of status, because the costs of cheating are imposed socially. Although some data on males support these general statements, knowledge of the costs of various col-

Female Coloration

295

Size Immunocompetence Adult viability

Age

Female quality Reproductive success

Body condition Maternal care Offspring viability

Figure 7.4. Aspects of female quality that may be related to female coloration in birds.

ors is still scant and the evidence complex (McGraw et al. 2002; Jawor and Breitwisch 2003a). Many male ornamental traits, including colors, have been shown to be condition-dependent (Andersson 1994; Sheldon 2000b; Chapter 12, Volume 1; Chapter 6). In a simplistic correlated-response model of female coloration, one might expect females to inherit the color but not the condition from the males. However, if there is a genetic basis for and a developmental mechanism linking condition to color, this mechanism should typically be present in females as well. Thus relationships between color and condition in females may either be due to signal selection in males, in females, or both (e.g., see Cotton et al. 2004; Bonduriansky and Rowe 2005). Age Avian coloration is often a reliable signal of age, a very important aspect of quality that may relate to acquired experience, dominance, or other fitnessenhancing factors. The relationship is particularly clear for species with delayed plumage maturation, in which younger but sexually mature individuals look distinctly different from individuals in definitive breeding plumage. Delayed plumage maturation has been primarily studied in males (e.g., Lyon and Montgomerie 1986; Hill 1996) but also occurs among females of at least some species (e.g., Stutchbury and Robertson 1987b; Thompson and Leu 1995). More commonly, age may relate to subtle differences in color among mature individuals (Table 7.1). For instance, 1-year-old Bluethroat females are overall less colorful than older ones (T. Amundsen et al., unpubl. data), but there is much overlap in coloration between the two age classes. Notably, two studies based on more limited samples have provided contradictory results (one positive [Rohde et al. 1999] and one negative [Amundsen et al. 1997]), suggesting that statements on age-color relationships based on small samples should be treated with caution. Similar patterns are found in many

Table 7.1. Studies Testing for a Relationship between Female Coloration and Some Aspect of Female Quality Plumage part

Similarity to malea

Color

Color typeb

Eye, postocular stripe Pectoral band, spots Curled feathers Chest band

I

Yellow

P,(C)

I

Black

M

I

Black

M

I

Rusty-red

M

Wing patch

SW

White

M

Rump, tail

SW

Gray

(M)

Comb

SW

Red

I,C

+

Head, back

SS

(M)

0

Breast

SW

Rusty-red, brown Rusty-red

Body

I

Brown, light

(M)

Moustache, wattles Head plumes, bill Adbominal patch Underside spottiness

I

White, yellow

O,(C)

I

M,(C)

SW

White, black, red Red

SS

Black

M

Tawny Owl (Strix aluco) Tree Swallow (Tachycineta bicolor)

Head, body

I

M

Upperparts

SW

Reddish brown to gray Brown-blue

M,(S)

Pied Flycatcher (Ficedula hypoleuca) Bluethroat (Luscinia svecica)

Forehead patch Throat patch

SW

white

M

SW

Blue, rufous, black

M,S

Cedar Waxwing (Bombycilla cedrorum) Great Tit (Parus major)

Waxlike wing patches Breast, breast band

I

Red

C

SW

Yellow, black

C,M

Species Coloration Yellow-eyed Penguin (Megadyptes antipodes) Magellanic Penguin (Spheniscus magellanicus) Black Swan (Cygnus atratus) Common Shelduck (Tadorna tadorna) Common Goldeneye (Bucephala clangula) Lesser Kestrel (Falco naumanni) Domestic Chicken/ Red Junglefowl (Gallus gallus) Red-necked Phalarope (Phalaropus lobatus) Bar-tailed Godwit (Limosa lapponica) Parasitic Jaeger (Stercorarius parasiticus) Inca Tern (Larosterna inca) Least Auklet (Aethia pusilla) Burrowing Parrot (Cyanoliseus patagonus) Barn Owl (Tyto alba)

Size

M

0

Pf

+

Condition

Age

+

+

Para/ Immuc

Reproductive success

Maternal care

Adult survival

Offspring quality

+ 0

Massaro et al. (2003)

0

0

(0) (+) (+) +

0

Tella et al. (1997)

+

Zuk et al. (1998); Pizzari et al. (2003)

0

Reynolds (1987)

+

0

0

0

+

+

+

+

0

0

0 +

0

0 +

0

+

+

+ +

+

+

(+)

0

+

0

+

0

+/0

0

+

(+) (+)

Ferns and Lang (2003) Ruusila et al. (2001)

0

+

0/+

Forero et al. (2001) Kraaijeveld et al. (2004)

(+)

0

Reference

0

0

+

Piersma and Jukema (1993); Piersma et al. (2001a,b) Phillips and Furness (1998) Velando et al. (2001) Jones (1990); Jones and Montgomerie (1992) Masello and Quillfeldt (2003) Roulin et al. (2000, 2001a,b, 2003a); Roulin (2003); Roulin and Dijkstra (2003) Roulin et al. (2003b) Stutchbury and Robertson (1987a); Lozano and Handford (1995) Potti (1993); Potti and Merino (1996) Amundsen et al. (1997); Rohde et al. (1999); Smiseth and Amundsen (2000); T. Amundsen et al. (unpubl. data) Mountjoy and Robertson (1988) Horak et al. (2001); Senar et al. (2003)

Table 7.1. (continued) Species Blue Tit (Cyanistes caeruleus) Black-billed Magpie (Pica pica) Pinyon Jay (Gymnorhinus cyanocephalus) Rock Petronia (Petronia petronia) European Starling (Sturnus vulgaris) Eastern Bluebird (Sialia sialis) Zebra Finch (Taeniopygia guttata)

Plumage part

Similarity to malea

Color

Color typeb

Size

Breast

I/SW

Yellow

C

0

Tail

SW

Shiny blackish

O,(S)

Malar feathers

SW

Bluish

(S)

Breast patch

I

Yellow

(C)

+

Throat

SW

M,S

0

Breast, rump, tail Bill

SW

“Dark,” gray, iridescent Blue, chestnut

M,S

SW

Orange-red

C

House Finch (Carpodacus mexicanus) White-throated Sparrow (Zonotrichia albicollis)

Under-side, head, rump Head

SW

Red

C

I

White/black/ brown

M

Northern Cardinal (Cardinalis cardinalis) Red-winged Blackbird (Agelaius phoeniceus)

Underwing, body Epaulet

SW

Red

C

SW

Pale yellow to orange

M,C

Tail streamers

SW

Red

(C)

Crest

I

Black

O,(M)

Crest/head plumes Tail length

I

Black/white

O,(M)

Tail length

SW

Other ornamental traits Red-tailed Tropicbird (Phaethon rubricauda) European Shag (Phalacrocorax aristotelis) Crested Auklet (Aethia cristatella) Scissor-tailed Flycatcher (Tyrannus forficatus) Barn Swallow (Hirundo rustica)

SW

O,(M) Black

O,(M)

Notes: +, Positive relationship; 0, no relationship; –, negative relationship. Parentheses indicate less conclusive evidence. a. Similarity to male: I, Indistinguishable; SW, similar but weaker ornament expression; SS, similar but stronger ornament expression. b. C, carotenoid-based coloration; I, integument; M, melanin-based; O, ornamental feather structure (e.g., tail, crest); P, pterin-based; Pf, psittacofulvin based; S, structural. Judged mainly from visual appearance. c. Para/Immu, parasites and immunity.

Female Coloration

Condition

Age

Para/ Immuc

299

Reproductive success

Maternal care

Adult survival

Offspring quality 0

0

0 +

+

+

+

(+)

0

0

Komdeur et al. (2005)

0

+

+

+

Siefferman and Hill (2005) Burley (1986); Burley et al. (1991, 1992); Price and Burley (1994) Hill (1993a,b)

0

Knapton and Falls (1983); Knapton et al. (1984); Kopachena and Falls (1993b) Linville et al. (1998)

–

–

–

0

0

0

0 +

+

0

0

+

+/0

Muma and Weatherhead (1989); Johnsen et al. (1996) 0

0 (+)

Andersson et al. (1998); Senar et al. (2002) Blanco and De la Puente (2002) Johnson (1988) Pilastro et al. (2003)

–

0

Reference

+

Daunt et al. (2003)

+

0

+ +

Jones et al. (2000, 2004)

(+) 0

+/0

Veit and Jones (2003)

0

0

Regosin and Pruett-Jones (2001) Møller (1993, 1994); Cuervo et al. (1996); Saino et al. (1997); Safran and McGraw (2004)

species, with color sometimes being a strong predictor of age. Examples include Yellow-eyed Penguins (Megadyptes antipodes; Massaro et al. 2003), Least Auklets (Jones 1990; Jones and Montgomerie 1992), Lesser Kestrels (Falco naumanni; Tella et al. 1997), Pinyon Jays (Gymnorhinus cyanocephalus; Johnson 1988), Cedar Waxwings (Bombycilla cedrorum; Mountjoy and Robertson

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1988), and Red-winged Blackbirds (Agelaius phoeniceus; Plate 11; Muma and Weatherhead 1989; Johnsen et al. 1996). However, the correlation between female color and age is not ubiquitous: no such relationship was found when tested for in Northern Cardinals (Linville et al. 1998; Table 7.1). House Finches represent a notable exception to the general pattern of increasing brightness with age, with yearling females on average being more colorful than older ones (Hill 1993a). Body Size In some species, including Bluethroats (Amundsen et al. 1997) and Rock Petronias (Pilastro et al. 2003), female coloration appears related to structural body size (Table 7.1). Size may be particularly important for females of species with physical female-female conflict, such as Eurasian Dotterels (Owens et al. 1994) and Capuchinbirds (Perissocephalus tricolor; Trail 1990). Body Condition Body condition is typically defined operationally as residuals from a body mass versus skeletal size regression (or by similar indices). In essence, this measure reflects nutritional status, which can be very important for any energy-demanding activity, including territorial defense, egg production, incubation, and feeding and defense of dependent offspring. Studies of several species have reported positive correlations between female color and body condition (Table 7.1). Examples include Yellow-eyed Penguins (Massaro et al. 2003), Bar-tailed Godwits (Limosa lapponica; Piersma and Jukema 1993), Inca Terns (Velando et al. 2001), Least Auklets (Jones 1990), Tree Swallows (Tachycineta bicolor; Plate 27; Lozano and Handford 1995) and Rock Petronias (Pilastro et al. 2003). However, there are also a number of species for which no such relationship has been found, including Lesser Kestrels (Tella et al. 1997), Black-billed Magpies (Pica pica; Blanco and De la Puente 2002), and House Finches (Hill 1993a). Interestingly, Senar et al. (2003) found a positive relationship, which seemed unaffected by sex, between carotenoid-based yellow breast and tail growth in Great Tits (Parus major; Plate 11). They did not find a similar effect of the melanin-based breast stripe. In summary, even though female coloration in many species is condition-dependent, this appears not to be universally true. The reasons for such interspecific variability are un-

Female Coloration

clear, but it is noteworthy that melanin-based colors in several species appear to be condition-dependent (Table 7.1). One particularly strong approach to studying condition dependence of coloration is experimental manipulation of nutrition. Adopting this technique, Hill (2002) showed that food stress negatively affected the yellow-orange plumage color of female House Finches. In a recent study, Siefferman and Hill (2005) found that nutritional stress affects structural but not melanin-based coloration in female Eastern Bluebirds (Sialia sialis; Plate 32, Volume 1). Immunocompetence The ability to withstand parasites (from viruses to insects) is of major importance for fitness. Studies aiming to test whether colors are signals of immune capacity (Hamilton and Zuk 1982; Folstad and Karter 1992) have related color either to parasite load or to responses from immune-challenge techniques (Westneat and Birkhead 1988; Norris and Evans 2000). In some species, negative relationships between female color and parasite infections have been found. Examples include tapeworms (cestodes) in Bar-tailed Godwits (Piersma et al. 2001b), trypanosomes in Pied Flycatchers (Ficedula hypoleuca; Plate 18; Potti and Merino 1996), and blood parasites in Great Tits (Horak et al. 2001). However, such results can be explained not only by variation in parasite resistance but also by variation in parasite exposure. Therefore correlational studies do not provide conclusive evidence that female color reflects quality in the form of immunocompetence. Experimental infections of female House Finches with coccidia suggest that such parasites inhibit carotenoid-based coloration (Hill 2002). Similarly, females with more mites in Blue Tits (Cyanistes caeruleus; Plate 18), Great Tits, and Eurasian Greenfinches (Carduelis chloris) grew duller plumages after molt (Harper 1999). Immune responses in offspring have been related to maternal color in two species. The strongest evidence is for Barn Owls (Tyto alba; Plate 29, Volume 1), in which nestling antibody response was related to spottiness of the genetic mother (Roulin et al. 2000; Figure 7.5). By cross-fostering young, Roulin et al. (2000) removed confounding environmental effects (but not any maternal egg quality effect), a technique he also used to document other indices of high immunocompetence among offspring of highly spotted females (Roulin et al. 2001b). In Inca Terns, offspring of females with long white head plumes showed a stronger cell-mediated immune response (Velando et al. 2001) than

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302

Residual anti-SRBC titer

0.4

0.2

0

–0.2

–0.4 0

1

2

3

Plumage spottiness of genetic mother

Figure 7.5. Immune response (production of antibodies to sheep red blood cells, or SRBC) of Barn Owl nestlings in relation to spottiness of their genetic mother. The nestlings were cross-fostered to avoid the confounding effect of maternal care, and residual immune response was calculated after controlling for the pair of cross-foster nests, rearing environment, and age of nestlings. Redrawn from Roulin et al. (2000).

did those of short-plumed mothers. In Bluethroats, neither structural nor melanin throat ornamentation was related to cell-mediated immune response in adult females (Pärn et al. 2005). To our knowledge, this is the only study that has reported immune challenge responses in relation to color in adult females. We strongly encourage studies using immune-challenge techniques to test immune responses in females and their offspring relative to color. To establish a general understanding of how female colors among birds relate to immunocompetence, measures of immune response that are unaffected by current parasite load are needed. Most of the current evidence (Table 7.1), based on observed correlations between trait expression and parasite load, is only suggestive in this context. Maternal Care If female coloration reflects some basic quality or condition of the individual, one might expect a positive relationship between color and resources provided to the offspring. Accordingly, if males prefer colorful females, a high-quality mother could be an important benefit of choice (the “good parent process,”

Female Coloration

Hoelzer 1989). Such direct benefits may often be more important in sexual selection than indirect, genetic benefits (Kirkpatrick and Barton 1997). Parental care includes a series of important activities, all of which may potentially relate to coloration: nest construction, incubation, brooding, nestling feeding, and feeding and defense of young that have left the nest (either as altricial fledglings or right after hatching among precocial birds; Clutton-Brock 1991). In light of the common nature of maternal care in birds, including feeding and defense of offspring, it is surprising that few studies have related levels of female care to female coloration. The studies that exist have focused on nestling feeding and have provided equivocal results. The first study to report a positive relationship between female color and parental care was on Northern Cardinals, in which Linville and co-workers (1998) found that both the female proportion of all feeds and the number of feeds per nestling correlated positively with carotenoid-based reddish female under-wing color. However, under-wing color was not correlated with the total feeding rate to each brood, and female body color was not correlated with any measure of female care (Linville et al. 1998), rendering the overall relationship somewhat unclear. Moreover, because female care is typically inversely related to male care and brood size affects parental effort, observations of females tending variable brood sizes together with males are inherently confounded by male and brood size effects and are thus not conclusive. This limitation also applied to studies of House Finches (Hill 2002) and Bluethroats (Rohde et al. 1999), which reported no relationship between female coloration and parental care. To circumvent this problem, Smiseth and Amundsen (2000) removed the male temporarily in Bluethroats and recorded female feeding rate to broods of a standardized size. This study confirmed the lack of a relationship between female color and level of care in Bluethroats (Smiseth and Amundsen 2000). Due to the few studies conducted (Table 7.1) and the difficulties outlined above, very little is currently known about how female color relates to maternal care. Far more studies are needed, not only in relation to nestling feeding, but also to incubation, brooding, and offspring defense. Reproductive Success Several studies have related female coloration to female reproductive success (Table 7.1), typically measured as numbers of or body masses of fledged offspring. With reproductive success being a principal component of fitness, any relationship with female coloration may have evolutionary significance. For

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instance, successful breeders among Inca Terns had longer white head plumes than less successful breeders, and chicks of long-plumed mothers were also heavier and in better condition (Velando et al. 2001). Similarly, Yellow-eyed Penguin females with yellower eyes had higher reproductive success (Massaro et al. 2003), and Burrowing Parrot (Cyanoliseus patagonus; Plate 16) females with large red abdominal patches produced heavier offspring (Masello and Quillfeldt 2003). Notably, neither the yellow eyes of the Yellow-eyed Penguin (Chapter 8, Volume 1) nor the redness of Burrowing Parrot feathers (Masello et al. 2004) is due to carotenoids (Chapter 8, Volume 1). In the polyandrous Red-necked Phalarope, maternal coloration was unrelated to the fate of nests (Reynolds 1987). Fitzpatrick and co-workers (1995) have pointed out that females more than males have to trade off limited resources between fecundity and sexual ornamentation and have suggested that this may constrain the evolution of showiness in females. The consequences of such trade-offs for the evolution of female ornamentation, including coloration, remain to be explored. Adult Survival An essential assumption of sexual selection theory (Andersson 1994; Andersson and Iwasa 1996) is that secondary sexual traits result in a survival cost. At the same time, honest signaling theory posits that only individuals of a high quality can afford the more costly and extravagant ornament expressions (Zahavi 1975; Grafen 1990). In sum, it is less than trivial whether coloration should be positively or negatively related to survival. Theoretically, all forms of relationship are possible (Kokko et al. 2002). We are only aware of a few species in which tests for relationships between female coloration and adult survival have been made. For most of these species, no relationship was found: Least Auklets (Jones and Montgomerie 1992), Lesser Kestrels (Tella et al. 1997), Tawny Owls (Strix aluco; Roulin et al. 2003b), and House Finches (Hill 1993a). Only in Great Tits has a positive relationship been reported (Horak et al. 2001). In captive Zebra Finches, female bill redness was negatively related to survival, suggesting a net cost of coloration (Price and Burley 1994). In summary, the current evidence is mainly negative and suggests that female survival is only rarely related to coloration. In future studies, variation in female coloration across years will need to be considered. Accordingly, it may be meaningless to relate survival over many years to female color in one year. Instead, one should either relate annual survival to color expression in the

Female Coloration

preceding breeding season or long-term survival to mean female coloration across years. Offspring Quality If female colors reflect either phenotypic or genetic quality, a direct or indirect effect on the quality of offspring would be expected. Such qualities could include fledging body size, parasite resistance, survival, or fecundity of the offspring. However, few studies have investigated any of these parameters in relation to female colors. The strongest evidence that colorful females produce better offspring comes from the studies of immune capacity and parasite resistance in Barn Owls (see the discussion of immunocompetence above). Strong evidence for a relationship also exists for female color versus reproductive success in some species (see the discussion of reproductive success above). In Eastern Bluebirds, more colorful females produced offspring in better condition (Siefferman and Hill 2005), whereas in Bluethroats, two studies found no relationship between female coloration and brood mass (Rohde 1999; Smiseth and Amundsen 2000). However, studies of overall reproductive success or nestling quality are sensitive to confounding factors, including the quality of the male mate.

Female Colors: Signals of Status? During the past few decades, it has become clear that female birds can be far more competitive than previously thought (e.g., Petrie 1983; Slagsvold et al. 1992; Sandell and Smith 1997; Langmore 1998, 2000; Sandell 1998). For instance, it is now recognized that females of several bird species vocalize or “sing” in competitive contexts, either to defend a nonsexual resource or a mating partner (Cooney and Cockburn 1995; Langmore 1998, 2000; Sæther 2002). Despite the well-established status signaling function of color in male birds (Rohwer 1975; see Chapter 3), however, it is less clear whether females use visual displays, including colors, in such contexts (Amundsen 2000b). One of the first researchers to suggest that female conspicuous traits, including colors, could serve a competitive function was West-Eberhard (1979, 1983). She argued that, in species living in social groups, coloration could serve as a status signal, effectively reducing aggressive interactions over resources and thus promoting social stability. Focusing mainly on nonsexual resources, West-Eberhard termed this process “social selection,” which she considered a

305

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306

Female status signaling

Versus females in contests over:

Versus males in contests over:

Sexual Nonsexual resources resources (e.g., mates) (e.g., food)

Nonsexual resources (e.g., food)

Sexual selection Natural selection Social selection

Signal selection

Figure 7.6. Potential contexts in which female colors may be used to signal competitive status and the kinds of selection implied. The term “social selection” to cover all competitive contexts was suggested by West-Eberhard (1979, 1983), and the term “signal selection” by Zahavi (1987).

broader class of selection encompassing sexual selection (Figure 7.6). She argued that this process could explain coloration in, for instance, toucans and parrots. Distinguishing whether the contest is over mates or other resources is important because competition in relation to sexual resources would imply sexual selection (Andersson 1994), while competition in other contexts would imply natural selection (Figure 7.6). Note, however, that the distinction is less fundamental if, instead of a sexual/natural selection dichotomy (Darwin 1871; Andersson 1994), one adopts a signal/nonsignal selection approach (Zahavi 1987; Johnstone 1997). Then, all nonutilitarian (Zahavi 1987) colors would be subject to fundamentally the same sort of selection for efficient and, in most cases, reliable communication (Johnstone 1997). Colors could act as status signals in nonsexual competition not only with other females, but also with males (Figure 7.6). Female-Female Competition over Food Perhaps the strongest evidence that female colors affect dominance comes from a study of European Starlings (Sturnus vulgaris; Plate 23, Volume 1), in which the degree of chest spottiness was related to dominance both among naturally colored females and when spottiness was experimentally manipulated

Female Coloration

(Swaddle and Witter 1995). At the same time, it is probably the least extravagant form of female coloration in any of the species studied with respect to dominance (Table 7.2). Nonetheless, white-spottiness of female starlings appears to be related to individual quality, because more spotted females seem to start breeding earlier (Swaddle and Witter 1995). In contrast to what was observed for starlings, no relationship was found between carotenoid- and melanin-based epaulet color and dominance or aggression among female Redwinged Blackbirds (Muma and Weatherhead 1989, 1991). However, manipulation of plumage (e.g., darkening of hood, addition of white tail feathers) in female Dark-eyed Juncos (Junco hyemalis) that had previously been subdominant resulted in reversal of dominance, strongly suggesting a status signaling function of either head blackness, tail whiteness, or both (Holberton et al. 1989). Many of the passerine species that have been subject to tests of the statussignaling hypothesis live in mixed-sex flocks outside the breeding season. Several studies of such flocks have been performed, typically recording both intraand intersexual interactions. These studies have provided mixed results in regard to the relationship between female coloration and intrasexual dominance rank. One study of Harris’ Sparrows (Zonotrichia querula) suggested that female blackness is positively related to dominance rank (Watt 1986), whereas another study in this species found no such relationship (Jackson et al. 1988). In the White-throated Sparrow (Z. albicollis), both males and females appear in two morphs: tan striped and white striped. Ficken and co-workers (1978) found the whiter morph to more often be the aggressor in conflicts during spring migration, whereas previous work has suggested that tan-striped individuals are dominant in winter flocks (Watt et al. 1984). Other work on the species suggests a function of female color in competition for attractive mates (see below). However, in the closely related and morphologically very similar White-crowned Sparrow (Z. leucophrys), crown coloration has been reported not to affect winter dominance in either sex (unpubl. data cited in Fugle and Rothstein 1985). Similarly, winter dominance status in captive all-female flocks of House Finches was unrelated to female carotenoid-based coloration (Hill 2002). In Great Tits, the black breast stripe is weakly positively related to dominance in females (Wilson 1992), whereas no relationship between female comb size and dominance was found during feeding competition among Red Junglefowl (Gallus gallus; Zuk et al. 1998). In hummingbirds (Trochilidae), females are either partly or wholly responsible for territory defense. Hummingbird territories are mainly for feeding,

307

Conspicuous coloration Red Junglefowl (Gallus gallus) Eurasian Dotterel (Charadrius morinellus) Least Auklet (Aethia pusilla) Purple-throated Carib (Eulampis jugularis) Tourmaline Sunangel (Heliangelus exortis) Amethyst-throated Sunangel (H. amethysticollis) Sunangels spp. (Heliangelus spp.) Capuchinbird (Perissocephalus tricolor) Tree Swallow (Tachycineta bicolor) Bluethroat (Luscinia svecica) Great Tit (Parus major) Pinyon Jay (Gymnorhinus cyanocephalus)

Species SW SS I I SW SW SW I SW SW SW SW

Belly, cap, breast

Underparts

Throat, breast

Throat

Throat

Throat

Head, wing, tail

Upper parts

Throat patch

Breast stripe

Throat patch, malar feathers, head

Similarity to malea

Comb

Body part

Gray-blue

Naked bluegray, black Brown-blue, blue Blue, chestnut, black Black

Glittering rosy

Glittering rosy

Glittering rosy

Purple

Black, chestnut White-black

Red

Color

(S)

M

S,M

M,(S)

(I),M

(S)

(S)

(S)

(S)

M

M

I,C

Color typeb

+

(+)/0

(+)

(+)

(+)

+

Sexual competition

+

0/(+)

(+)

(+)

(+)

(+)

0

Nonsexual competition

Johnson (1988)

Stutchbury and Robertson (1987a,b) T. Amundsen et al. (unpubl. data) Wilson (1992)

Trail (1990)

Bleiweiss (1992b)

Bleiweiss (1992a)

Bleiweiss (1985)

Wolf (1969)

Jones (1990)

Owens et al. (1994)

Zuk et al. (1998)

Reference

Table 7.2. Studies Testing for a Function of Female Ornamentation in Female-Female Competition in Relation to Mates or Other Resources

Forehead crest

Bill, underwing, face Epaulette, chin

M

SW

SW

Black

White, browngray, white Red-orange, red, blackish Pale yelloworange, pale yellowyellowish pink

SW

I

Head

White, black, brown White, black, gray

Black

SW

Head

Black

White spots

I/SW

SW

Crown, throat

Crown, throat, breast Body, tail

D

Chest

O

C

C,M

M

M/S

M,(S)

M

M,S

+

(+)

0/0/+

(+)

0

+

0

+

(+)/0

(+)/(–)

(+)

Jones and Hunter (1999)

Muma and Weatherhead (1989, 1991)

Fugle and Rothstein (1985) Ficken et al. (1978); Watt et al. (1984); Kopachena and Falls (1993a); Houtman and Falls (1994) Watt (1986); Jackson et al. (1988) Holberton et al. (1989) Jawor et al. (2004)

Swaddle and Witter (1995) Stutchbury (1994)

Notes: +, Positive relationship; 0, no relationship; –, negative relationship. Parentheses indicate less conclusive evidence. a. Similarity to male: I, indistinguishable; SW, similar but weaker ornament expression; SS, similar but stronger ornament expression. b. C, carotenoid-based coloration; I, integument; M, melanin-based; O, ornamental feather structure (e.g., tail, crest); P, pterin-based; Pf, psittacofulvin-based; S, structural. Judged mainly from visual appearance.

Other conspicuous plumage traits Crested Auklet (Aethia cristatella)

Harris’ Sparrow (Z. querula) Dark-eyed Junco (Junco hyemalis) Northern Cardinal (Cardinalis cardinalis) Red-winged Blackbird (Agelaius phoeniceus)

European Starling (Sturnus vulgaris) Hooded Warbler (Wilsonia citrina) White-crowned Sparrow (Zonotrichia leucophrys) White-throated Sparrow (Z. albicollis)

310

trond amundsen & henrik pärn and territoriality can be displayed outside as well as within the breeding season. Although hummingbirds as a family display an enormous variety of flashy colors and appendages, mainly in males, females are also quite colorful in a number of species (e.g., Bleiweiss 1992b). Such coloration seems to coincide with territorial defense (Wolf 1969; Bleiweiss 1985, 1992a,b). In sunangel hummingbirds (Heliangelus spp.), females often have conspicuous colors that have been hypothesized to function in territorial defense (Bleiweiss 1992b). However, no direct test relating female hummingbird coloration to social dominance (or correlates thereof, e.g., territory size) has yet been performed. Female-Female Competition for Mates Few studies have specifically tested whether female coloration affects dominance in direct competition for mates (see Table 7.2). Most likely, the scarcity of such studies reflects the commonly held view that females normally do not compete for mates (“conventional sex roles”; see below). However, females of many species with conventional sex roles have been shown to compete in a mating context. One example is competition among females to monopolize male care by preventing secondary matings, for instance in European Starlings (e.g., Sandell 1998) and Pied Flycatchers (Slagsvold et al. 1992). In most such instances, it is entirely unknown if color signaling is involved in the competition. In the sex-role reversed Eurasian Dotterel (Plate 20), however, more colorful females spent more time fighting, courting males, and patrolling the edge of the mating arena (Owens et al. 1994). Dotterel plumage is mainly rufous and blackish, suggesting a melanic basis (Chapter 6, Volume 1). Female Eurasian Dotterels often fight during courtship, with courting individuals being attacked by other females. Colorful females both initiated and won such fights more often than did drab ones (Figure 7.7). As pointed out by Owens et al. (1994), only if females can repel same-sex competitors in such fights can they be successful in courtship. Overall, this study provides compelling evidence that color relates to dominance in dotterel mating contests. However, the lack of experimentation makes it as yet unclear whether the relationship between color and dominance was causal or a correlated effect of other qualities reflected in coloration. Somewhat similar to dotterels, female Capuchinbirds visit leks in groups, and courtship is frequently terminated by femalefemale interference, often in the form of threat displays (Trail 1990). Trail (1990) suggested that such female-female competition could balance malemale competition and thus account for sexual monomorphism in the species

Female Coloration

311

Proportion of fights won

1

0 brighter

same color

duller

Plumage of opponent

Figure 7.7. Success in female-female conflicts (proportion of fights won) in Eurasian Dotterels when the opponent is brighter, of the same color, or duller. Redrawn from Owens et al. (1994).

(both males and females displaying long tails and crests), and possibly also in other lekking birds. Another line of evidence comes from colonial seabirds. Both Least (Jones 1990) and Crested Auklet (Jones and Hunter 1999) females frequently engage in disputes with consexuals (and heterosexuals) at or near mating arenas in the colonies. Studying Least Auklets, Jones (1990) recorded natural encounters and responses to models in relation to plumage (blackness of chest; Plate 12) and found that lighter plumaged birds won more natural conflicts and behaved more boldly toward models (Jones 1990). However, he was unable to sex most individuals observed, so it is unclear to what extent these findings have a bearing on female mating competition. Least Auklets can fight over access to mates or nest sites (Jones 1990); only the former would count as mating competition unless nest site occupancy affects attractiveness. In Crested Auklets, in which both sexes possess a highly conspicuous yet individually variable black forehead crest, naturally long-crested individuals won against same-sex shorter-crested individuals both among males and females ( Jones and Hunter 1999). Fights also occurred between males and females, and in such cases, males tended to win even when they had shorter crests ( Jones and Hunter 1999). Taken together, the auklet evidence suggests that ornamentation,

312

trond amundsen & henrik pärn including coloration, may relate to dominance in females as well as males, but the functions of competitive interactions are not well understood. In Pinyon Jays, females vary in the degree of bluish male-like coloration of the malar feathers. Females compete for food, nest sites, and access to males ( Johnson 1988). In aviary trials, female competition was most pronounced in the presence of a male and stronger if the male was high quality. Females competed for the male’s attention by calling to him and attempting to feed him in the presence of the other female. Female competition was related to brightness of the malar feathers ( Johnson 1988). In White-throated Sparrows, the white-striped morph was competitively superior to the tan-striped morph in both sexes but was less attractive in female choice (Houtman and Falls 1994). Houtman and Falls (1994) have suggested that white-striped females may outcompete tan-striped ones for access to white-striped males, but provide no direct evidence for this suggestion. Playback experiments conducted in breeding territories also showed that white-striped females were more aggressive (Kopachena and Falls 1993b). Observations of Scarlet-tufted Malachite Sunbirds (Nectarinia johnstoni; Evans and Barnard 1995) and Bluethroats (H. Pärn et al., unpubl. data; see Langmore 2000) have revealed that coloration is often displayed in conflicts between resident and intruder females, possibly over mating with the territorial male. Female Status Signaling: Common or Rare? Amundsen (2000b) emphasized the need for more studies addressing the possible function of female ornaments (including colors) in female-female competition. Still, relatively few studies have critically tested whether female colors relate to intrasexual dominance, and even fewer have adopted the experimental approach that is required for conclusive statements on causality. The paucity of studies designed specifically to test the role of color in female dominance makes it hard to generalize as to whether female-female competition is a primary determinant of female coloration. Berglund and co-workers (1996) have suggested that many display traits are or have been (over evolutionary time) used both in competition and for mate attraction, but that the initial selection has typically been for a competitive function. This thesis somewhat conflicts with the view that badges of status should be cheap (Maynard Smith and Harper 1988) but ornaments for attraction costly (Zahavi 1975; Grafen 1990).

Female Coloration

Female Colors: Attractive to Males? Sexual selection is now well established as perhaps the most important process leading to extravagant colors among male birds (e.g., Andersson 1994, Chapter 4). Male competition for access to female sexual partners selects for qualities that make males successful in intrasexual contest, but also for traits that make them attractive to females, such as conspicuous colors (Andersson 1994). Similarly, female colors may be attractive to males and may have been selected for that reason. That males are normally the more competitive sex by no means precludes females from competing, nor does choosiness in one sex preclude choosiness in the other. Under certain conditions, mutual sexual selection, with both sexes being similarly competitive and similarly choosy, should be expected. This situation is, however, apparently not the norm (Kokko and Johnstone 2002), at least not among the rather limited set of species so far studied in the context of sexual selection. Nonetheless, even if males of many species should mainly be selected for maximizing the number of female sexual partners, they should sometimes be concerned with the quality of their partner (Parker 1983; Owens and Thompson 1994). The quality of a female partner can have a great impact on male reproductive success, for instance, in bi-parental monogamous species. It is poorly known whether such benefits of choice often outweigh the costs of choice among male birds, and thus whether male choice is common or rare in nature. Below, we summarize the current empirical evidence relating to male choice for female coloration in birds (Figure 7.8). Indirect Tests of Mating Preference One early approach in studies of male choice for female ornamentation was to test whether more ornamented females bred earlier (Møller 1993, 1994; Tella et al. 1997). A much larger number of studies has tested whether males and females mate assortatively with respect to coloration (Table 7.3). A majority of the latter studies has provided evidence of positive assortative mating. Early breeding and assortative mating are consistent with the hypothesis of male mate choice for extravagant ornamentation (coloration). However, both early breeding and assortative mating can occur for a number of reasons. Therefore neither type of data constitutes strong evidence for male (or female) mate choice in relation to coloration (Figure 7.8).

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314

a

Inferential value of approaches Timing of pairing or egg-laying

Differential allocation by males

Assortative mating

Male mate choice

Obs

Exp

Lab preference tests

b

Obs

Exp

Field preference tests

Empirical frequency of approaches Timing of pairing or egg-laying

Differential allocation by males

Assortative mating

Male mate choice

Obs

Exp

Lab preference tests

Obs

Exp

Field preference tests

Figure 7.8. Schematic representations of different approaches that can be used to study male mate choice for female coloration, showing (a) the strength of inference that can be drawn from various approaches, and (b) the actual frequency of studies that have adopted the various approaches, based on data in Table 7.3 and text. Wider arrows indicate (a) stronger inference and (b) more studies.

Studies of assortative or dissassortative mating patterns with respect to avian coloration have mostly been performed on species in which the two sexes are similar in appearance. Many of these species (e.g., Parasitic Jaegers [Stercorarius parasiticus], Gouldian Finches [Chloebia goulidiae; Plate 18]) display genetically determined plumage polymorphisms, but assortative mating also occurs in species with continuously varying condition-dependent colors (e.g., Blue Tits, American Goldfinches [Carduelis tristis; Plate 30, Volume 1], House Finches; Table 7.3). Assortative mating has been reported for structural as well as pigment-based coloration. However, not all species tested mate assortatively

Female Coloration

by color (Table 7.3). Interestingly, Northern Cardinals mate assortatively with respect to carotenoid-based plumage and bill color but not with respect to black mask color or red crest length (Jawor et al. 2003). Similarly, Least Auklets mate assortatively for plumage color, a melanin-based trait important in status signaling, but disassortatively for facial plumes (Jones and Montgomerie 1991). It is also noteworthy that assortative mating occurs in relation to carotenoid-based, melanin-based, psittacofulvin-based, and structural colors. That some species mate disassortatively with respect to plumage may reflect conflicting selection pressures on coloration (Houtman and Falls 1994). Despite inferential limitations, we recommend studies of assortative mating when controlled mate choice studies are not practically feasible, in particular, for species in which both sexes are conspicuously colorful. Assortative mating by color is consistent with the idea of mutual mate choice; it would thus be useful to know how common such patterns are among birds. Such analyses should ideally control for potential confounding factors like age or time of breeding for which birds could mate assortatively. If these or other factors are related to color display, a pattern of assortative mating by color could equally be due to choice for old or early-breeding partners as to choice for colorful ones. Direct Tests of Mate Preference The strongest evidence for male mate preferences in relation to female color comes from controlled mate preference tests either in the lab or in the field. Some of these tests include manipulation of the female ornament and are thus more conclusive. One standard way of testing for mate preferences is to allow a respondent (“chooser”) to select among two or more opposite-sex stimuli that differ in coloration (or other qualities). Such studies can be made in test cages indoors or outdoors (e.g., Hill 1993a; Hunt et al. 1999) or sometimes in the breeding habitat of the species (e.g., Amundsen et al. 1997). Mate choice trials of this kind have been widely adopted in studies of female preferences (e.g., see Chapter 4) and are now also being used to test for male preferences. Such tests have revealed male preferences for more colorful females in Bluethroats (Amundsen et al. 1997; Figure 7.9) and House Finches (Hill 1993a), and for a novel color ornament in Javan Munias (Lonchura leucogastroides; Witte and Curio 1999; see Table 7.3). In Zebra Finches, Burley and Coopersmith (1987) found a male preference for intermediate (orange) female bill color, unlike the red male bills preferred by females, and Vos (1995) later found that males preferred

315

Table 7.3. Studies Testing Whether Male Birds Prefer More Colorful Females Species Conspicuous coloration Yellow-eyed Penguin (Megadyptes antipodes) Magellanic Penguin (Spheniscus magellanicus) Northern Fulmar (Fulmarus glacialis) Blue-footed Booby (Sula nebouxii) Black Swan (Cygnus atratus) Snow Goose (Chen caerulescens)

Common Shelduck (Tadorna tadorna) Common Buzzard (Buteo buteo) Domestic Chicken (Gallus gallus) Eurasian Dotterel (Charadrius morinellus) Red-necked Phalarope (Phalarope lobatus) Parasitic Jaeger (Stercorarius parasiticus) Least Auklet (Aethia pusilla) Rock Pigeon (Columba livia) Budgerigar (Melopsittacus undulatus) Burrowing Parrot (Cyanoliseus patagonus) Barn Owl (Tyto alba) Northern Flicker (Colaptes auratus) Barn Swallow (Hirundo rustica) Bluethroat (Luscinia svecica) Blue Tit (Cyanistes caeruleus) Pinyon Jay (Gymnorhinus cyanocephalus) European Starling (Sturnus vulgaris) Rock Petronia (Petronia petronia)

Similarity to maleb

Color

Color typec

I

Yellow

P,(C)

I

Black

M

I

Dark/light gray

(M),(S)

I

Blue

(S)

I

Black

M

I

Brown, black, white, bluish-gray

M,(S)

Chest band

SW

Rusty-red

(M)

Body (P)

I

Brown/light

(M)

Comb

SW

Red

I, C

Cap, breast, belly Head, back

SS

(M)

Body (P)

I

Black, rufousred Rusty-red, brown Brown/white

Underside, head plumes, bill Neck, breast (P) Crown, cheeks

I

Black, white, red

M,(C)

I/SW

Blue, ash red

(S),(M)

I

S

I/SW

Fluorescent, UV Red

SS

Black

M

SW

Black, red

M,C

SW

Rusty-red

M

Throat patch

SW

Blue, chestnut, black

M+S

Crown

I/SW

Blue, UV

S

Malar feathers

SW

Bluish

(S)

Throat

SW

M,S

Breast

SW

“Dark,” gray, iridescent Yellow

Plumage parta Eye, postocular stripe Pectoral band, spots Body (P) Feet Body,wings Curled feathers Body, wings (P)

Abdominal patch Underside spottiness Moustache, nape Underside

SS

(M) M

Pf

C

Assortative mating

Association (time)

Study type e

Reference

+

FO

Massaro et al. (2003)

0/0

FO

Forero et al. (2001)

0

FO

Hatch (1991)

FE

Torres and Velando (2005)

FO

Kraaijeveld et al. (2004)

FO

Courtship

DAd

+ + +

+

+

FO

Cooke and Cooch (1968); Cooke et al. (1972, 1976); Cooke and McNally (1975); Findlay et al. (1985) Ferns and Lang (2003)

+

FO

Krüger et al. (2001)

(F)E

Pizzari et al. (2003)

FO

Owens et al. (1994)

+ + 0

Reynolds (1987)

+

FO

O’Donald (1959)

+/–/0

FO

Jones and Montgomerie (1991)

LO

Burley (1977, 1981b)

LE

Arnold et al. 2002

FO FO/FE

Masello and Quillfeldt (2003); Masello et al. (2004) Roulin (1999)

+

FO

Wiebe (2000)

+

FO

Safran and McGraw (2004)

LO

Amundsen et al. (1997); Smiseth and Amundsen (2000); Johnsen et al. (2003) Andersson et al. (1998); Hunt et al. (1999) Johnson (1988)

(0)

+

+

+ + +

+

+

+/0

+

0

+

LE

0

LO

(+) +

Komdeur et al. (2005) +

+

FO/FE

Griggio et al. (2003, 2005); Pilastro et al. (2003)

Table 7.3. (continued) Species Eastern Bluebird (Sialia sialis) Zebra Finch (Taeniopygia guttata) Gouldian Finch (Chloebia gouldiae) Javan Munia (Lonchura leucogastroides) House Finch (Carpodacus mexicanus) American Goldfinch (Carduelis tristis) White-throated Sparrow (Zonotrichia albicollis) Dark-eyed Junco (Junco hyemalis) Northern Cardinal (Cardinalis cardinalis) Red-winged Blackbird (Agelaius phoeniceus) Other conspicuous plumage traits Red-tailed Tropicbird (Phaeton rubricauda) European Shag (Phalacrocorax aristotelis) Crested Auklet (Aethia cristatella) Scissor-tailed Flycatcher (Tyrannus forficatus) Barn Swallow (Hirundo rustica) Bearded Reedling (Panurus biarmicus) Northern Cardinal (Cardinalis cardinalis)

Similarity to maleb

Color

Color typec

Breast, rump, tail Bill

SW

Blue, chestnut

M, S

SW

Orange

C

Face (P)

SW

Black/red/gold

M,(C), (S)

Novel trait: forehead feather Body

-

Red

(C)

SW

Red

C

Body

SW

Yellow

C

Head (P)

I

Black, white, brown

M

Tail

SW

White

M

Under-wing, body, face Epaulet

SW

Red/black

C,(M)

SW

Pale yellow to orange

C

Tail streamers

SW

Red

(C)

Crest

I

Black

M

Forehead crest

I

Black

O,(M)

Tail length

SW

Tail length

SW

Blackish

M

Tail length

SW

Light brown

O

Crest

SW

Red

O, (C)

Plumage parta

O

Notes: As evidenced by assortative mating, time spent in association with particular females, distribution of courtship, or differential allocation. +, Positive relationship; 0, no relationship; –, negative relationship. Parentheses indicate less conclusive evidence. a. (P), Genetically determined distinct color morphs (two or more). b. Similarity to male: I, indistinguishable; SW, similar but weaker ornament expression; SS, similar but stronger ornament expression. c. C, Carotenoid-based coloration; I, integument; M, melanin-based; P, pterin-based; Pf, psittacofulvinbased; S, structural; O, noncolor ornament (e.g., tail, crest). Judged mainly from visual appearance. d. DA, Differential allocation in relation to partner’s plumage, either in terms of sperm injected, time spent mate guarding, or paternal care. e. Type of study: FO, field observational; FE, field experimental (i.e., ornament manipulation); LO, lab (i.e., captive conditions) observational; LE, lab experimental.

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Assortative mating

Association (time)

319

Courtship

DAd

Study type e

0

Siefferman and Hill (2005)

–

+

+

0 –

+

+

–

+

+

+ –

Reference

(+)

0

LO/LE LO

Burley (1986); Burley and Coopersmith (1987) Fox et al. (2002)

LE

Witte and Curio (1999)

LE

Hill (1993a,b; 2002)

FO

MacDougall and Montgomerie (2003) Knapton and Falls (1983); Houtman and Falls (1994); Tuttle (2003) Wolf et al. (2004)

FO/LO

0

LE

+/0

FO 0

0/(+)

(0)

FE/ FO

Linville et al. (1998); Jawor et al. (2003) Muma and Weatherhead (1989)

+

FO

Veit and Jones (2003)

+

FO

Daunt et al. (2003)

FE

Jones and Hunter (1993)

(+)

FO

Regosin and Pruett-Jones (2001)

+/(+)

FE

Møller (1993); Cuervo et al. (1996) Romero-Pujante et al. (2002)

+

+ 0

+

0

LE

Jawor et al. (2003)

females with their mother’s bill color. Mutual mate choice can also occur for colors invisible to the human eye: both male and female Zebra Finches have been shown to take UV into consideration in mate choice (Bennett et al. 1996; Hunt et al. 1999), and male and female Budgerigars (Melopsittacus undulatus) use either UV or fluorescent cues in these contexts (Arnold et al. 2002; see Chapter 4; Table 7.3). In contrast, Dark-eyed Junco males showed no preference for whiter female tails (Wolf et al. 2004), and Gouldian Finch males

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Time near female (s)

1600

1200

800

400

0 colorful

drab

Female phenotype colorful

drab

Proportion of sexual behaviors

1

0.5

0 approach

display

association

Male behavior

Figure 7.9. Preference for colorful females by male Bluethroats, as shown by the time spent near colorful and drab females, and the proportions of sexual behaviors directed at colorful and drab females. Males were given a choice between two females that were markedly dissimilar in coloration but very similar in other respects. Males had visual but not physical access to the females, whereas the females were not permitted visual contact. Graph shows mean + standard error for each category. Redrawn from Amundsen et al. (1997).

Female Coloration

showed no preference for brighter female mask morphs (Fox et al. 2002). Some but not all of these studies involved color manipulation; the experimental studies of male choice have revealed evidence for choice in some species (Burley and Coopersmith 1987; Hill 1993a; Hunt et al. 1999; Arnold et al. 2002) but no evidence for choice in others (Wolf et al. 2004). In Bluethroats, males have been shown to prefer symmetrical over asymmetrical artificial female coloration (Hansen et al. 1999). Based on this limited set of studies, no conclusive statement can be made as to whether male birds generally favor more colorful females. Along with field experimentation, “choice chamber” studies have the greatest potential for revealing male preferences, and more such studies are obviously needed, preferably on a wider range of species than so far studied. Although it is understandable that small birds, such as passerines, have been much used in such contexts, future research should ideally include nonpasserine models as well as more tropical species with truly conspicuous colors. Even if the current evidence does not allow wide-ranging conclusions, it is clear that male birds are not always indifferent to female beauty when given a simultaneous choice in a lab setting. Such a male preference could be due to selection on the males or it could be a correlated effect of selection for choosiness in females (Halliday and Arnold 1987). Whether explained by selection on males or females, such choosiness would select for conspicuous female coloration. However, it is not obvious that mate preferences expressed in the lab translate into choosiness in the wild (Amundsen et al. 1997). The degree to which choosiness should be favored in the wild would very much depend on the actual social and mating system of each species. For instance, the opportunity for choice should be greater for species that assemble in social groups or colonies than among those defending individual territories. When the mating behavior of a species can be easily observed in the field, male (as well as female) mate preferences can be recorded from observations on natural populations. Combining trait-manipulation experiments in the field with laboratory mate-choice studies is the strongest approach and the one to be recommended whenever feasible (Figure 7.8; see also Chapter 4). The best known study of this kind relates to preferences not for color, but for a conspicuous black crest in colonial-nesting Crested Auklets. By manipulating crest size in male and female models and placing them at mating arenas in the midst of the colony, Jones and Hunter (1993, 1999) showed that both males and females performed more displays to long-crested than to short-crested members of the opposite sex. Similarly, Torres and Velando (2005) manipulated

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female foot color in Blue-footed Boobies (Sula nebouxii; Plate 16) and found that drab-footed females received less courtship both from their social mate and from males seeking extra-pair copulations. A recent study experimentally reducing the size of the yellow breast patch in Rock Petronias (Griggio et al. 2005) found that more colorful females received more courtship and were more successful in mating. In Eurasian Dotterels, naturally brightly colored females were more likely to be mated than drab-colored ones, but it is not known whether this pattern was due to male mate choice (Owens et al. 1994). Similarly, female Great Tits that paired with locally territorial males had wider breast stripes than females not pairing locally (Wilson 1992). Female partners of the same Barn Owl male were similarly spotted in successive years, suggesting male choice (Roulin 1999). Differential Allocation The differential allocation hypothesis (Burley 1986, 1988; Sheldon 2000a) posits that individuals mated to attractive partners should provide better parental care, because offspring of attractive partners are supposedly of a higher quality (thus of a higher value). This idea, however, does not necessarily imply mate choice. Even if the hypothesis was initially formulated to explain patterns of female care in relation to male color, differential allocation by males in relation to female color has now been reported both with respect to male feeding effort and male nest defense. In Barn Owls, males mated to females that had been manipulated to become less spotted fed their offspring less and had reduced reproductive success (Roulin 1999). Similarly, House Finch males fed the offspring of brightly colored females more than those of drab females (Hill 2002). By contrast, Linville and co-workers (1998) found no relationship between female under-wing color and male feeding rate in Northern Cardinals. In Rock Petronias, observational (Griggio et al. 2003) and experimental (Pilastro et al. 2003) work has revealed that males show greater nest attendance and are thus more active in nest defense when mated to females with larger yellow breast patches. One cryptic form of prefertilization differential allocation may be how males that mate with several females allocate their limited sperm stores (e.g., see Wedell et al. 2002). Pizzari and co-workers (2003) recently found that roosters injected more sperm when mating with hens having the largest red combs, mainly because such hens were paired first. Apparently, male choice should not be disregarded even for promiscuous or polygynous species. In such species,

Female Coloration

choosiness may not be reflected in whether males mate or copulate, but in the temporal distribution of matings and thus in sperm allocation. Another form of prefertilization differential allocation may be the degree to which males guard their mates against extra-pair copulations. Because mate guarding is costly and conflicts with mate attraction (e.g., Johnsen et al. 1997), males mated to attractive females might respond by guarding more strongly. However, a study on Bluethroats found no such relationship (Johnsen et al. 2003). Taken together, the current evidence is far too limited to generalize on the merits of differential allocation by males in response to female coloration; more studies of this kind are needed. Male Mate Choice: Common or Rare? Until recently, male choice in birds was not considered a realistic possibility, apart perhaps from polyandrous species. It is now well established, however, that males can be selective in their choice of social and extra-pair partners and in how much they care for offspring. How common each of these phenomena are among the many avian taxa, or how important they are in the evolution of female ornaments, including coloration, remains to be shown. We would particularly encourage future work on species where both sexes are conspicuously colorful, aiming to simultaneously test for competition and mate choice in both sexes. The addition of male mate choice and female-female competition to the well-established processes of female choice and male competition can make animal mating dynamics far more complex than previously thought (Amundsen 2000b; Forsgren et al. 2004). However, we currently have little idea how common mutual mate choice and competition in both sexes are among birds. As is generally the case, the strongest approach to test whether female colors are attractive to males is the experimental one, which in turn is strongest when performed in the field (Figure 7.8a). However, only a small proportion of studies relating to male mate preferences have been of this kind (Figure 7.8b). Instead, the majority of studies cited in this article (see Table 7.3) reports patterns of assortative mating, the perhaps least conclusive approach of all, and most preference tests for female color have been made in the lab rather than in the field (Figure 7.8b). There is a striking discrepancy between which kinds of studies would be most informative about male choice for female coloration (Figure 7.8a), and which kinds of studies have actually been performed (Figure 7.8b).

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A Hormonal Byproduct? Many of the differences in showiness between males and females (that share a largely common genome) are likely mediated by sex-specific hormonal mechanisms (Chapter 10, Volume 1; Figure 7.1). Observations of colorful females in species where females are normally thought to be drab (e.g., Bluethroats) have often been attributed to hormonal anomalies. This attitude may reflect a conventional view that males but not females should carry extravagant ornamentation. Similarly, female vocalizations were long considered to be caused by hormonal anomalies, but have later been proven to function in communication (Langmore 1998, 2000). The idea that male-like colors in females are due to hormonal anomalies has assumed that female colors are caused by excess testosterone, either as a byproduct of selection on males or as a result of malfunctioning of the endocrine regulatory system. However, Owens and Short (1995) have pointed out that male-like coloration in females of many avian taxa result from low estrogen rather than high testosterone levels; such deficiencies can occur at postreproductive ages or if the reproductive system is malfunctioning. A survey by Kimball and Ligon (1999) has shown that the hormonal basis of conspicuous coloration varies greatly among avian taxa, the colors being regulated by estrogen in some and testosterone in others (e.g., Eens et al. 2000) and also by other hormones. Additionally, some color traits appear not to be hormonally regulated. Taken together, the hormonal control of avian colors appears complex and taxonomically diverse (Owens and Short 1995; Kimball and Ligon 1999; Chapter 10, Volume 1). One should bear in mind that even if studies of hormonal regulation provide insights into the development and physiological causation of female colors, they cannot be used to infer the ultimate function of such traits. Any hormonal mechanism that results in maladaptive female coloration should be selected against, provided that the hormonal mechanism in itself is not beneficial. It seems unlikely that particularly high levels of male sex hormones, or low levels of female sex hormones, should be beneficial to a female. If female coloration is hormonally induced but carries no benefit, its likely cost (e.g., in terms of energy expenditure, predation risk) should eventually lead to a modification of the hormone-color connection and a consequent reduction in female coloration. Even though such an evolutionary process may take time (Lande 1980), it is unlikely that severely maladaptive female colors would be maintained in natural populations.

Female Coloration

Other Explanations of Female Color Concealment of Sexual Identity In social birds, females may sometimes be subject to sexual harassment or other negative interactions that relate to sexual identity. This circumstance may result in selection for concealment of sexual identity (Burley 1981a), leading to a male-like appearance. Even if such a plumage is costly for females, these costs may sometimes be compensated by the benefits of concealing sexual identity (Figure 7.1). Burley’s (1981a) idea has not been subject to much empirical testing (but see Langmore and Bennett 1999) and deserves further attention.

Species Recognition Species recognition was long considered a main cause of conspicuous coloration (and other ornaments) in birds and other animals (Mayr 1963; but see discussions in Cronin 1991; Andersson 1994; Figure 7.1). In particular, this idea has been adopted to explain similarly conspicuous coloration in the two sexes, thus including many cases of female coloration. However, current knowledge suggests that there is no conflict between species recognition and sexual functions of an ornament, and that, typically, sexual selection precedes species diversification rather than vice versa (e.g., Sætre 2000; Seehausen 2000; Panhuis et al. 2001; Stuart-Fox and Owens 2003). Sexual imprinting on parental appearance (Owens et al. 1999; Slagsvold et al. 2002) may facilitate such diversification. Critical tests of species recognition as an explanation of bright monochromatism are needed, and the idea should not yet be dismissed (see Chapters 1 and 2).

Signaling Readiness to Mate Females of several fishes seem to signal their readiness to spawn by temporary coloration (e.g., Rowland et al. 1991; McLennan 1995). Most female bird colors are not transient, however, and would not be informative is such contexts. One possible exception is the blood-red cloacas that female Alpine Accentors (Prunella collaris) and some other species display when they are ready to mate (Nakamura 1990).

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Female Colors and Sex Roles The traditional emphasis on extravagant coloration as a male trait is tightly linked to the equally traditional view that, by and large, animals have conventional sex roles. That is, males compete for access to female mates while females compete little, if at all, for access to males (Vincent et al. 1992). Male mating competition should favor traits in males that signal their abilities to compete successfully with other males or that make their bearer attractive to females (Andersson 1994). Provided that conventional sex roles were ubiquitous, selection for conspicuousness should be largely on the males. Accordingly, females would be expected to be drab and cryptic. However, sex roles are not always conventional. Ever since Darwin (1871), we have known that some species appear to have “reversed” sex roles, with males being a limited resource to females rather then the reverse. Darwin elaborated this issue using painted snipes, phalaropes, and dotterels as examples, and pointed out the typical reversal of parental roles. Today, phalaropes, in particular, are often communicated in popular media as an example of sexual selection favoring conspicuous coloration in females. Given such conventional wisdom, it is notable that the only study testing for functions of coloration in phalaropes found very little evidence that colorful females obtain any breeding benefits (Reynolds 1987). However, in pipefishes, the most well-studied group of sexrole reversed animals, there is ample evidence that female coloration and patterning is related to intrasexual competition and male mate choice (Berglund and Rosenqvist 2003). Considerable variation in plumage expression of males and females exists among polyandrous species. Painted snipes are strongly dichromatic, with only the females displaying conspicuous colors; phalaropes and dotterels are weakly dichromatic (females more colorful); jacanas are conspicuously monomorphic; Spotted Sandpipers (Actitis macularia) monomorphically drab. Clearly, reversed dichromatism is not a necessary consequence of polyandry. Assuming that polyandry reflects reversed sex roles (i.e., mating competition), there appears to be no strong link between sex roles and color patterns. The lack of a simple relationship between coloration and sex roles is even more evident from a survey of the vast majority of bird species that have rather conventional sex roles. This list includes all species in which males are either socially or sexually polygamous. Provided there is a reasonably unbiased sex ratio, mating competition should be stronger in males than in females of such species. The diversity of male and female coloration in this large group of birds

Female Coloration

is enormous, encompassing everything from no ornamental coloration in females to highly conspicuous female colors. A recent survey of more than one thousand bird species by Dunn and co-workers (2001), however, showed that socially polygamous species are generally more dichromatic (and size dimorphic) than are monogamous ones. Notably, there was no similar effect of sexual polygamy as evidenced by testis size, a measure of sperm competition (Dunn et al. 2001). Conspicuously monochromatic birds are often monogamous (Badyaev and Hill 2003), but not always. One feature that seems to unite many species in which both males and females are colorful, however, is that both sexes are heavily involved in parental care. Parental care may be crucial in determining sex roles, by affecting the operational sex ratio (Emlen and Oring 1977), through effects on reproductive costs (Kokko and Monaghan 2001), or both. Sex roles, in turn, determine the direction and strength of sexual selection—when sex roles are similar, sexual selection may be equally strong in the two sexes. There is no established term for this situation, but it could, for instance, be termed “balanced” or (more anthropomorphically) “egalitarian” sex roles. Given that many species of birds have bi-parental care, many avian species likely fulfill the criterion for “balanced sex roles.” A similarity of parental roles could potentially explain why so many species have similar coloration (and other forms of ornamentation) in the two sexes. However, the idea that extensive bi-parental care is a key to monochromatic coloration remains hypothetical and requires extensive testing. Traditionally, empiricists have explicitly or implicitly assumed that when one sex (typically the female) is choosy, the other (typically the male) is not. This need not be true, however. In fact, any combination of choosiness in the two sexes is theoretically possible under certain conditions (Parker 1983; Johnstone et al. 1996; Kokko and Johnstone 2002). That choosiness in one sex does not preclude choosiness in the other may be illustrated by Johnson’s (1988) study of Pinyon Jays, for which the sex ratio in the population suggested that all females could acquire a mate and mating competition therefore was stronger in males. Nonetheless, females still competed for the highestquality mates. Recent studies have revealed that roles may vary dramatically not only among but also within species (e.g., Gwynne et al. 1998; Forsgren et al. 2004). Such variation can occur because of variation in operational sex ratios (Emlen and Oring 1977; Kvarnemo and Ahnesjö 1996) or as a result of sex-specific reproductive costs (Kokko and Monaghan 2001; Kokko and Johnstone 2002). Unfortunately, knowledge of natural variation in the operational sex ratios of

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animals, including birds, is scant (but see Colwell and Oring 1988). However, bird species that are structured into small, discrete subpopulations may experience such fluctuations, spatially and temporally, and thus be subject to fluctuating selection pressures for male versus female coloration.

Challenges in Future Research: Methods The Risk of Publication Bias A majority of published work on female coloration has reported positive results (see Tables 7.1–7.3), which may at first be taken to indicate very clear patterns of support for functional hypotheses and consistent selection pressures across species. Unfortunately, it may also reflect a publication bias in favor of positive results (e.g., Møller and Jennions 2001; Jennions and Møller 2002), leaving the interpretation uncertain. We believe that this problem may have been more severe some years ago, when much research on female ornamentation was the byproduct of research on male coloration, leading to a risk that only “exciting patterns” were published. Today, with more projects focusing specifically on female colors, it is more likely that results are published whether they are positive or negative. We strongly encourage researchers addressing female colors to publish all robust datasets they produce, thereby establishing an unbiased literature for general inferences about the functions of female coloration. The Need for Experiments Until recently, almost all work on female coloration was observational, in the sense that colors were not manipulated. Lack of experiments has significantly hampered inferences about causality in studies of female colors (and other ornaments). Experimentation has been more widely adopted in studies of males, and the paucity of experimental studies of female coloration may again reflect that such studies often were based on observations made as byproducts of male studies. Now, as work focused specifically on females becomes more common, so does experimentation in studies of female color (e.g., Vos 1995; Hunt et al. 1999; Arnold et al. 2002; Hill 2002). Color manipulation is perhaps most easily used in studies of female mate attraction. Future work should also aim to refine methods for sensible experimentation in studies relating female color to quality, competition, and other issues. To allow strong inference, it is im-

Female Coloration

perative that treatments in future work are realistic and within the natural range of variation for the species in question. It is also imperative that the typical sample size is increased; many studies of female coloration (see Tables 7.1– 7.3) have been based on samples sizes that are less than 20 and sometimes less than 10, which does not allow for robust conclusions.

Summary There is now quite conclusive evidence that coloration in female birds can function in intra- and intersexual signaling. It is not yet clear, however, whether certain kinds of colors are more important than others in competitive or mate attraction contexts, or more likely to reflect certain qualities of the bearer. Even if the study of female colors and other ornaments has developed significantly during the past 5 years (cf. Amundsen 2000a,b), many questions are still open. Here we briefly summarize the current knowledge, focusing on topics that deserve attention in future studies. Most studies of female coloration in birds have been conducted on species in which either both sexes or females are not strikingly conspicuous to human eyes. We recommend a stronger focus on species in which females are as colorful as the males. We also recommend a future focus on bird species that have different yet conspicuous coloration in the two sexes; it is a puzzle why these species have evolved color patterns different from most other birds. The question of whether the same colors should be expected to function both in competitive and mate attraction contexts is theoretically not trivial. On the one hand, signals may have a dual utility. On the other hand, it has been suggested that status badges could be cheap but signals for mate attraction costly. Melanin-based traits have been thought to fit the former requirement, carotenoid-based traits the latter. Studies of female coloration have not produced any clear pattern with respect to the use of different (or similar) colors in the two contexts. Moreover, studies to date have produced mixed patterns for the function of female coloration. In certain species, female colors seem to function in male choice but not female competition; in other species, the function is competition but not male choice. Even opposing selection by female competition and male choice has been found. More studies are needed before any patterns to guide a general understanding can emerge. In quite a number of species, coloration relates to some kind of quality of the female. However, for about half of these species, it is unknown whether coloration functions in female competition or male mate choice (Figure 7.10).

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Number of species

16

12

8

4

0 FQ+ FFC– MP–

FQ+ FFC+ MP–

FQ+ FFC– MP+

FQ+ FFC+ MP+

FQ– FFC+ MP–

FQ– FFC– MP+

FQ– FFC+ MP+

Aspects of female color investigated Figure 7.10. Number of species for which various aspects of female coloration have been investigated. Whether or not a particular aspect has been studied is represented by + and –, respectively. Hence, the figure illustrates the extent to which various issues relating to female coloration have been scientifically studied, not whether these studies produced positive or negative results. Based on data in Tables 7.1–7.3. Studies that provide only circumstantial evidence relating to a function in female-female competition (FFC) or male mate preference (MP) (viz., female territoriality for FFC and assortative mating for MP) are not included. FQ, female quality.

Likewise, for many of the species in which males display preferences for female color, it remains to be determined what males gain by such choice (Figure 7.10). Although some evidence exists that female color reflects age, body condition, immunocompetence, or maternal care in certain species, much more research is needed before we can judge which of these qualities are more often related to female coloration. We also need to know which qualities are reflected in which sorts of colors and color patterns (and other ornaments). Female colors can either be under simple genetic control with discrete color morphs, or they can show continuous variation, which may reflect some kind of condition dependence. These two phenomena likely require different explanations, but few attempts have been made to clarify the underlying differences in evolutionary dynamics.

Female Coloration

A disproportionately large number of studies of female coloration has been conducted on passerines. In particular, this restriction to passerines applies to many of the more conclusive tests of color functions in female competition and male mate choice. Such a narrow taxonomic range in the choice of model species limits the generality of inference to be drawn, and we welcome the recent increase in studies of nonpasserines. Work done during the past few decades has convincingly demonstrated that female colors may reflect a variety of qualities and have a multitude of functions; the more important likely being status signaling and mate attraction. However, there are still more questions than conclusive answers on this issue and much more work is needed before we can reach a robust and comprehensive understanding of why females of so many bird species are beautifully colored.

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trond amundsen & henrik pärn Roulin, A., and C. Dijkstra. 2003. Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the Barn Owl. Heredity 90: 359–364. Roulin, A., T. W. Jungi, H. Pfister, and C. Dijkstra. 2000. Female Barn Owls (Tyto alba) advertise good genes. Proc R Soc Lond B 267: 937–941. Roulin, A., C. Dijkstra, C. Riols, and A. L. Ducrest. 2001a. Female- and male-specific signals of quality in the Barn Owl. J Evol Biol 14: 255–266. Roulin, A., C. Riols, C. Dijkstra, and A. L. Ducrest. 2001b. Female plumage spottiness signals parasite resistance in the Barn Owl (Tyto alba). Behav Ecol 12: 103–110. Roulin, A., A. L. Ducrest, F. Balloux, C. Dijkstra, and C. Riols. 2003a. A female melanin ornament signals offspring fluctuating asymmetry in the Barn Owl. Proc R Soc Lond B 270: 167–171. Roulin, A., B. Ducret, P. A. Ravussin, and R. Altwegg. 2003b. Female colour polymorphism covaries with reproductive strategies in the Tawny Owl Strix aluco. J Avian Biol 34: 393–401. Rowe, L., and D. Houle. 1996. The lek paradox and the capture of genetic variance by condition-dependent traits. Proc R Soc Lond B 263: 1415–1421. Rowland, W. J., C. L. Baube, and T. T. Horan. 1991. Signalling of receptivity by pigmentation in female Sticklebacks. Anim Behav 42: 243–249. Ruusila, V., H. Pöysä, and P. Runko. 2001. Female wing plumage reflects reproductive success in Common Goldeneye Bucephala clangula. J Avian Biol 32: 1–5. Sæther, S. A. 2002. Female calls in lek-mating birds: Indirect mate choice, female competition for mates, or direct mate choice? Behav Ecol 13: 344–352. Sætre, G.-P. 2000. Sexual signals and speciation. In Y. Espmark, T. Amundsen, and G. Rosenqvist, ed., Animal Signals, 237–257. Trondheim: Tapir Academic Press. Safran, R. J., and K. J. McGraw. 2004. Plumage coloration, not length or symmetry of tail-streamers, is a sexually selected trait in North American Barn Swallows. Behav Ecol 15: 455–461. Saino, N., J. J. Cuervo, P. Ninni, F. de Lope, and A. P. Møller. 1997. Haematocrit correlates with tail ornament size in three populations of the Barn Swallow (Hirundo rustica). Funct Ecol 11: 604–610. Sandell, M. I. 1998. Female aggression and the maintenance of monogamy: Female behaviour predicts male mating status in European Starlings. Proc R Soc Lond B 265: 1307–1311. Sandell, M. I., and H. G. Smith. 1997. Female aggression in the European Starling during the breeding season. Anim Behav 53: 13–23. Seehausen, O. 2000. Explosive speciation rates and unusual species richness in haplochromine cichlid fishes: Effects of sexual selection. Adv Ecol Res 31: 237–274. Senar, J. C., J. Figuerola, and J. Pascual. 2002. Brighter yellow Blue Tits make better parents. Proc R Soc Lond B 269: 257–261.

Female Coloration Senar, J. C., J. Figuerola, and J. Domenech. 2003. Plumage coloration and nutritional condition in the Great Tit Parus major: The roles of carotenoids and melanins differ. Naturwissenschaften 90: 234–237. Sheldon, B. C. 2000a. Differential allocation: Tests, mechanisms and implications. Trends Ecol Evol 15: 397–402. Sheldon, B. C. 2000b. Environmental dependence of genetic indicator mechanisms. In Y. Espmark, T. Amundsen, and G. Rosenqvist, ed., Animal Signals, 195–207. Trondheim: Tapir Academic Publishers. Siefferman, L., and G. E. Hill. 2005. Evidence for sexual selection on structural plumage coloration in female Eastern Bluebirds (Sialia sialis). Evolution 59: 1819–1828. Slagsvold, T., T. Amundsen, S. Dale, and H. Lampe. 1992. Female-female aggression explains polyterritoriality in male Pied Flycatchers. Anim Behav 43: 397–408. Slagsvold, T., B. T. Hansen, L. E. Johannessen, and J. T. Lifjeld. 2002. Mate choice and imprinting in birds studied by cross-fostering in the wild. Proc R Soc Lond B 269: 1449–1455. Smiseth, P. T., and T. Amundsen. 2000. Does female plumage coloration signal parental quality? A male removal experiment with the Bluethroat (Luscinia s. svecica). Behav Ecol Sociobiol 47: 205–212. Stuart-Fox, D., and I. P. F. Owens. 2003. Species richness in agamid lizards: Chance, body size, sexual selection or ecology? J Evol Biol 16: 659–669. Stutchbury, B. J. 1994. Competition for winter territories in a Neotropical migrant: The role of age, sex and color. Auk 111: 63–69. Stutchbury, B. J., and R. J. Robertson. 1987a. Behavioral tactics of subadult female floaters in the Tree Swallow. Behav Ecol Sociobiol 20: 413–419. Stutchbury, B. J., and R. J. Robertson. 1987b. Signaling subordinate and female status: Two hypotheses for the adaptive significance of subadult plumage in female Tree Swallows. Auk 104: 717–723. Swaddle, J. P., and M. S. Witter. 1995. Chest plumage, dominance and fluctuating asymmetry in female starlings. Proc R Soc Lond B 260: 219–223. Tella, J. L., M. G. Forero, J. A. Donazar, and F. Hiraldo. 1997. Is the expression of male traits in female Lesser Kestrels related to sexual selection? Ethology 103: 72–81. Thompson, C. W., and M. Leu. 1995. Molts and plumages of Orange-breasted Buntings (Passerina leclancherii): Implications for theories of delayed plumage maturation. Auk 112: 1–19. Tomkins, J. L., J. Radwan, J. S. Kotiaho, and T. Tregenza. 2004. Genic capture and resolving the lek paradox. Trends Ecol Evol 19: 323–328. Torres, R., and A. Velando. 2005. Male preference for female foot colour in the socially monogamous Blue-footed Booby, Sula nebouxii. Anim Behav 69: 59–65. Trail, P. W. 1990. Why should lek-breeders be monomorphic? Evolution 44: 1837– 1852.

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8 Colorful Phenotypes of Colorless Genotypes: Toward a New Evolutionary Synthesis of Color Displays alexander v. badyaev

Evolution of Development in Color Displays: A Need for a New Conceptual Framework Few animal taxa rival birds in richness and diversity of color displays, and few traits have stimulated more studies of natural and sexual selection than animal coloration. Although we have some understanding of why and when such diversity is favored, we know exceptionally little about how this diversity is generated and how it evolves. This is especially unfortunate, given that studies of color variation were central to the foundational work in quantitative genetics and evolutionary theory. Working with distinct color variants of flowers, Gregor Mendel discovered discrete and heritable segregation of color between individuals, leading him to conclude that the phenotypic differences are caused by the sorting of heritable and environmentally invariant internal factors. Observing differences among species and domestic breeds in plumage color, Charles Darwin suggested that the differences among individuals and species are caused by their fit to the external environment or to the tastes of animal breeders. A synthesis of these two great insights posited that internal factors cause variation, whereas independent external factors sort, delete, or retain these variants (Lewontin

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alexander v. badyaev 1983). Thus, at the base of the current theory of evolution is the foundational assumption of population genetics, stating that evolutionary change is an outcome of spontaneous and random generation of genetic variation and subsequent retention and sorting of this variation by natural selection and genetic drift (Futuyma 1998). Yet this view skips a crucial step in organic evolution—production of the phenotype—and so decouples the causes of within-generation variation from the causes of among-generation variation and thus of evolution (Schmalhausen 1949; Whyte 1965; Lewontin 1983; West-Eberhard 1989; Schlichting and Pigliucci 1998; Oyama 2000; Griffiths and Gray 2001). The result is that population genetics theory, which assumes that phenotypes are direct and heritable representations of genotypes (Falconer and MacKay 1996; Graur and Li 2000), does not provide a sufficient framework for understanding the origin and evolution of phenotypes, including the formation and diversification of color displays. At the same time, studies of animal coloration are uniquely positioned to resolve these conceptual difficulties and to contribute to the novel evolutionary synthesis that explicitly integrates the origination, variability, and evolutionary maintenance of traits. For example, current evolutionary theory assumes that developmental processes that produce a phenotype are not dependent on the selection acting on that phenotype (and thus are not “visible” to this selection). Yet many avian studies document sexual selection for greater conditionand health-dependency of color ornaments (Chapter 4), explicitly suggesting that selection can act on the underlying development of displays (Badyaev 2004a; Badyaev and Young 2004). Moreover, the assumption that phenotypic differences are generated in a predictable manner by internal organismal factors is violated in several types of animal pigmentation that require consumption and subsequent developmental incorporation of pigments obtained from the external environment (Brush and Power 1976; Endler 1983; Hill 1992; Knüttel and Fiedler 2001). Similarly, the environment external to the organism is invariably incorporated into avian color displays that require environmental matching (e.g., bowerbirds displaying their plumage colors against their externally collected nest objects (Plate 20, Volume 1) or manakins exposing a particular color pattern under a certain ambient light (Plate 3, Volume 1)). The crucial importance of cultural inheritance and sexual imprinting (whereby phenotypes of one generation determine patterns and direction of sexual selection in the next; Cate and Bateson 1988; Grant and Grant 1996; Irwin and Price 1999; reviewed in Odling-Smee et al. 2003), sensory bias processes in mate choice (Sargent et al. 1998; Kamo et al. 2002; Rodd et al.

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2002), and the importance of prior experience in both development of and selection on sexual traits (e.g., Badyaev and Qvarnström 2002; Sockman et al. 2002; Badyaev and Duckworth 2005) further violate the notion of the independence of selection and development of the phenotype. More generally, the failure to incorporate a developmental perspective in studies of the diversification of animal displays has left us largely unprepared to explain a great number of fascinating empirical results. For example, despite an amazing diversity of avian color patterns, there is also an equally remarkable convergence of complex pigmentation patterns among phylogenetically distinct species (Price and Pavelka 1996; Omland and Lanyon 2000; Plate 32). Apparently, once formed, these patterns can be preserved without being expressed for millions of generations, suggesting that their highly modular (i.e., context-independent) genetic and developmental organization allow these patterns to appear intact in distinct lineages. Similarly, complex sex-specific color patterns can lay dormant in the opposite sex and appear under hormonal treatment or when selection against such expression ceases (Winterbottom 1929; Kimball and Ligon 1999; Lank et al. 1999; Badyaev 2002; reviewed in Badyaev and Hill 2003). What enables such complexity to be preserved when not expressed? And how is it created in the first place? Moreover, in all pigment classes of avian coloration, there are two distinct expressions of withinspecies variation (Chapter 2): continuous variation and dichotomous variation, in which individuals have distinct morphs of coloration (including those related to age and sex). Are these patterns a continuum produced by the same mechanisms? Why does color polymorphism in some species result from developmental pathways that, invariably from the external environment or the organism’s state, deliver the effects of a single point mutation to the expression of color in the entire phenotype (Ritland et al. 2001; Theron et al. 2001; Nachman et al. 2003; Mundy et al. 2004; Rosenblum et al. 2004), whereas in other species, the same color phenotype is accomplished by a multitude of variable and reversible epigenetic effects of temperature (Iljin and Iljin 1930), hormonal state (West and Packer 2002), and nutrition (Brush and Power 1976; Stradi et al. 2001)? Of the many mutations in hundreds of loci that affect diverse pigmentation within species (Barsh 2001; Bennett and Lamoreux 2003), why do only a handful account for nearly all cases of polymorphism within species, populations, and even animal classes (Newton et al. 2000; Ling et al. 2003; Mundy et al. 2004)? For example, the effect of a point substitution in the melanocortin-1 receptor (MC1R) gene on the production of white/black and

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Figure 8.1. Conceptual illustration of within-phenotype color production and expression at four production stages (rectangular frames) and among individual elements (circles). Color production within a generation is a result of bottom-top interactions of elements at the stage of initial acquisition or genetic encoding (signified by a1, etc.), at the stage of development (d1, etc.), at the stage of phenotypic expression (e1, etc.), and the stage of courtship or other signaling displays that involve phenotypic expression of both color and behavior (c1, etc.). At each stage, production includes incorporation of elements external to the organism (x1, etc.), and expression of all elements within a phenotype (although not transitional pathways among them, shown by straight arrows) is subject to external selection (S). The expression of elements at each production stage consists of a combination of organismal elements at that and lower production stages, including incorporated external elements. For example, expression element e2 consists of incorporation (developmental entanglement) of external element x1 by acquisition element a1 and development elements d1 and a2, as well as d3 effects on d2, and d2 itself. External selection at each stage acts on some elements and their combinations. For example, expression of d2, d4, and d6 has fitness consequences during the stage of development. Both selection patterns and the elements of external environments (x elements) are not independent among production stages (dashed lines and arrows). Interactions among organismal elements within and between levels can be both linear and nonlinear; thus the cumulative effects of elements on one another are not additive.

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black/yellow phenotypes is modular enough to persist in grafts transplanted between different animal classes (Ling et al. 2003), yet color polymorphism in congeners and even conspecifics is often produced by distinct and variable mechanisms (Barsh 1996; Hoekstra and Nachman 2003; MacDougall-Shackleton et al. 2003). Similarly, why do some bird species possess developmental processes that enable them to maintain carotenoid-based coloration in captivity despite drastic changes in diet, whereas other, often closely related species lose their coloration after the first molt (Dormidontov 1930; Stradi et al. 1997, 2001)? Central, but implicit, in these questions is the notion that the processes and elements involved in color acquisition, encoding, development, and expression vary in their modularity—the ability to form and maintain a stable and largely independent network that retains its integration in different contexts and over evolutionary time scales (Wagner 2001; Schlosser and Wagner 2004; Callebaut and Raskin-Gutman 2005). In this chapter, I suggest that explicit consideration of the origin and inheritance of modularity and of the directionality and linearity of interactions between elements at different levels of color development (Figure 8.1) not only answers these questions, but also provides important insight into the evolution of diversity in avian color displays.

Evidence for Modularity in Encoding, Development, and Expression of Plumage Coloration The variability and diversification of avian color displays are best understood by considering plumage ontogeny and evolution as a series of hierarchically arranged and recurrent developmental and functional modules, from feathergerm precursors to coordination of pigment distribution among follicles to complex courtship displays (Jiang et al. 1999; Chuong et al. 2000; Price 2002; Prum and Dyck 2003; Badyaev 2004b; Figure 8.1; Plate 24). Classic experiments that surgically transplanted feather follicles among body parts and individuals (Lillie and Wang 1941; Willier 1941) established the feather follicle as a module capable of normal feather morph production and pigment metabolism and uptake in a variety of contexts. For example, follicles transplanted from the embryonic wing bud of the striped mutant chicken (Gallus gallus) produced the striped phenotype in an unstriped host (Danfort and Foster 1929; Willier 1941; Nickerson 1944). Recent studies extended these findings by documenting remarkably conserved signaling modules at the level of the follicle and repeated co-option of early signaling pathways in distinct

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Figure 8.2. Conceptual illustration of modularity in color production across elements at three general production levels: encoding (signified by g1, etc.), development (d1, etc.), and expression (e1, etc.). (a) Modularity across all stages is produced by duplication of a pathway from g1 to d1, by strengthening pathways between d1 and d2 and e1 and e2 within stages, and by constructing pathways d1 → e1 and d2 → e2 (e.g., decoupling digestion of carotenoids from general metabolism and depositing them in integument). (b) Modularity between the encoding and expression stages is accomplished by a deletion of an intermediate stage and strengthening the pathways among elements within stages (e.g., direct/passive deposition of environmentally derived pigment into plumage, MC1R mutation of high developmental penetrance). (c) Modularity in the stages of development and expression is produced by incorporation of a shared environmental element (x1) that influences d2 and d3 at the developmental stage and e2 and e3 at the expression stage, thus producing direct paths d2 → e2 and d3 → e3 (e.g., incorporations of an environmentally derived substance such as oil that influences development of both pigment and feather structure and thus their coexpression). (d) Modularity in expression is produced by the effect of a modifier (m1) at encoding stage on expression of both d1 and d3, thus causing co-expression of e1 and e3 (e.g., influence of a modifier on early developmental effects of testosterone influencing both later expression of behavior and concurrent metabolism of melanin).

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developmental contexts (Harris et al. 2002), as well as significant molecular linkage of genes encoding developmental aspects of plumage coloration (Bitgood and Somes 2003). At first, such modularity in the encoding of early developmental pathways may not seem surprising—modularity in gene sequences (e.g., intron structure) is typical of eukaryotes and is thought to result from enhancer-independent transcription and from the versatility and complexity of developmental systems (Patthy 1999, 2003; Mattick and Gagen 2001). Yet phenotype-genotype modularity in coloration might be a highly derived outcome of selection. I suggest here that the MC1R genetic and developmental module of color production in the examples mentioned above or the effects of chromosome inversion on color morphs in some birds (Houtman and Falls 1994; Krüger et al. 2001) is an end-point of selection for the most predictable and efficient (i.e., context-independent) expression of a particular color (see below; Figure 8.2). In any source of coloration, including carotenoid- and melanin-derived pigmentation, development of color expression can be either context-dependent (e.g., condition-dependent) or context insensitive (i.e., modular). The controversy over greater “condition dependence” of some pigments over others, especially in the behavioral ecology literature, stems from the assignment of the function (e.g., condition dependence) to a particular form (e.g., pigment in the food) prior to selection that produces (and defines) that function during development. Thus, as long as the function (here, condition dependence) is seen as pre-existing and uncoupled from a sexual ornament’s development, it does little to uncover the evolution of either condition dependence or a sexual ornament. It is not surprising, therefore, that some species with carotenoid-based ornamentation produce stable plumage color on virtually any diet, whereas the coloration of others is highly sensitive to pre-molt consumption of carotenoids. Similarly, in some species, melanin-based ornamentation is produced by environment-, context-, and sometimes taxa-invariant modular developmental processes, whereas in others, it depends on the local environment and individual health (reviewed in Badyaev 2004b). In either pigmentation type, a complete modularity in production of color (i.e., a linear representation between phenotype and genotype) is probably rare in natural systems. Genetically heritable color morphs, however, are common, especially in domestic breeds, where they can persist even in hybrids by forming intermediate patterns of color distribution and feather structures (e.g., Price 2002).

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alexander v. badyaev Extensive pleiotropic effects of color production on general growth and metabolism in poultry demonstrate that color production is often accomplished by recruitment of developmental pathways shared with other organismal functions (Somes 1980; Minvielle et al. 1999; Merat 2003; see also Badyaev 2005a). Because of such integration, the production of color display has to be decoupled from other organismal functions (Badyaev 2004a; Figure 8.2) to enable predictable and heritable expression of a color morph. Consequently, in most systems, modularity is confined to the late developmental stages; for example, sex- and age-specific pigmentation are accomplished at the level of the follicle and involve predictable epigenetic interactions (Punnett and Pease 1930; Somes 1971; George et al. 1981; Abdellatif 2001) rather than genetic mechanisms (Somes 2003). Late-stage regulation of melanin pattern expression may enable the historical persistence of developmental modules. Price and Pavelka (1996) hypothesized that, when the developmental module of a melanin-based pattern is formed, its phenotypic expression and retention are mediated by a switch-like sensitivity of regulatory receptors at late developmental stages. Thus, complex melanin-based coloration patterns, once formed, can appear in distant lineages without the need to construct complex developmental pathways anew, accounting for the striking similarity in complex melanin pigmentation patterns among unrelated species (Price and Pavelka 1996). In a series of recent studies, Prum and co-workers (Prum and Williamson 2001, 2002; Prum and Dyck 2003) showed that within-feather pigmentation is produced by coordination of several basic modules of feather growth and pigment uptake (see also Jiang et al. 1999; Smyth 2003), so that almost the entire observed diversity of within-feather coloration patterns can be produced by a modification of only a few regulatory interactions between feather growth and pigment-uptake modules. Whereas phenotypic expression of each of these modules is context-independent, the regulatory interactions between them are mostly caused by diverse epigenetic and condition-dependent interactions, such as resource partitioning (Worley et al. 2003; Badyaev and Young 2004). Because such interactions are often diverse, novel, context-dependent, and non-additive, it is difficult for selection to accomplish their modification (Wagner and Mezey 2004). For example, artificial selection of poultry morphs with a goal of repeatable co-expression of a particular combination of pigmentation and feather patterns requires careful and lengthy breeding protocols that focus specifically on elimination of context-dependent and epistatic interactions among feather growth and pigment-uptake modules (Bartels 2003;

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Smyth 2003). Similarly, in natural systems, sexual selection on maximum elaboration of color ornamentation acts, indirectly, on integration of developmentally distinct modules of plumage production by enhancing condition dependence in the relationships among modules (Badyaev et al. 2001; Badyaev and Young 2004). Finally, color patterns can result from hierarchical and temporal displacement and juxtaposition of several color-producing modules (e.g., carotenoid and melanin interactions at the level of follicle; Dickman et al. 1988; Maderspacher and Nusslein-Volhard 2003), although this mechanism is poorly studied in birds (Burtt 1986; Badyaev and Hill 2003). From the classical melanocyte transplant experiments to modern studies of sexual selection, the development and expression of melanin-based pigmentation in birds is often described as more modular in production and deposition than other sources of pigmentation, such as carotenoid-derived colors. Indeed, internally produced melanins can be incorporated into keratin in a highly structured fashion and often form complex patterns of plumage coloration (Jawor and Breitwisch 2003; Chapter 6, Volume 1; Plate 24). Moreover, transplants of melanocytes between embryos in poultry show that melanin synthesis and uptake is highly modular and host independent (e.g., Brumbaugh 1967). In the same breeds of poultry, however, the accumulation and distribution of melanin in follicles and feather tracts and the uptake of melanin into feathers are often regulated by complex signaling of hormones (e.g., estrogen, thyroid hormone, testosterone; George et al. 1981), as well as the effects of nutrition and temperature (Hutt 1949). Thus, in these cases, the development of melanin-based colors is modular, whereas its final expression varies across physiological and environmental contexts. For cases of nonmodular development of melanin-based pigmentation see Badyaev (2004b). Whereas in the majority of cases, melanin-based coloration is produced by flexible and diverse interactions of genetic and developmental mechanisms (Barsh 1996, 2001), there are several examples of nearly complete modularity across levels of genetic encoding, development, and phenotypic expression of melanin-based coloration. Because the population genetics’ assumption of a linear and accurate representation of genotype in phenotype is satisfied in these exceptional cases, evolutionary theory can provide adequate explanations not just for the maintenance of the resulting morphs at the population level, but also for their evolutionary dynamics (Price and Bontrager 2001; Hoekstra and Price 2004). But such “textbook examples” are often the only examples; most gene and environment products involved in color development interact in complex and nonlinear ways, and the linear phenotype-genotype

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representation is, most likely, a highly derived product of external selection (von Dassow and Munro 1999; West-Eberhard 2003). In many taxa, allelic variation in the MC1R receptor gene acts as an on-off switch determining the deposition of melanin in the follicle, and several point mutations in this locus have been associated with cases of naturally and artificially selected color polymorphism. In wild birds, point mutations in MC1R lead to development of distinct plumage coloration in Lesser Snow Geese (Chen caerulescens), Parasitic Jaegers (Stercorarius parasiticus), and Bananaquits (Coereba flaveola; Theron et al. 2001; Mundy et al. 2004; Plate 28, Volume 1; Plate 26), where the phenotypic effects of such mutations are under strong sexual and natural selection. Generally, a mutation can be expressed at the level of phenotype (and thus become visible to selection) only if the phenotype can produce it (Arthur 2004; Figure 8.3). This, in turn, depends on a mutation’s utilization of existing developmental routes—witness the major pleiotropic effects of many color mutations (Merat 2003; Somes 2003; Keeling et al. 2004)—as well as its ability to generate novel developmental pathways (Figure 8.3). In most cases, selection for the fixation of phenotypic expression of a mutation is very slow, not only because of the exceptional rarity of such mutations, but also (and mostly) because the developmental pathways by which such mutation is expressed differ among individuals, making selection ineffective. Thus, the key to the persistence of the MC1R mechanism across species might be a combination of its high mutability and a remarkable absence of pleiotropic effects (i.e., modularity in development and expression;

Figure 8.3. Conceptual illustration of within-generation interactions between novel and “inherited/existing” (here meaning either inherited by an organism or constructed at prior stages) components of color production at acquisition/encoding, development, expression, and display stages. (a) Default state. Appearance of a novel element at a lower level (e.g., genetic mutation, inclusion of novel environmental component) can be expressed and transferred to the upper level only if it can be accommodated by existing developmental pathways. Because of the complexity of developmental cascades, different phenotypes will transmit and express the effects of a novel element or mutation differently and by different developmental pathways, lowering the likelihood of its exposure to selection and evolutionary retention. (b) A major mutation of high developmental penetrance or a novel external element can construct novel color production directly, which will maximize both the chances of expression of a novel element and similarity of its expression among phenotypes. (c) Appearance of a novel element at the base level can influence existing pathways at the later stages that can express it with relatively small distortion and high similarity among phenotypes.

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Figure 8.4. Conceptual illustration of the evolution of modularity within and across three production levels—development (signified by d1, etc.), expression (e1, etc.), and courtship (c1, etc.)—along four consecutive generations (t to t + 3). Within each generation, all production stages can incorporate elements of the environment (x1, etc.) and are subject of external selection on courtship (Sc ), on color expression (Se ), and on color development (Sd ). At generation t, the phenotype is a nonmodular, patterned structure with developmental incorporation of x1 (e.g., pigment precursor) at the stage of development, x2 (e.g., social interaction affecting hormone levels, precursor of feather structure) at the stage of expression, and x3 (e.g., ambient light, background color for display) at the stage of courtship. Sc (t) acts indirectly on the most efficient incorporation of environmental elements into production of color. Because phenotypic expression of the courtship stage at generation t could influence Sc at generation t+1 (e.g., via sexual imprinting, the sensory drive process, or cultural inheritance), Sc (t) will have an indirect effect on the most efficient incorporation of x2 and e1 into production of c1 (e.g., formation of a module that combines the effect of the external environmental cue for breeding with selection of the most favorable lighting in which to display). Therefore, c1(t + 1) will have independent fitness consequences and Sc (t + 1) can act on the efficiency of producing c1, whereas Se (t + 1) will have an indirect effect on the efficiency and reliability of incorporating x1(t + 2) into d1(t + 2) because of correlation between x1 and x2, which is now a part of the expression module and because of the dependence of Sd , Se , and Sc within each generation; dashed arrows. At generation t + 3, x1, x2, and x3 are reliably incorporated at corresponding levels; the context independency of the resulting modules is assured by direct interactions between levels, their functional independence (being subject to Se ), and limited interactions with the elements outside modules at each level.

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Ling et al. 2003; Mundy et al. 2004). Interestingly, the MC1R-produced modular polymorphisms only involve cases in which (1) melanin is distributed across most of the plumage area of a bird in an all-or-nothing pattern, (2) deposition of melanin is not coordinated with complex and variable interactions with feather structure, and (3) there is no age-dependency in color expression. In all other cases—for example, when melanin-based coloration involves parts of plumage involved in different functions (e.g., when plumage areas form the distinct functional modules for prey flushing and sexual displays in Phylloscopus warblers; Marchetti and Price 1997)—selection favors diverse genetic and developmental mechanisms of melanin deposition (Hoekstra and Nachman 2003; MacDougall-Shackleton et al. 2003; Doucet et al. 2004). Carotenoid-based pigmentation differs from other types of pigmentation in that most of its components have to be obtained from the environment (e.g., consumed during foraging, delivered by parents during feeding, supplied with the yolk of eggs; Slagsvold and Lifjeld 1985; Hill 1992; Surai 1998; Fitze et al. 2003). Thus, all else being equal, early incorporation of externallyderived carotenoid components into an ornament’s developmental pathways should lead to diverse ways by which individuals and species proceed with development of carotenoid-based colors, thereby resulting in greater individualand condition-dependency of such ornamentation (Badyaev and Hill 2000; Badyaev et al. 2002; Chapter 12, Volume 1; Chapter 4; Figures 8.3 and 8.4). In theory, environmental variation in the availability and type of carotenoid precursors, as well as the diversity and complexity of developmental cascades of carotenoid metabolism, should prevent easy formation of modularity in carotenoid acquisition and development (but not in the expression; see below). Yet evidence suggests that, in the absence of selection causing and maintaining condition dependence in development, and under selection favoring the most efficient acquisition of color displays, evolutionary modularity evolves readily even in carotenoid-based ornamentation (Badyaev and Snell-Rood 2003; Badyaev 2004b). In some species, direct and thus condition-independent phenotypic expression of acquired carotenoids results from the inability of developmental systems to recognize them. Such is the case of novel pigments from fruits of introduced ornamental shrubs appearing in the diet and coloration of Cedar Waxwings (Bombycilla cedrorum; Plate 30, Volume 2; Mulvihill et al. 1992; Witmer 1996) or from synthetic pigments provided to birds in captivity (e.g., Hill and Benkman 1995). In other species, such direct and context-invariant

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alexander v. badyaev transmission is accomplished by evolved modular pathways of carotenoid development, storage, or expression, as is the case with carotenoid plumage of flamingos, tanagers, and bullfinches (Brush 1990; Stradi et al. 1997, 2001). The difference between species in the environment- and context-dependency of their carotenoid-based plumage is well illustrated in captivity, where closely related birds with diverse types of carotenoid plumage are often kept on the same diet. Some species (e.g., Common Rosefinch [Carpodacus erythrinus], Pine Grosbeak [Pinicola enucleator; Plate 25, Volume 1]) are sensitive to the loss of the usual carotenoid precursors in their diet and change their color after a single molt. Other species (e.g., Common Redpolls [Carduelis flammea], Eurasian Bullfinch [Pyrrhula pyrrhula]) are remarkably versatile in extracting or converting carotenoids and maintain species-specific carotenoid coloration for several molts (pers. obs.). Also crucial to this maintenance is the ability to store externally derived carotenoids, which gives individuals greater independence from the external environment and thus facilitates the formation of modularity in the acquisition and development of carotenoid coloration. Similarly, expression and courtship displays associated with plumage coloration often involve the close integration of distinct organismal functions (e.g., color production, motor functions) and external environment (e.g., background matching). At first consideration, one might suppose that evolutionary modules in color expression and behavior would be rare. However, two factors might favor the evolution of integration of color expression, behavioral displays, and components of the external environment. First, behavioral displays involve only late stages of color production and require fewer interdependent stages (Figures 8.2 and 8.3). Second, the higher fitness of optimum color displays often requires their co-occurrence with some aspects of behavior (e.g., Badyaev and Duckworth 2005), such as displaying a particular color under particular ambient light or in a certain pattern against a particular background (Gilliard 1956; Endler and Théry 1996; Uy and Endler 2004). When such selection on co-expression is strong and recurrent, it can result in evolutionary coupling (see below) of behavior, color expression, and plumage patterns. This process is evident in the transference of plumage display postures among different contexts within and among species (Andrew 1960), in the cases of genetic inheritance of patterns of color displays (Price 2002), in the remarkable evolutionary retention of behavioral syndromes associated with feathers despite the loss of feathers (Vestergaard et al. 1999), and in modification of feather microstructure for deposition of different carotenoid types in sister taxa (Hudon 1991). Finally, distinct external selection on components of color or plumage

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type can facilitate modularity in expression. Examples include cases in which feather tracks differ in the formation of fault bars in relation to strength of external selection on their functional significance (Burtt 1986; Fitzpatrick 1998; Aparicio et al. 2003; Jovani and Blas 2004), and when integration among developmentally distinct components of carotenoid-based coloration of House Finches (Carpodacus mexicanus; Plate 14) varies adaptively among populations, degrees of elaboration, and subsequent molts (Hill 1996; Badyaev et al. 2001; Badyaev and Duckworth 2003; Badyaev and Young 2004).

Selection on Modularity in Encoding, Development, and Expression of Color Displays Changes in the modularity in development require complementary effects of modifying integration both inside and outside of module components (Figure 8.2). For example, modularity in color production might be accomplished by duplication of elements or pathways (Figure 8.2a), by selection for linearity between elements at different developmental stages (Figure 8.2b), by eliminating or shortening developmental steps (Figure 8.2c), or by selection on intermediate modifiers that strengthen the relationship between elements of the module (Figure 8.2d; Badyaev 2004a). There are six general scenarios for selection on the modularity of color production. First, modularity across production stages is favored when selection acts on color expression only and when this selection is recurrent, stabilizing, and consistent across environments (e.g., selection maintaining taxa-specific color patterns or distinct, genetically-based color morphs within a species). Second, when selection acts on color expression only (e.g., predation; Plate 4), but such selection fluctuates among ecological or social environments, two patterns of modularity evolve: (1) selection can favor the evolution of a contextsensitive threshold that regulates expression of color produced by alternative developmental modules (Badyaev and Qvarnström 2002), or (2) selection can favor the evolution of complex sexual traits that consist of developmentally independent modules (Wedekind 1992; Moore 1997; Badyaev et al. 2001). Selection might favor modularity in expression when the same color pattern has functions in different contexts with distinct fitness consequences (Badyaev and Hill 2003), for example, when color pattern is used in both flush-pursuit foraging and sexual displays. Third, when selection is on color expression only, but is directional, it can act on the efficiency of color acquisition and development and will favor

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alexander v. badyaev modularity in both. For example, signaling functions of sexual displays are ensured by the costs of color expression and production (Andersson 1994). Selection for reduction of such costs will favor evolution of modularity in these stages (Badyaev 2004a). The combination of selection for reduction in color signal costs (e.g., within males) and opposing selection to restore condition dependency of color signals (e.g., by females) should result in the evolution of facultative and context-dependent expression of color displays or in evolution of complex displays consisting of several distinct modules (Hill 1994; Badyaev 2004a). For example, selection against modularity in sexual ornamentation can capitalize on developmental integration of feather growth and withinfeather pigmentation (Prum and Williamson 2002) by favoring the evolution of new color expression that indicates condition-dependent growth of feathers, such as selection for pigment markings to reinforce condition-dependence of elongated ornamented feathers (Fitzpatrick 1998). Fourth, when selection on color expression also acts directly on color acquisition and development, as does selection for condition dependency in sexual ornamentation, such selection will act against modularity in color acquisition and development, yet it might favor modularity at the expression stage. For example, consistent directional selection on the expression of carotenoid-based coloration in the absence of selection maintaining condition dependence in its production results in genetically inherited efficiency in extracting and storing carotenoids from carotenoid-poor environments (e.g., in modularity in carotenoid acquisition and development; Ryan et al. 1994; Craig and Foote 2001). However, in species in which external selection maintains conditionand environment-dependence in carotenoid expression, such expression is closely dependent on the local availability of carotenoids in the environment (i.e., strong context-dependency; Grether 2000; Hill et al. 2002). Fifth, the importance of cultural inheritance, sexual imprinting, contextdependency, and prior experience in determining the direction and patterns of future selection on sexual traits (Odling-Smee et al. 2003) favor modularity in the expression of sexual ornamentation, because such modularity enhances functional versatility. For example, the evolution of complex visual displays in bowerbirds is favored by context- and age-dependency of selection on the expression of such displays (Coleman et al. 2004). Finally, in the absence of consistent selection either on expression or on development (i.e., when the preferred color expression is not known from generation to generation), epigenetic developmental cascades (i.e., gravitation towards a particular state without a predetermined path; Sachs 1988) might be

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favored over modularity because such development provides the cheapest way of developing color patterns and displays. This possibility has not been studied in birds, but many selectively neutral changes in coloration (as in some island birds) that are often attributed to “genetic drift” (Peterson 1996; Badyaev and Hill 2003; Johnson 2003) might be due to this mechanism.

Evolution of Modularity in Color Displays: Constructing Ways with Inherited Means Selection on modularity in color displays is common and often favors coexpression of traits with distinct developmental histories and origins, for example, a combination of particular plumage colors, colorful items of environmental origin, and particular display behaviors. How can reliable and heritable associations among these traits evolve when, in isolation, each of these components would have no function? Most theoretical studies assume that phenotypic modularity evolves as a direct consequence of modularity at the level of genotypes—gene duplication or novel mutation facilitate the formation of novel developmental pathways and thus enable phenotypic modularity (Wagner et al. 1997; Wagner and Mezey 2000; Ohta 2003; Force et al. 2004). This is difficult to accomplish because the downstream development is usually novel and diverse among individuals, and its (often epigenetic) patterns are unpredictable from the level of the genotypic module (Wagner and Mezey 2004; Wagner et al. 2005). (Interestingly, strong directional selection on expression of a trait might facilitate proliferation of novel developmental pathways to produce the trait and thus lead to its lower heritability. Whereas this phenomenon is usually explained by the exhaustion of genetic variance and fixation of preferred trait appearance, it can also be due to increased variability of production). Moreover, even when one assumes a direct and linear relationship between phenotype and genotype, modularity is still highly unstable under fluctuating directional selection on the phenotype (Wagner and Mezey 2000). Clearly, developmental complexity plays a crucial role in maintaining the stability of phenotypic modules once they evolve. Yet developmental complexity and variability is considered to be the main obstacle to the evolution of modularity in the first place. This difficulty can be resolved if it is realized that all sources of organismal variation (Figure 8.1) are ultimately expressed by the same developmental pathways (Cheverud 1982) and have the potential to have the same effect on fitness (i.e., selection is insensitive to whether phenotypic variation is induced

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alexander v. badyaev environmentally, epigenetically, or genetically; Meiklejohn and Hartl 2002; Siegal and Bergman 2002). Some developmental pathways evolve under external selection for the most accurate or efficient expression, but others are related to cohesiveness, control, and regenerative functions of the developmental systems themselves (Schmalhausen 1949; Whyte 1965; Schlichting and Pigliucci 1998; Arthur 2004). These are subject to the environment-invariant and the final-expression-invariant internal selection, and it is complexity and canalization of these previously established (“pre-existing” sensu West-Eberhard 2003) pathways that produce stability and directionality in development (Sachs 1988; Jablonka et al. 1992; Waxman and Peck 1998). For example, Badyaev and Foresman (2000, 2004; Badyaev et al. 2005) found a nearly complete congruence of phenotypic and genetic variation in complex morphological characters, driven by selection-independent developmental patterns. Similarly, Ancel and Fontana (2000) showed that certain phenotypic patterns of RNA folding are particularly stable and less costly to produce, leading secondarily to genetic canalization of most adapted phenotypes. The same principle applies to the evolution of modularity in color displays (Figure 8.4). Within each generation, a color pattern of an individual is constructed by an array of interacting elements, some inherited (genetically, behaviorally, ecologically, or parentally), some not, operating at the levels of color encoding, acquisition, development, and expression (Figure 8.1). To the extent they have independent effects on fitness, these components and their functional associations at each developmental stage are influenced by external selection (Figure 8.4). Persistency and consistency of such selection favors stable configuration among elements (Figure 8.4). In turn, the extent to which such functional modularity can be accomplished, when favored, depends on the similarity and predictability of developmental processes among phenotypes in a population (Arthur 2002; West-Eberhard 2003). Selection favoring modularity within or among levels is the selection for linear, more additive relationships between components across developmental levels (Rice 2001; Figure 8.2). In turn, the complexity of developmental processes, through canalizing effects of previously formed structures, can lead to the appearance of a novel developmental pathway in many individuals simultaneously, which greatly facilitates its evolutionary persistence (Jablonka et al. 1992; Badyaev and Foresman 2004; Badyaev 2005a,b). This can eventually lead to its genetic assimilation either when the fitness of individuals possessing the pathway is higher or when the costs of phenotype production with the incorporated component are lower (Masel 2004; Palmer 2004; Rice 2004b; Badyaev 2005a).

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Interestingly, such “top-down” processes in the evolution of sexual displays are often, although implicitly, invoked in the studies of the sensory drive process. A sensory bias of the receiver initiates the selection for elaboration of sexual ornament of a signaler, with condition dependence in the development of such ornaments evolving secondarily under continuing selection for ornament elaboration (Schluter and Price 1993; Rowe and Houle 1996; Garcia and Ramirez 2005). Production of color involves the developmental incorporation of components of the external environment (e.g., pigments or display conditions). Such developmental “entanglement” (sensu Rice 2004a) between elements at different levels can generate novel developmental arrangements and can bias evolutionary change (Fusco 2001; Salazar-Ciudad et al. 2001; Rice 2004a; Badyaev 2005b). When external selection acts on the co-occurrence of distinct developmental elements or when it acts on the efficiency of incorporating environmental components, it can have an effect on these developmental processes (Masel 2004; Rice 2004b; Figures 8.2 and 8.4). The developmental entanglement of inherited and noninherited components of color production (e.g., integration of a consumption of a certain carotenoid and the feather structure required for its expression, integration of color pattern and display behavior) can lead to their genetic canalization and coinheritance (i.e., evolutionary modularity; Fuller and Travis 2004; Palmer 2004; Rice 2004a). In some interesting cases, inclusion of the external environment influences both the development of the phenotype and selection on the phenotype simultaneously (Ryan et al. 1994; Sockman et al. 2002, 2004; Badyaev 2005a). For example, developmental incorporation of environmentally derived carotenoids into both integument coloration and the visual sensory system is important for development of both red plumage and visual preferences for such plumage (Bowmaker et al. 1993). Once formed, the inheritance of complex color patterns that produce locally favored sexual signals depends on the transmission of an array of developmental resources necessary for reliable acquisition, development, and expression of its components across generations. Thus, crucial to the understanding of the evolution of sexual displays is the notion of plurality of inheritance systems, when the wide array of developmental resources and conditions transferred between generations enables similarity in developmental processes and phenotypes (Oyama 2000; Jablonka 2001). Moreover, behavioral inheritance and parental imprinting set the stage for the direction of selection in the next generation (Lewontin 1983; Wolf et al. 1998; Odling-Smee et al. 2003; Wolf

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2003). For example, offspring preferences for sexual displays are often largely determined by parentally imprinted or learned local dialects and local, often artificial, appearances (Cate and Bateson 1988; Irwin and Price 1999; Sockman et al. 2002; Madden et al. 2004). Similarly, learned preference for certain foods can be crucial to acquisition of species-specific precursors of pigments, whereas learned preference for habitat features of display arenas can facilitate reproductive success (e.g., Cushing 1944). Moreover, sexually imprinted and genetically encoded traits can co-evolve and jointly determine predisposition to species-specific color displays and courtship patterns (Lachlan and Slater 1999; Rice 2004b). The interaction between behaviorally and genetically inherited preferences plays an important role in the evolution of genetic predisposition to displays that indicate local function versus displays that indicate species -specificity (Lachlan and Feldman 2003). Such interaction can explain the contrasting results of studies showing open-ended (Ryan et al. 2003) versus species-specific (Hill and McGraw 2004) preferences for the elaboration of condition-dependent sexual displays.

A Final Note As I am writing this page, a bright magenta male Pyrrhuloxia (Cardinalis sinuatus; Plate 25) from my study population leads his three fledglings from one Prickly Pear Cactus (Opuntia) to another, feeding them pieces of red fruits outside my window. His fledglings acquired their red ornamentation while in the nest, with parents providing all the carotenoid precursors for their current plumage, some of which will be retained for their first breeding. As the fledglings follow the male, begging and waiting for food, they try to open the fruits on their own, learning both the appropriate sources of carotenoid precursors and the ways to find and acquire them—that is, learning both the problems and the solutions to the problems that existed in prior generations. The fledglings’ imprinting on their parents’ plumage phenotype not only results in species-specific affiliations—the fledglings do not mix with a large brood of Northern Cardinal (C. cardinalis; Plate 25) fledglings feeding with their parents on the pollen of the saguaro flowers nearby—but also sets the stage for their future preferences for sexual displays. It is hard to disagree that, in this case, developmental resources, behaviors, and preferences that are transferred across overlapping generations are at least as important to the production of offspring color display and shaping selection on this display as are the offspring’s inherited genes. It is also clear from their current plumage color that

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the young Pyrrhuloxias vary in how their developmental systems are utilizing these acquired and inherited resources to construct their phenotypes. To understand the evolution of color displays and to guide our empirical studies, we need a new conceptual framework that integrates explicitly the production of the phenotype within a generation with its change between generations.

Summary The conventional interpretation of the modern evolutionary synthesis states explicitly that internal organismal factors (e.g., genes) that cause variation operate independently of external factors (e.g., selection) that delete or retain these variants. It has long been noted that such thinking skips a crucial step in organic evolution—the actual production of phenotype—and, as such, separates the causes of within-generation variation from the causes of among-generation variation. Very much alive is the general notion that Darwinian evolution requires a strict separation and independence of pre-existing (inherited) form and created (acquired) form. The result is that fascinating scientific advances in our understanding of developmental processes and molecular mechanisms co-exist currently with embarrassingly vague notions about the origin of these forms, the nature of deterministic forces in development, and, most importantly, the origin of genes. I suggest that studies of animal coloration are uniquely suited for a novel evolutionary synthesis that integrates the origination, maintenance and evolution of traits. I review the literature on avian coloration and build a conceptual framework that traces an evolutionary sequence from environmental induction of developmental plasticity, through phenotypic and genetic accommodation facilitated by developmental complexity and extended inheritance, to the evolution of genes and genetic inheritance as guarantors of the most recurrent and consistent organism-environment interactions. The ultimate reward of such a framework in relation to animal coloration, if successful, would be the answer to the foundational question of organic evolution—how to reconcile persistent within-species continuity in the development of displays with an origin of striking diversity in displays among species.

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9 Ecological Explanations for Interspecific Variability in Coloration ian p. f. owens

The striking variation in color among bird species is a classic biological puzzle and has played an important role in stimulating ideas in evolutionary biology and ecology (e.g., Darwin 1871; Wallace 1889; Huxley 1942; Lack 1968; Andersson 1994; Zahavi and Zahavi 1997; Maynard Smith and Harper 2004). Why are male and female Mallards (Anas platyrhynchos; Plate 15) so different from one another with respect to plumage that they were originally classified as different species, whereas in many species of seabird, the plumage of the two sexes is almost identical? And why do finches make such abundant use of bright yellows and reds and oranges, whereas sparrows and buntings predominantly display browns and blacks? Avian color diversity is not only remarkable in its extent, but also in the many forms that it can take. Such diversity offers an ideal opportunity to understand the origins and maintenance of diversity. The overall aim of this chapter is to review ecological explanations for color variation among avian species. Because my focus is on hypotheses for interspecific variation per se, I make frequent use of comparative analyses. I chose this approach not because traditional empirical studies say nothing about diversification, but because they are limited in their ability to differentiate between competing hypotheses. Empirical studies are typically limited to making comparisons between just two species or two populations, and although the

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suggested ecological explanation for the difference between the species or populations is often plausible, there are usually insufficient degrees of freedom to take the argument any further (Garland and Adolph 1994). In this review, I therefore focus on those studies that have included a sufficient range of taxa to be able to perform statistically robust tests of competing hypotheses.

Are Comparative Analyses Valid? It has been claimed that, in comparison with experimental methods, the comparative approach tells us very little about evolutionary processes (e.g., Leroi et al. 1994). By focusing on large comparative analyses, I am not claiming that the experimental method is flawed or that the comparative approach is perfect. As Bennett and Owens (2002) discussed at greater length, the experimental method is ideally suited to testing hypotheses about current function. For instance, experimentally manipulating the black chest plumage of male sparrows is an excellent way of testing whether such plumage does indeed affect agonistic interactions. The trouble is that not all research questions involve current function. Would it be possible to do an experiment to test why sparrows appear to use their black chest plumage, rather than using tail length, as a signal in agonistic interactions? Or to experimentally test why sparrows appear to use melanin-based chest plumage, whereas cardueline finches use carotenoid-based colors? Such experiments would be difficult for two reasons —first, the question relates to events that have happened in the evolutionary past rather than events that are happening in the present, and second, the questions relate primarily to diversity among species rather than function within a single species. For these types of questions, the experimental approach is relatively weak. In contrast, the comparative approach is relatively poorly suited to tackling questions about current function and relatively well suited to tackling questions concerning evolutionary history and interspecific diversity. It would be straightforward, for instance, to use a comparative approach to test for ecological differences between species that used color as signal and species that used tail length, or between species that used melanin- versus carotenoid-based signals. Such comparative analyses could not unambiguously prove which factors led to color variation among species, but they could certainly test the relative likelihood of different hypotheses. It is because of this utility in exploring interspecific diversity that I make such extensive use of comparative analyses in this chapter.

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Methods in Comparative Analysis Considerable debate exists over the best way to perform comparative analyses. The two core questions are, first, whether (or when) is it necessary to account for phylogenetic relationships among species, and second, how best to incorporate phylogeny when such a procedure is necessary. These debates have been thoroughly reviewed elsewhere (e.g., Harvey and Pagel 1991; Price 1997; Harvey and Rambaut 2000; Martins 2000), so I do not go into details here. Instead, the important point to note for this review is that I have attempted to include all studies, irrespective of the exact comparative methodology they have used. I have not, therefore, excluded studies that based their analyses on raw species data, rather than using one or more method(s) to incorporate phylogenetic information (e.g., higher taxon comparisons, using matched pairs or independent contrasts). However, in most cases, I have drawn attention to results if they are supported only by nonphylogenetic analysis. This emphasis reflects my general approach that, because it is often difficult to identify the perfect method of comparative analysis, it is prudent to check important biological results using more than one method.

What Aspects of Plumage Coloration? Given the enormous number of ways that bird species differ from one another with respect to coloration (e.g., patterns, biochemical/structural mechanisms), what aspects should be included in this review? Rather than attempt to cover every aspect of color variation and every comparative analysis that has ever been performed on bird coloration, I have chosen to focus primarily on three aspects of variation—sexual dichromatism, delayed plumage maturation, and coloration itself. Each of these aspects was chosen for a different reason. Sexual dichromatism is a hot topic in behavioral ecology and has been the subject of a great deal of work. I therefore think it is a good showpiece for comparative biology. Delayed plumage maturation is an old question but one that deserves new attention in phylogenetic contexts. Why different species have different types of coloration (e.g., melanin versus carotenoid pigmentation versus structural coloration) and different manifestations of display within a color type (e.g., red versus yellow, many colored feathers versus few colored feathers) are, I believe, the next big questions in understanding plumage diversity.

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Although the main body of this review focuses on these three aspects of avian coloration, I have also included a section on other aspects of coloration. In this section, I briefly discuss a number of other aspects of plumage coloration that are of interest from a comparative perspective (e.g., color types, polymorphisms, bare-part coloration), but space does not allow a fuller treatment. They are included, albeit briefly, to encourage further work in those areas.

Sexual Dichromatism The study of sexual selection dominated the field of behavioral ecology throughout the 1990s. It is not surprising, therefore, that there have been a number of excellent reviews on the evolution of both sexual dimorphism in general, and sex-specific coloration in birds in particular (e.g., Andersson 1994; Savalli 1995; Ligon 1999; Badyaev and Hill 2003). Given this previous effort, is it worth using sexual dimorphism as one of the major examples in this review of interspecific diversity in coloration? I believe that it is for two reasons. First, those previous reviews were typically aimed at understanding the function of sexual ornaments rather than explaining diversity in ornaments across species. Previous reviews therefore tended to focus on the adaptive function of particular plumages rather than ask why different species have different plumages. In contrast, I dwell almost exclusively on the question of interspecific diversity. Second, because sexual selection has been such a touchstone for behavioral ecological research, there has been an enormous number of studies on the ecological correlates of sexual dichromatism. Reviewing the literature on comparative studies of sexual dichromatism provides, therefore, an unusual opportunity to see what the comparative approach can achieve. Mating System, Extra-Pair Paternity, and Parental Care Although measuring the strength of sexual selection is notoriously controversial, many studies have attempted to test for an association between various indices of sexual selection and sexual dimorphism. The traditional method of measuring interspecific variation in the strength of sexual selection is to categorize species on the basis of their social mating system as being either socially monogamous or socially polygamous (e.g., Lack 1968; Møller 1986; Davies 1991; Ligon 1999). Using this approach, there has been a substantial number of tests of the links between social mating system and sex differences in both

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ian p. f. owens size (Höglund 1989; Björklund 1990; Oakes 1992) and color. The classic early study on avian color variation was by Crook (1964), who showed that, among African weavers, socially polygynous species were more likely to be sexually dichromatic than were socially monogamous species. It was this study that influenced David Lack so deeply and subsequently was to form a cornerstone of Lack’s Ecological Adaptations for Breeding in Birds (1968), which is still often cited as the primary evidence for co-variation between social mating system and plumage dichromatism in bird species (see also Verner and Wilson 1969). The evidence is, in fact, more complex. Although it is true that several studies have succeeded in finding a significant association between interspecific variation in social mating system and sexual dichromatism (e.g., Scott and Clutton-Brock 1989; Dunn et al. 2001), there is another body of studies that failed to find such a relationship (e.g., Møller 1986; Owens and Hartley 1998; Figure 9.1). Why have different studies produced such different results for such an apparently simple analysis? The answer is not as simple as “it only works in certain taxonomic groups,” or “it requires a large sample size to detect a significant effect,” because these characteristics do not predict whether a significant association is found between mating system and sexual dichromatism. Instead, Badyaev and Hill (2003) have suggested that the studies that are most likely to detect a significant relationship are those that define social mating system on a very detailed scale and in which the index of sexual dichromatism does not confuse different aspects of coloration. I think this is a key insight and, although there are too few comparative studies to conduct a formal metaanalysis, it explains the pattern well. My current belief, therefore, is that there is a general relationship between sexual dichromatism and social mating system, but that it is not straightforward, because other factors can also affect dichromatism and, to make things worse, some of those co-factors may co-vary with social mating system. So what are the other factors that may confuse the relationship between social mating system and sexual dichromatism? One obvious source is the existence of alternative reproductive strategies, such as extra-pair paternity, which are not included in traditional definitions of social mating systems. The application of molecular methods to avian breeding systems has revealed enormous variation among species in the incidence of extra-pair paternity (reviewed in Bennett and Owens 2002; Griffith et al. 2002), and it has been suggested that it is this variation that may explain some of the more prominent anomalies in the relationship between dichromatism and mating system (Harvey and Brad-

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Figure 9.1. Interspecific associations between sexual dichromatism and social mating system (Kendall’s tau = 0.07, p > 0.90), sex differences in the extent of brood provisioning by parents (tau = 0.34, p < 0.0001), and the incidence of extra-pair paternity (tau = 0.70, p < 0.0001). Plumage dichromatism was scored from 0 (monochromatic) to 10 (maximally dichromatic); social mating system as 0 = social monogamy, 1 = occasional polygamy, 2 = regular polygamy, and 3 = obligate polygamy; sex bias in brood provisioning as 0 = both sexes contribute equally, 1 = both sexes care but one sex provides more care than the other, 2 = one sex usually cares alone with only occasional help from the other sex, and 3 = obligate uniparental care from one sex; and frequency of extra-pair paternity as the percentage of offspring fathered by a male outside the social pair or group. Area of dots is proportional to the number of overlapping data points, with the smallest dot size representing one data point in each case. Redrawn from Owens and Hartley (1998).

bury 1991). Many socially monogamous species show striking sexual dichromatism, for instance. Could this be because, in such species, sexual selection remains strong, despite social monogamy, because males differ greatly in their success in obtaining extra-pair copulations? Comparative tests have generally supported this idea, with interspecific variation in the extent of sexual dichromatism being positively associated with interspecific variation in indices of the incidence of sexual selection via sperm competition (Møller and Birkhead 1994; Owens and Hartley 1998; Dunn et al. 2001; Figure 9.2). Moreover, the relationship seems reasonably robust with respect to the exact measure of sperm competition employed—it remains intact whether the index is based directly on the proportion of offspring fathered through extra-pair paternity (Møller and Birkhead 1994; Owens and Hartley 1998) or indirectly through relative testis size (Dunn et al. 2001; Figure 9.3).

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Figure 9.2. Sexual dichromatism in birds in relation to social mating system. Plumage dichromatism was scored from 0 (monochromatic) to 10 (maximally dichromatic). Species data are used to show plumage dichromatism in relation to social mating system, whereas independent contrasts were estimated assuming both gradual and punctuated models of branch length evolution. Species graph shows means + standard errors and sample sizes to the right of each bar. Redrawn from Dunn et al. (2001).

Another factor that complicates interspecific relationships between social mating system and sexual dichromatism is parental care. The link between social mating system and parental investment is particularly strong in birds, with a series of comparative studies having shown that social polygamy is most common in species with reduced parental care (e.g., Owens and Bennett 1997). But is interspecific variation in parental effort also associated with the extent of dichromatism? Again, the available comparative evidence tends to support this idea, with dichromatism being particularly common in those species for which there is a large sex difference in care, usually attributable to males providing rather little care (e.g., Verner and Wilson 1969; Scott and Clutton-Brock 1990; Owens and Hartley 1998; Soler et al. 1998). Once again, the association appears to be largely robust with respect to the aspect of parental care studied and the exact form of comparative analysis (but see Dunn et al. 2001). The relationship between sexual dichromatism and breeding ecology is therefore a complex one, involving interspecific diversity in social mating systems, alternative reproductive strategies, and the amount of parental care.

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Parasites and the Hamilton-Zuk Debate Parasites and parasite resistance have played a special role in the debate concerning the evolution of avian coloration in general, and explanations of interspecific variation in sexual dichromatism in particular. Historically, this special role arose because, when Hamilton and Zuk (1982) advanced their famous hypothesis that parasites mediate the relationship between genetic quality and sexual ornamentation, they used bird coloration as their primary example. Moreover, in the absence of data on the intraspecific link between parasite resistance and color, they used an interspecific analysis to test for a relationship between parasite abundance and plumage “showiness” in North American passerine birds. As predicted by their new theory, Hamilton and Zuk (1982) reported that male plumage showiness was greater in those species that appeared to harbor a greater variety of blood-borne parasite species (Figure 9.4). The subsequent reaction to Hamilton and Zuk’s (1982) comparative analysis reads like a microcosm of the wider debate regarding comparative analyses in the mid- to late 1980s. Hamilton and Zuk’s original paper was published at a time when it was still relatively commonplace to use raw species values in comparative tests, and this is exactly what they did. Over the next few years, however, a series of key papers were published that unambiguously identified the potential weaknesses of treating species as independent data points (Ridley 1983, 1989; Clutton-Brock and Harvey 1984; Felsenstein 1985; Grafen 1989). Given the high profile of the Hamilton-Zuk hypothesis during these years, it is not surprising that Read (1987) chose to repeat Hamilton and Zuk’s (1982) original analysis, but this time used mean generic values as independent data points and multivariate analyses to control for potentially confounding variables. Using Hamilton and Zuk’s (1982) original data on interspecific variation in plumage showiness and parasite abundance in North American passerines, Read’s (1987) new analyses showed that the positive association between male plumage brightness and parasite abundance was not an artifact of phylogenetic nonindependence and did not appear to be the result of an obvious third variable, such as body size. In addition, Read (1987) compiled a comparable dataset on European bird species and showed that the same basic patterns appeared to hold in that group as well. The phylogenetic reanalysis of the raw data therefore supported the original nonphylogenetic analysis (see also Read 1988). The story changed dramatically in 1989 when, in collaboration with Harvey, Read published a second reanalysis of the Hamilton and Zuk study (Read

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Strength of association Figure 9.4. Distribution of measures of the strength of the association between display characters and the incidence of blood parasites in North American passerine birds. The upper three graphs show the patterns for male brightness (MBR), male song (MS), and female brightness (FBR). The lower two graphs illustrate male showiness (male brightness + male song) and bisexual brightness (male brightness + male song + female brightness). In each case, the null hypothesis of no relation between display characters and parasite prevalence predicts a normal distribution with mean of zero. All of the mean values are significantly greater than zero (for MBR and FBR, p < 0.05; for MS, p < 0.01; and for both MBR+MS and MBR+MS+FBR, p < 0.0001). The symbol over each distribution shows the observed mean ± standard error. Redrawn from Hamilton and Zuk (1982).

and Harvey 1989a). This time, as well as controlling for phylogenetic independence and confounding ecological factors, Read and Harvey (1989a) had collated a new set of data for plumage brightness, which were from six independent observers that were naïve of the hypothesis being tested. The results were different in several respects. Most importantly, for the North American species that Hamilton and Zuk (1982) had investigated, there was no longer a general positive relationship between male plumage showiness and parasite abundance (see also Johnson 1991). Intriguingly, Read and Harvey (1989a) did find such a positive relationship in the parallel analysis they performed on

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ian p. f. owens a database on European bird species, but here again there was a problem. The pattern for the European species was due to the inclusion of a small number of species that had been surveyed for parasites only very rarely; once these poorly surveyed species were removed, the positive association was no longer present. In the subsequent exchanges in the pages of Nature, Hamilton and Zuk (1989) and Read and Harvey (1989b) debated the relative merits of each others’ scoring methods and other fundamental philosophical issues, such as whether one- or two-tailed tests are most appropriate under these circumstances. The biological issues are quickly lost in this sort of exchange, but it is fair to say that, whatever the truth about Hamilton and Zuk’s core idea that parasites play a key role in sexual selection, Read and Harvey’s (1989a) analyses showed that the interspecific relationship between sexual ornamentation and parasite abundance is far more complex that originally proposed (see also Pruett-Jones et al. 1990). Even in the best case scenario, the relationship appeared to be idiosyncratic rather than general. The debate concerning the Hamilton and Zuk comparative analyses no longer dominates the pages of the leading international journals, perhaps because it is now broadly recognized that comparative analyses alone cannot test the core idea that well-developed sexual ornaments reflect the bearer’s genetic predisposition to parasite resistance (Read 1988). Nevertheless, in the context of this chapter, in which the emphasis is on the ecological variables that may explain interspecific variation in avian colors, it is still relevant to know whether differences in the parasite fauna of species are indeed associated with differences in sexual dichromatism. Related to this question, an important development is the more recent study by John (1995), who, like Hamilton and Zuk (1982), investigated blood parasites and plumage showiness in North American passerines, but used modern phylogenetic methods and excluded species for which there was insufficient parasitological information. John (1995) also analyzed the color of different body regions separately, arguing that birds are more likely to use ventral plumage in sexual displays. Using this approach, he found that, when all species and body regions were lumped together in the same analysis, there was no robust association between male coloration and parasite abundance. However, in these coarse analyses, John noted, first, that the relationships appeared to be stronger for ventral plumage, and second, that there was a complex correlation between the main variables under study—color and parasite load. John (1995) therefore repeated his analyses on socially monogamous species only and revealed a robust, significant, positive association between ventral plumage brightness and relative parasite presence. This analysis

Ecological Explanations for Interspecific Variability

is extremely revealing, as it agrees with Badyaev and Hill’s (2003) ideas regarding the relationship between mating system and sexual dichromatism. It also appears that this relationship is most likely to be found when factors are defined very carefully and great effort is made to ensure that like is being compared to like. In the case of John’s (1995) final analyses, for instance, it is noteworthy that interspecific variation in parasite abundance explained only about 10% of the overall variation in frontal plumage brightness of monogamous Nearctic passerines. This observation suggests that differences among species in parasite abundance are linked to plumage color diversity, but the relationship is far from straightforward, and several other factors are also involved. Natural Selection and Crypsis Theory predicts that the extent of sexual elaboration should be determined not only by the strength of sexual selection for display but also by the balancing strength of natural selection for crypsis. However, in contrast to the plethora of comparative studies that have tested for interspecific differences in the intensity of sexual selection, there has been a surprising paucity of studies examining the evolution of sex differences in crypsis. Perhaps this disparity is because human observers feel more confident scoring variation in the degree of ornamentation than they do in scoring variation in crypsis. If so, then the good news is that the development of new physiological models of avian vision now allows crypsis to be quantified from the perspective of an avian predator, and this quantification has been used to study the evolution of crypsis in Australian dragon lizards (e.g., Stuart-Fox et al. 2004), although not yet to study avian coloration. Given the lack of studies that explicitly attempt to explain differences among species in crypsis, our knowledge of the balancing role of natural selection on sexual dichromatism must be accumulated indirectly from studies of ornamentation. The core prediction concerning the balancing role of natural selection is that, if sex differences in the need for crypsis play an important role in determining interspecific variation in sexual dichromatism, then the extent of sexual dichromatism should be positively related to the extent of sex differences in the risk of predation. Or, in other words, sexual dichromatism should be most pronounced in species in which one sex experiences a much greater risk than the other sex, at least in taxa subjected to high predation risk. Testing these predictions is not trivial, because they require information on sex differences in mortality rates, which is rarely available (see Owens and Bennett

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ian p. f. owens 1994). One way in which the role of predation on the evolution of crypsis has been tested is to examine the association between nesting habit and sexual dichromatism. For instance, in a series of related studies, Martin and colleagues (Martin and Li 1992; Martin 1995; Martin and Badyaev 1996) have used comparative analyses to demonstrate convincingly that both nest height and nest location have an important effect on likely predation rates in passerine birds, with predation being higher in species that nest in open rather than in closed nests, and higher in species that nest at intermediate heights (in shrubs) rather than very low (on the ground) or high (in trees). Using this pattern, Martin and Badyaev (1996) were able to show that, although interspecific variation in male plumage color was not significantly associated with differences in predation risk, female plumage coloration was indeed closely linked to nesting habit. Female plumage was significantly more drab in those species that nested in riskier microhabitats, and this pattern was particularly strong in species in which the female was providing most of the parental care at the nest (e.g., incubation). As a result, interspecific variation in sexual dichromatism was also significantly associated with nesting habit (Martin and Badyaev 1996; see also Dunn et al. 2001; Figure 9.5). As predicted by the crypsis hypothesis, therefore, dichromatism is greatest when there is a big sex difference in the risk of predation (in this case, when females provide the majority of care at risky nest sites). Another line of evidence that suggests, albeit less directly, that sex differences in the strength of natural selection for crypsis affect the evolution of sexual dichromatism is the pattern of association between parental care and dichromatism mentioned in the earlier section on mating systems. To recapitulate, several comparative analyses have shown that dichromatism tends to be greatest in those species that show the largest sex differences in parental care (e.g., Sillen-Tullberg and Temrin 1994; Temrin and Sillen-Tullberg 1994, 1995; Owens and Hartley 1998). Because these comparative analyses have been performed on species with “conventional” (i.e., the female tends to provide more care and the male tends to have more showy plumage) rather than “reversed” sex roles, this observation shows that females are more drab in those species in which they provide relatively more care and therefore face a greater risk of predation (Owens and Bennett 1994). Coming from a different perspective, Badyaev (1997) has also reported that sexual dichromatism tends to be less pronounced in species living at higher altitudes, which he interprets as being due to such environments placing a greater requirement on substantial parental care from both the male and female parents. This scenario is sup-

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Figure 9.5. Associations between nest location and (a) nest predation (F = 6.9, n = 35, p = 0.0003), (b) male brightness (F = 9.5, n = 110, p < 0.0001), and (c) sexual dichromatism (F = 3.8, n = 110, p = 0.03) among bird species. Nest predation rate is measured as the proportion of nests that were depredated; plumage brightness is measured from 1 (dull) to 6 (bright) for each sex separately; sexual dichromatism is measured as the difference in plumage brightness scores between the sexes. Redrawn from Martin and Badyaev (1996).

ported by the additional observation that the negative association between dichromatism and altitude is largely powered by a reduction in male showiness at greater altitudes, which suggests that male plumage tends to become more female-like when the form of natural selection acting on the two sexes is very similar. Again, this idea supports the prediction that dichromatism is not

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only influenced by the extent of sex differences in the strength of sexual selection for elaboration but also by sex differences in the strength of natural selection for crypsis. What is now needed, however, is a multivariate comparative analysis that explicitly estimates the relative importance of sexual versus natural selection in determining interspecific variation in avian dichromatism, as has recently been performed for agamid lizards (Stuart-Fox and Ord 2004).

Delayed Plumage Maturation and Subadult Plumage Delayed plumage maturation (DPM) is the phenomenon in which younger individuals in a population, usually first-year males, do not adopt the elaborate nuptial coloration that is otherwise characteristic of their species and instead take on a drab appearance (reviewed in Rohwer 1975; see also Chapters 2 and 3). DPM is initially puzzling, because such males are not physiologically immature and, in later years, these individuals will typically develop adulttype nuptial color. From a comparative perspective, therefore, the question is why some species exhibit DPM, whereas in closely-related species, immature males molt without delay into showy nuptial plumage. Breeding Season Hypotheses The earliest quantitative comparative analyses of DPM was that by Rohwer et al. (1980). They collated a database on North American passerines and, as was typical of the early 1980s, used raw species values as independent data points. This pioneering analysis laid the groundwork for much of what was to follow, not only in terms of the North American passerine database, but also for large-scale ecological patterns. Rohwer et al. (1980) found that DPM was more common in species in which sexual selection was thought to be strong (e.g., sexually dichromatic, polygynous). These findings were interpreted as supporting the idea that DPM is most common in species in which there is intense reproductive competition among males. But why does DPM help young males cope with such competition? Rohwer et al. (1980) then went on not only to score whether species showed DPM, but also the extent to which the delayed male plumage resembled that of adult females. In other words, they scored interspecific variation in the extent to which young males resembled adult females. They found that, in species that showed DPM, young males tended to resemble females far more strongly than expected by chance. These researchers subsequently developed what has become known as the “female

Ecological Explanations for Interspecific Variability

mimicry hypothesis.” This hypothesis suggests that young males gain from delaying plumage development because their appearance fools adult males into treating them like females, thereby allowing young males access to females and/or other territorial resources. The female mimicry hypothesis was subsequently challenged by Studd and Robertson (1985), who used the original database on North American passerines of Rohwer et al. (1980) but restricted analyses to dichromatic species. This approach showed that DPM was also associated with large body size, and Studd and Robertson (1985) suggested that, given that large body size tends to be associated with a “slow” life-history in birds, DPM may, in fact, be just another manifestation of delayed reproductive investment in long-lived species. This conjecture was subsequently refuted by Montgomerie and Lyon (1986), who again used a version of the North American passerine database (Rohwer et al. 1980) and species as independent datapoints, but this time specifically collected data on longevity and found no robust association with the extent of DPM. Instead, Montgomerie and Lyon (1986) supported the original view of Rohwer et al. (1980) that species differences in DPM were due to differences in reproductive behavior and that interspecific variation in the extent of delay was associated with differences between species in the type of breeding territory. DPM was more common, Montgomerie and Lyon (1986) suggested, in those species in which the males and females foraged in groups away from the nesting territory, compared to those species in which males and females foraged in isolation in their own multipurpose territory. This finding was subsequently supported in an analysis that used mean genus values as independent data points (Lyon and Montgomerie 1986). It was interpreted as evidence for the importance of differences among species in the exact form of malemale competition in determining interspecific variation in the extent of DPM. Nonbreeding Hypotheses Although Rohwer et al. (1980), Studd and Robertson (1985), Montgomerie and Lyon (1986), and Lyon and Montgomerie (1986) presented different views on the relative importance of various factors in determining why some species showed DPM whereas others did not, they all tended to focus on factors concerning reproductive and territorial behavior during the breeding season. However, these passerine species also differ greatly in nonbreeding-season behaviors, especially in the extent to which individuals compete for resources, such as access to food. Could these differences in nonbreeding behavior also

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be important? Rohwer and Butcher (1988) compiled a database on the timing of DPM in birds and pointed out that, in those species in which young males adopt a subadult plumage, the subadult male plumage often disappears before the first full breeding season. Moreover, they could find no convincing cases of species in which subadult plumage specifically develops prior to the breeding season. As Rohwer and Butcher (1988) pointed out, this is a surprising pattern if the adaptive function of such plumage is to minimize the effect of male-male competition during the breeding season. Instead, it suggests that DPM, in some species at least, may be an adaptation for interactions that occur outside the breeding season. This suggestion that behavior during the nonbreeding season may play an important role in the development of DPM has recently been tested by Beauchamp (2003), who used a pairwise analysis on a taxonomically diverse range of bird families to test the relative roles of breeding and nonbreeding biology. Beauchamp’s (2003) phylogenetically controlled analysis confirmed many of the basic predictions of the breeding-season hypotheses, such as DPM being much more common in species with pronounced sexual dichromatism and unusual breeding systems, but it also identified a number of nonbreedingseason correlates. Of prime importance among these was winter flocking behavior, with DPM being significantly more common in species that feed in large nonbreeding flocks. This result strongly suggests that species differences in the adoption of subadult plumage by males is the result of differences in male competition, and that such competition can occur during the breeding or the nonbreeding season.

Color—Hue, Chroma, and Brightness In comparison with the multitude of overlapping studies that have investigated interspecific variation in sexual dichromatism and DPM, there have been rather few quantitative studies on the ecological basis of differences in coloration itself. So, although we have a reasonably good explanation for why such species as the Indian Peafowl (Pavo cristatus; Plate 8, Volume 1) and the Greater Bird-of-Paradise (Paradisaea apoda) exhibit dramatic sex differences in plumage color, we know much less about why males of these two species use such very different colors and color combinations in their nuptial plumage. Why should peacocks use such a range of iridescent colors and complex eye-spot patterns? Or, given that they have such extraordinary plumage modification,

Ecological Explanations for Interspecific Variability

why not use highly saturated yellows and reds that are so widely used among the birds-of-paradise? I suggest that the reason for this paucity of knowledge on the ecological basis interspecific variation in coloration has little to do with plausible hypotheses, of which there are many, and everything to do with the difficulties of comparing colors in a meaningful way. It is reasonably easy to score species for whether they appear to be sexually dimorphic, or whether they show DPM, but it is much harder to put a meaningful number on coloration. Fortunately, methods for scoring coloration have substantially improved in the past few years (Chapters 2 and 3, Volume 1). The widespread adoption by ecologists of spectroscopic methods of color measurement has allowed quantification of reflectance spectra (Endler 1990), and the development of physiological models of color vision has provided a framework for comparing those spectra (e.g., Vorobyev and Osorio 1998; Vorobyev et al. 1998). As yet, relatively few comparative tests have been performed on these sorts of data, but here I review the progress that has been made so far. Species Recognition The traditional explanation for color differences among closely related species is that such differences are an adaptation to aid in species recognition and thereby prevent harmful hybridization (see Wallace 1889; Huxley 1942; Mayr 1942, 1963; Grant 1965, 1975; Lack 1968). The key evidence that has been used to support this hypothesis is the occurrence of reproductive character displacement between sister taxa in areas of sympatry—the classic avian examples are Red-winged (Agelaius phoeniceus; Plate 11) versus Tricolored Blackbirds (A. tricolor), and Pied (Ficedula hypoleuca; Plate 27, Volume 1) versus Collared Flycatchers (F. albicollis; Plate 18; Hardy and Dickerman 1965; Orians and Christman 1968; Alatalo et al. 1994; Sætre et al. 1997). Despite the existence of these classic examples, there have been, until recently, very few quantitative comparative tests. It remains unknown, therefore, whether the Agelaius blackbirds and Ficedula flycatchers illustrate a general pattern, or whether such reproductive character displacement in coloration is idiosyncratic to a small proportion of bird species. The first quantitative comparative test of the species-recognition hypothesis in birds was recently performed by McNaught and Owens (2002), who compiled a database on Australian bird species. The hypothesis predicts that,

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if avoidance of hybridization is a major selective force in color evolution, color divergence should be greater between pairs of species living in sympatry than between pairs of species living in allopatry. To test this prediction, McNaught and Owens (2002) identified 20 sets of species trios, with each trio composed of two sets of matched pairs of closely related species. In each trio, therefore, there was a pair of species that lives in sympatry and a pair that lives in allopatry, with one species being in common to both pairs. They then used a combination of reflectance spectrophotometry to measure coloration and Endler’s (1990) method of calculating total Euclidean distance between colors to test whether sympatric pairs of species really were more divergent than matching allopatric pairs. The results did not confirm the predictions of the species-recognition hypothesis. In the majority of trios, the sympatric species were, in fact, more similar to one another than to the allopatric species (Figure 9.6). This was the case even when the analysis was restricted to those plumage regions of maximum contrast between sympatric pairs as well as for those areas used in display, and the same results were obtained irrespective of which analytical methods were used to quantify color variation. That the sympatric species were not more different from one other than expected by chance suggests that, among the Australian species examined by McNaught and Owens (2002), species recognition is not an important determinant of interspecific variation in plumage color. Light Environment and Habitat An alternative framework for explaining interspecific variability in coloration is that different species use different colors because they inhabit different light environments (e.g., Endler 1993; Marchetti 1993; Endler and Théry 1996; Zahavi and Zahavi 1997; Andersson 2000). Several authors have made explicit predictions concerning which colors are most suitable for use in which light environments, based on maximizing contrast against the background in the dominant ambient light environment (see Endler 1993; Marchetti 1993; Endler and Théry 1996; Zahavi and Zahavi 1997; Andersson 2000). For instance, in closed habitats, such as forests and woodlands, oranges and reds are predicted to be used in signaling because these colors reflect the long-wavelength light that dominates the ambient light spectrum in these habitats and contrast well against the surrounding vegetation (Endler 1993). Species that live in such closed habitats should have generally more reflective, or brighter, plumage than those species living in open habitats, because the

Ecological Explanations for Interspecific Variability

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Figure 9.6. Association between patterns of sympatry and extent of divergence in coloration, based on (a) all body regions (Wilcoxon signed-ranked test: z = 1.2, n = 20, p > 0.25), and (b) only those color regions of maximum contrast (z = 1.1, n = 20, p > 0.25). Data are the number of cases, out of 20 trios of bird species, that the most divergent pair of species had sympatric geographic distributions versus allopatric geographic distributions. Redrawn from McNaught and Owens (2002).

overall level of luminescence is lower in closed habitats (Marchetti 1993). Once again, however, until recently, there has been a notable lack of statistically robust comparative tests. One of the first quantitative tests of the light-environment hypothesis was performed by Marchetti (1993), who focused on Phylloscopus warbers, a genus of Old World leaf warblers. These warblers are typically rather drab in comparison with North American wood-warblers, but their enormous benefit for this type of study is that interspecific variation in plumage brightness can be scored unambiguously without the need for spectrophotometric measurement. This advantage comes about because, although the general plumage color of Phylloscopus warblers is a rather dull green, some species have brightly colored yellow patches on their head, wings, and rump (Plate 29), and these patches are used in displays. Marchetti (1993) was therefore able to quantify differences

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ian p. f. owens among species in plumage brightness by simply measuring the relative size of these yellow patches. Using this approach, Marchetti (1993) showed that differences in plumage brightness among species were indeed associated with habitat use and light environment—species dwelling in dark, closed habitats tended to have more bright plumage patches than did corresponding species from open habitats. This observation confirmed the core prediction of the lightenvironment hypothesis, that interspecific variation in coloration is linked to differences in the signaling environment. More recently, McNaught and Owens (2002) used reflectance spectrophotometry in Australian birds to test two predictions of the light-environment hypothesis: that species living in relatively closed environments should tend to make more use of long-wavelength colors, such as red and orange, than do those living is relatively open environments (Endler 1993); and that species in relatively closed environments should have plumage that reflects more light than those living in relatively open ones (Marchetti 1993). To test these predictions, McNaught and Owens (2002) collated reflectance spectra from the plumages of 20 matched pairs of species, each of which was one of a pair of closely related species, one of which lives in a relatively open habitat and the other in a relatively closed one. McNaught and Owens (2002) then again used Endler’s (1990) color-space concept to measure hue and brightness and tested whether there were consistent differences between closed- and open-dwelling species in these parameters. In general, the results supported the idea that the light environment is an important factor in determining interspecific variation in plumage color, with significant associations between patterns of habitat use and interspecific variation in both hue and brightness. In the case of the association between habitat use and hue, the relationship was in the direction predicted by Endler (1993), with species from closed habitats using colors that were more likely to be rich in long wavelengths compared to species from open habitats (Figure 9.7; Plate 28). This finding therefore agrees with the notion that plumage color is adapted to provide maximum chromatic contrast against backgrounds, taking into account ambient light conditions (see Endler 1993; Endler and Théry 1996). With regard to the association between habitat use and brightness, however, the direction of the relationship was the reverse of that found by Marchetti (1993), with species from closed habitats using colors that were less bright that those used by species from open habitats (Figure 9.7). This finding therefore agrees more with Zahavi and Zahavi’s (1997) prediction that species in open habitats should be more likely to use black and white plumage, because these spectra maximize contrast over long distances. The find-

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Figure 9.7. Association between habitat type (open versus closed) and coloration (hue and brightness), using analyses based either on all body regions or on only those body regions recorded as being used in courtship displays. Data shown are the number of cases, out of 20 pairs of bird species, that the species with the highest hue value, or highest brightness value, was from closed habitat versus open habitat. In each case, open and closed habitats were significantly different (p < 0.05, paired-circular tests). Redrawn from McNaught and Owens (2002).

ing therefore supports the notion that interspecific variation in plumage color may be an adaptation to differences in the distances over which signaling takes place (Zahavi and Zahavi 1997). It should be kept in mind, however, that an important difference between the study by McNaught and Owens (2002) and the earlier one by Marchetti (1993) is that McNaught and Owens (2002) measured parameters associated with the colors themselves, whereas Marchetti measured the relative size of bright patches of plumage. McNaught and Owens (2002) did not account for patch size in their comparisons. It seems likely, therefore, that the relationship between habitat use and plumage brightness may be rather complex, with the adoption of closed habitats perhaps leading to a general reduction in the brightness of the plumage but an increase in the size of a small number of highly reflective patches of plumage. Finally, the light-environment hypothesis has also received support from an extremely detailed test by Gomez and Théry (2004). Like McNaught and Owens (2002), they tested for an association between habitat use and plumage

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hue, but there were two novel aspects to their study. First, they quantified habitat in a far more detailed way than just open versus closed. Second, they noted that the light-environment hypothesis could be teased apart to give different predictions, depending on whether interspecific variation in coloration is primarily due to differences in the strength of sexual selection for signaling or differences in the strength of natural selection for crypsis. They argued that, if natural selection is the driving force, then species living in the understory should tend to be brown, whereas species living in the canopy should be green. But if sexual selection is the driving force, then species living in the understory should use yellow or red, whereas species living in the canopy should be use blue and ultraviolet (UV) wavelengths. In general, their results supported the scenario that interspecific variation in plumage hue appears to be matched to the needs of crypsis (Plate 28). The only robust exception to this was the frequent use of UV-reflective plumage by canopy-dwelling species, which would not be cryptic to avian predators and suggests a signaling function. In both cases, however, there was again evidence that light environment was closely linked to plumage coloration.

Other Aspects of Coloration Carotenoid- versus Melanin-Based Colors It has recently been suggested that there may be important differences in the control and function of carotenoid- and melanin-based coloration in birds (e.g., Badyaev and Hill 2000; McGraw and Hill 2000; Hill 2002; Jawor and Breitwisch 2003). Because birds must obtain carotenoids from their diet, whereas melanins can be synthesized de novo, carotenoid-based colors may be better signals of individual condition (reviewed in Lozano 1994; Olson and Owens 1998; Hill 2002; Chapter 12, Volume 1). Most comparative analyses performed to date have ignored such differences between carotenoid- and melanin-based patterns of coloration, perhaps because it is not always easy to distinguish among the different sources of pigmentation on the basis of color alone (McGraw et al. 2004). Nevertheless, by making the assumption that most highly saturated long-wavelength colors (e.g., bright red, bright orange, bright yellow) are most likely to be carotenoid based, whereas most blacks, browns, brick reds, and buff yellows are most likely to be melanin based, some analyses have attempted to explore the potential importance of pigmentation type in phylogenetic contexts.

Ecological Explanations for Interspecific Variability

One of the earliest studies of this type was by Gray (1996), who showed that carotenoid-based coloration appeared to be unusually closely linked to sexual dichromatism in many clades of North American passerines. From this, Gray (1996) went on to speculate that carotenoid-based coloration may play a special role in sexual communication because it has the potential to signal the health of the bearer. This is the conclusion also reached by Hill (1996) and Badyaev and Hill (2000), who both used cardueline finches as a model group to test the relative roles of different types of pigmentation in sexual dichromatism. Again, both studies found that interspecific variation in dichromatism was mainly the result of changes in carotenoid-based coloration, and Badyaev and Hill (2000) used a range of phylogenetic techniques to confirm that this observation was not an artifact of phylogenetic relationships. Instead, the explanatory role of carotenoid-based coloration appeared to be linked to its evolutionary flexibility, with the male plumage of closely related species being far more likely to vary with respect to carotenoid-based colors than with melanin-based ones (Badyaev and Hill 2000). A second approach that has been used to test for differences between carotenoid- and melanin-based pigmentation is to see whether the results of other comparative analyses change when colors are split up according to their likely pigment source. This is the approach used by Owens and Hartley (1998), who, as described in the earlier section on mating systems and sexual dichromatism, initially performed a general analysis to test for associations between sexual dichromatism and various aspects of breeding ecology (Owens and Hartley 1998). Subsequently, however, they scored sexual dichromatism separately for each source of avian coloration (carotenoids, melanins, and structural colors) and found that each source of coloration showed different associations with various aspects of breeding ecology (Owens and Hartley 1998). Again, this result supports the view that different sources of pigmentation may play very different roles in avian coloration, yet we still do not have a convincing general explanation for why different types of pigmentation are used in different contexts by different species. Most recently, Olson and Owens (2005) focused specifically on carotenoidbased coloration and tested the hypothesis that differences among species in the incidence of this aspect of coloration should be positively associated with the availability of carotenoids in the diet. They found that the strength of the interspecific relationship between carotenoid-based coloration and dietary carotenoids was dependent on the type of tissue and the color of pigmentation considered. The relationship between color and diet was most strong for

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red plumage coloration, which was strongly associated with a carotenoid-rich diet. The relationship was less strong for other colors of carotenoid-based plumage coloration, such as yellow, and was not significant at all for carotenoidbased coloration of the bare parts. Taken together, these results suggest that, even within a single type of coloration, there may be considerable variation in the ecological explanation for different uses of that coloration. UV Signals The realizations that avian plumage and bare-parts may reflect UV wavelengths of light (Burkhardt and Maier 1989) and that many species of birds are visually sensitive to UV light (reviewed in Hart 2001a,b), have prompted a rapid reassessment of avian signaling (reviewed in Cuthill et al. 2000). There is now strong evidence from behavioral experiments that many bird species use UV wavelengths as a cue during mate choice (e.g., Amundsen et al. 1997; Andersson et al. 1998), but from a comparative perspective, it remains unclear whether UV-based signals are of particular importance in sexual contexts. An early indication that UV wavelengths may play a special role in signaling came from the study by Owens and Hartley (1998), mentioned earlier in the context of carotenoid- versus melanin-based coloration. They divided sexual dichromatism according to whether it was due to carotenoid pigments, melanin pigments, or structural colors and then tested for associations with various aspects of breeding ecology. One of the more unexpected findings was a strong association between the extent of sexual dichromatism in structural colors and the strength of sexual selection, which was much stronger than the corresponding relationship for either carotenoid- or melanin-based colors. This observation led us to speculate that, because structural colors often reflect a high proportion of UV light, UV reflection may play a special role in sexual signaling. This suggestion was subsequently followed up in a study by Hausmann et al. (2002), who specifically tested whether UV reflection was unusually likely to be associated with sexual displays. They first used spectrophotometry to obtain reflection spectra from a wide range of Australian birds and then used those spectra to identify those body regions of each species that reflected UV wavelengths. They found that UV reflection was significantly more common in body regions that were actively moved or erected in sexual displays. Moreover, this relationship appeared to be specific to UV reflection, because when Hausmann et al. (2002) performed the same analyses on other wavelengths

Ecological Explanations for Interspecific Variability

(red and yellow), they found no significant association, and all of these patterns remained the same when they used higher-taxon comparisons to control for phylogenetic affinity. These results imply that UV reflection may well play a special role in sexual communication, but there is much yet to be discovered. For instance, although Hausmann et al. (2002) found a strong relationship between UV reflection and active sexual displays, a parallel study using the same methods found no association between UV reflection and sexual dichromatism (Hausmann et al. 2002, reported in Bennett and Owens 2002). In addition, the same methods failed to find a relationship between UV reflection and a range of other plausible ecological variables (Hausmann et al. 2002). A major comparative question therefore remains unanswered—why do some species use UV wavelengths whereas others do not? Color Polymorphism In addition to the well-recognized color differences between the sexes and between age groups, many species show what is known as “color polymorphism.” Color polymorphism is traditionally defined as the co-existence in a single population of at least two sharply distinct and genetically determined phenotypic morphs, in which the abundance of the least common morph is too great to be explained by recurrent mutation alone (e.g., Huxley 1955; Chapter 2). Well-studied examples with respect to bird coloration include the dark and light phases of the Lesser Snow Goose (Chen caerulescens; Plate 28, Volume 1), Arctic Skua (Stercorarius parasiticus; Plate 28, Volume 1), and Barn Owl (Tyto alba; Plate 29, Volume 1), but such phenotypic polymorphism is found in species from a huge range of birds families and is particularly common in such groups as the owls, hawks, and cuckoos (see Chapter 2). The striking form that plumage polymorphism takes in many species, coupled with its uneven phylogenetic distribution, has led to considerable speculation concerning its ecological explanation. For instance, one widely invoked explanation is that of balancing apostatic selection—color polymorphism is advantageous for raptorial species because the prey find it more difficult to form a “search image.” Other authors have invoked disruptive selection and even sexual selection. Yet despite a great many hypotheses of this nature, there has been, until recently, no quantitative comparative tests. The first quantitative comparative tests of the ecological basis of color polymorphism in birds were published simultaneously by Fowlie and Kruger (2003)

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and Galeotti et al. (2003). Both studies scored the incidence of polymorphism across species and both groups attempted to test hypotheses based on difference mechanisms of selection. The studies differed with respect to the taxonomic range of the species studied, however, with the analyses of Fowlie and Kruger (2003) restricted to hawks and owls, whereas that of Galeotti et al. (2003) considered all bird lineages. Interestingly, neither study supported the hypotheses based on apostatic selection, with no significant associations found between the incidence of polymorphism and foraging. Instead, each study identified a number of other likely correlates. In their analyses across all major avian groups, Galeotti et al. (2003) found strong evidence for an association between polymorphism and disruptive selection, with polymorphism being much more common in species that lived in variable-light environments. Among hawks and owls, however, Fowlie and Kruger (2003) found that the only robust ecological correlates were the extent of sexual dichromatism and measures of population size. They interpreted these results as evidence that the chances of a species being polymorphic is dependent, first, on the chance of a mutation occurring in the population (which is determined, in part, by population size) and, second, on whether such a mutation can subsequently be maintained by sexual selection. The next challenge is clearly to test whether there are indeed different explanations for polymorphism in different avian lineages. Nonplumage Coloration: Bills, Legs, Eyes, Combs, and Wattles Although this review has thus far focused exclusively on plumage coloration, birds also show striking interspecific color variation in their bare parts, including their bills, legs, eyes, combs, and wattles. Moreover, there is ample evidence from intraspecific experimental studies that these bare-part colors play a role in sexual selection, with the red bill color of male Zebra Finches (Taeniopygia guttata; Plate 18) and comb color of male Red Junglefowl (Gallus gallus; Plate 26, Volume 1) being two of the classic examples of mate choice cues in birds (e.g., Burley and Coopersmith 1987; Zuk et al. 1990). But how much is known about interspecific variation in bare-part coloration? As far as I am aware, the only published quantitative comparative study of bare-part coloration in adult birds was that of Olson and Owens (2005), who in their study of carotenoid-based pigmentation showed that this form of coloration was, in fact, more common in bare parts than in plumage. They also showed that the ecological correlates of carotenoid-based bare-part color-

Ecological Explanations for Interspecific Variability

ation were different from those in plumage, with interspecific variation in bare-part coloration being associated with differences among species in lifehistory and habitat use rather than the dietary availability of carotenoids, whereas plumage coloration was more commonly dependent on diet (Olson and Owens 2005). The only other published comparative studies of bare-part coloration that I have been able to locate are those by Kilner and colleagues (Kilner and Davies 1998; Kilner 1999), who have studied the ecological correlates of interspecific variation in a juvenile trait: nestling mouth color. The results are interesting, not only because of what they say about the evolution of chick mouth coloration and begging behavior, but also because of the way they echo the results of similar analyses on adult plumage color, in suggesting a complex interaction between intrinsic and extrinsic factors. In their initial analysis, Kilner and Davies (1998) used modern phylogenetic comparative analyses to specifically test the light-environment hypothesis of Marchetti (1993), which predicts that species inhabiting dim light environments should have brighter coloration (see the discussion above). Kilner and Davies (1998) therefore compared the mouth color of species that use open nest sites with species that use holes as nesting sites. They found that, although there was no association between nest type and the yellow-orange-red coloration of the mouth itself, hole-nesting species did tend to have larger and brighter flanges around the side of the mouth. They interpreted this observation as evidence that light environment has influenced the evolution of an aspect of a begging signal and pointed out the similarity with Marchetti’s (1993) finding that Phylloscopus warblers from dark habitats tend to have larger plumage patches than comparable species from more open habitats. Subsequently, Kilner (1999) tested for an interaction between light environment and the level of kin conflict among chicks within a nest—an intrinsic factor that theory predicts should have a strong effect on the evolution of begging signals. Using the prevalence of extra-pair paternity as an index of kin conflict (see also Royle et al. 1999), Kilner (1999) again used modern phylogenetic methods to show that, as predicted by kin-conflict theory, species with a higher level of conflict have more elaborate begging signals, which, in this case, was manifested as more red mouth coloration (Figure 9.8). The twist, however, was that this relationship was only robust among that subset of species that uses open nest sites. Kilner (1999) therefore summarized her findings by suggesting that species differences in the extent of kin conflict can affect the evolution of mouth color, but only in those light environments in which variation in mouth coloration is likely to be visible to the parent birds.

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Figure 9.8. Relation between nestling mouth color and the incidence of extra-pair young (EPY) for light and dark nest locations. Each data point represents a different species. The graph shows that in species in which the percentage of EPY is high and nests are in light locations, nestlings have redder mouths. No equivalent relationship exists for species with nests in dark locations. Redrawn from Kilner (1999).

Conclusions and Future Challenges For each of the three aspects of plumage coloration that I reviewed in detail, comparative analyses have helped to differentiate between potentially competing hypotheses. In each case, some predictions have received consistent support, whereas others have been equally consistently refuted. Much progress has therefore been made. But several general weaknesses remain. The most obvious is that each comparative study has tended to focus on just one or two hypotheses, which makes it extremely difficult to compare the relative importance of a whole class of hypotheses. More multivariate tests are required. A second general limitation is that many of the key comparative tests have been performed on a database that is restricted to a single taxonomic group and/or a single geographic region. At a proximate level, this restriction makes it very difficult to compare the results of different studies, but a more important effect is that we rarely know when we have identified a general phenomenon and when we are dealing with an idiosyncrasy. Finally, most tests have

Ecological Explanations for Interspecific Variability

been based on subjective, human-oriented indices of coloration. This bias means that it has been impossible to conduct detailed tests on such phenomena as crypsis, showiness, and pattern. Considering the nature of avian plumage color diversity, it is particularly disappointing that pattern has received so very little attention. Even the most recent studies based on reflection spectra data and color models have used crude comparisons between a single pair of colors to estimate visual contrast. This is an area where comparative biologists need the input of behavioral psychologists to understand how brains perceive spatial patterns and complex color combinations. Each of these criticisms can be illustrated by summarizing the findings for each of the major aspects of coloration reviewed. For instance, most work on the evolution of sexual dichromatism has focused on the role of sexual selection, and there is now a robust body of evidence that differences among species in the extent of sexual dichromatism are indeed associated with variation in the strength of sexual selection. Much less work has been done on the balancing role of natural selection for crypsis, but it does appear that species differences in parental care and the associated predation risk also influence interspecific variation in dichromatism. The ongoing challenges are, first, to quantify the relative roles of sexual selection for showiness versus natural selection for crypsis (see Stuart-Fox and Ord 2004), and second, to test whether there are major differences among different carotenoid-, melanin-, and structuralbased coloration. DPM has not been subjected to the same breadth of analyses as has sexual dichromatism. For instance, almost all recent comparative studies have been based on variations on the original database of North American passerines of Rohwer et al. (1980; but see Björklund 1991; Chu 1994). Among this group of studies, there is strong evidence that DPM has evolved as the result of strong competition among males. But again, there is a need to understand the relative importance of competition during the breeding season and during the winter. It seems likely that it would be fruitful to split up analyses according to the molt stage at which the subadult plumage is present (see Björklund 1991). Indeed, when this approach was pursued in a phylogenetic analysis of shorebirds, the conclusion was that DPM may not be an adaptive trait (Chu 1994). It would be shocking if this were also the case for passerines. Understanding interspecific variation in color intensity remains a huge challenge. Several recent studies have strongly supported the light-environment hypothesis, which is an exciting development, but there has been only one quantitative study of the species-recognition hypothesis. Again, it is difficult to

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be confident of the relative roles of different ecological mechanisms. But what is most needed in the study of coloration is a way of dealing with patterns and complex combinations of color. These are arguably the most inspiring aspects of avian plumage diversity, yet remain unquantified by our present methods.

Summary Why do different species of bird display different colors? The overall aim of this chapter is to review ecological explanations for variation between species in coloration. I focus on three particular aspects of interspecific variation— sexual dichromatism, DPM, and color intensity. Of these, sexual dichromatism is the best studied from a comparative perspective. There is a robust body of work showing that pronounced sexual dichromatism is associated with increased sexual selection, a large sex difference in parental care, and reduced need for crypsis. There have been fewer studies of delayed plumage maturation. These have generally supported the idea that delayed maturation is associated with increased competition among males, but the relative roles of breedingand nonbreeding-season interactions remain uncertain. Comparative studies on color intensity remain relatively rare, but in general, they support the hypothesis that the light environment is a key factor and that particular colors may be associated with particular forms of display. There has been no support for the hypothesis that interspecific variation in coloration is an adaptation to avoid hybridization among closely related species. Taken together, these findings are encouraging, because they suggest that our framework for understanding plumage coloration is biologically sensible, but they also show that our understanding is weakened by three serious limitations of the comparative studies conducted to date. First, because each study has tended to focus on just one or two hypotheses, we know rather little about the relative importance of different explanations. Second, because many of the tests have been conducted on taxonomically restricted databases, we know relatively little about the generality of each explanation. Finally, because most comparative studies of avian coloration are based on subjective, human-oriented indices of coloration, we know very little about such phenomena as crypsis, conspicuousness, and pattern. The good news is that, with the arrival of increasingly sophisticated comparative methods, large class-wide databases, and physiological vision models, all of these shortcomings can now be overcome. Avian plumage coloration provides a great model system for researchers interested in explaining biological diversity.

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ian p. f. owens Lozano, G. A. 1994. Carotenoids, parasites, and sexual selection. Oikos 70: 309–311. Lyon, B. E., and R. D. Montgomerie. 1986. Delayed plumage maturation in passerine birds: Reliable signaling by subordinate males? Evolution 40: 605–615. Marchetti, K. 1993. Dark habitats and bright birds illustrate the role of the environment in species divergence. Nature 362: 149–152. Martin, T. E. 1995. Avian life history evolution in relation to nest sites, nest predation and food. Ecol Monog 65: 101–127. Martin, T. E., and A. V. Badyaev. 1996. Sexual dichromatism in birds: Importance of nest predation and nest location for females versus males. Evolution 50: 2454–2460. Martin, T. E., and P. Li. 1992. Life history traits of open- vs. cavity-nesting birds. Ecology 73: 579–592. Martins, E. P. 2000. Adaptation and the comparative method. Trends Ecol Evol 15: 296–299. Maynard Smith, J., and D. Harper. 2004. Animal Signals. Oxford: Oxford University Press. Mayr, E. 1942. Systematics and the Origin of Species. New York: Columbia University Press. Mayr, E. 1963. Animal Species and Evolution. Cambridge, MA: Harvard University Press. McGraw, K. J., and G. E. Hill. 2000. Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc R Soc Lond B 267: 1525–1531. McGraw, K. J., S. Ito, K. Wakamatsu, P. M. Nolan, P. Jouventin, et al. 2004. You can’t judge a pigment by its color: Carotenoid and melanin content of yellowand brown-colored feathers in swallows, bluebirds, penguins, and Domestic Chickens. Condor 106: 390–395. McNaught, M., and I. P. F. Owens. 2002. Interspecific plumage colour variation in birds: Species recognition or light environment? J Evol Biol 15: 505–514. Møller, A. P. 1986. Mating systems among European passerines: A review. Ibis 128: 234–250. Møller, A. P., and T. M. Birkhead. 1994. The evolution of plumage brightness in birds is related to extra-pair paternity. Evolution 48: 1089–1100. Montgomerie, R. D., and B. E. Lyon. 1986. Does longevity influence the evolution of delayed plumage maturation in passerine birds? Am Nat 128: 930–936. Oakes, E. J. 1992. Lekking and the evolution of sexual dimorphism in birds: Comparative approaches. Am Nat 140: 665–684. Olson, V. A., and I. P. F. Owens. 1998. Costly sexual signals: Are carotenoids rare, risky or required? Trends Ecol Evol 13: 510–514. Olson, V. A., and I. P. F. Owens. 2005. Interspecific variation in the use of carotenoidbased coloration in birds: Diet, life history and phylogeny. J Evol Biol (in press).

Ecological Explanations for Interspecific Variability Orians, G. H., and G. M. Christman. 1968. A comparative study of the behavior of Red-winged, Tricolored, and Yellow-headed Blackbirds. Univ California Pub Zool 84: 1–81. Owens, I. P. F., and P. M. Bennett. 1994. Mortality costs of parental care and sexual dimorphism in birds. Proc R Soc Lond B 257: 1–8. Owens, I. P. F., and P. M. Bennett. 1997. Variation in mating system among birds: Ecological basis revealed by hierarchical comparative analysis. Proc R Soc Lond B 264: 1103–1110. Owens, I. P. F., and I. R. Hartley. 1998. Sexual dimorphism in birds: Why are there so many forms of dimorphism? Proc R Soc Lond B 265: 397–407. Price, T. 1997. Correlated evolution and independent contrasts. Phil Trans R Soc Lond B 352: 519–529. Pruett-Jones, S. G., M. A. Pruett-Jones, and H. I. Jones. 1990. Parasites and sexual selection in birds of paradise. Am Zool 30: 287–298. Read, A. F. 1987. Comparative evidence supports the Hamilton and Zuk hypothesis on parasites and sexual selection. Nature 328: 68–70. Read, A. F. 1988. Sexual selection and the role of parasites. Trends Ecol Evol 3: 97–102. Read, A. F., and P. H. Harvey. 1989a. Reassessment of comparative evidence for the Hamilton and Zuk theory on the evolution of secondary sexual characters. Nature 339: 618–620. Read, A. F., and P. H. Harvey. 1989b. Validity of sexual selection in birds—A reply. Nature 340: 105. Ridley, M. 1983. The explanation of organic diversity: The comparative method and adaptations for mating. Oxford: Oxford University Press. Ridley, M. 1989. Why not to use species in comparative tests. J Theor Biol 136: 361–364. Rohwer, S. A. 1975. The social significance of avian winter plumage variability. Evolution 29: 593–610. Rohwer, S. A., and G. S. Butcher. 1988. Winter versus summer explanations of delayed plumage maturation in temperate birds. Am Nat 131: 556–572. Rohwer, S. A., S. D. Fretwell, and D. M. Niles. 1980. Delayed plumage maturation in passerine plumages and the deceptive acquisition of resources. Am Nat 115: 400–437. Royle, N. J., I. R. Hartley, I. P. F. Owens, and G. A. Parker. 1999. Sibling competition and the evolution of growth rates in birds. Proc R Soc Lond B 266: 923–932. Sætre, G.-P., T. Moum, S. Bures, M. Kral, M. Adamjan, and J. Moreno. 1997. A sexually selected character displacement in flycatchers reinforces premating isolation. Nature 387: 589–592. Savalli, U. M. 1995. The evolution of bird plumage colouration and plumage elaboration: A review of hypotheses. Curr Ornithol 12: 141–190.

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ian p. f. owens Scott, D. K., and T. H. Clutton-Brock. 1990. Mating systems, parasites and plumage dimorphism in waterfowl. Behav Ecol Sociobiol 26: 261–273. Sillen-Tullberg, B., and Temrin, H. 1994. On the use of discrete characters in phylogenetic trees with special reference to the evolution of avian mating systems. In P. Eggleton and R. Vane-Wright, ed., Phylogenetics and Ecology, 312–322. London: Academic Press. Soler, J. J., A. P. Møller, and M. Soler. 1998. Nest building, sexual selection and parental investment. Evol Ecol 12: 427–441. Stuart-Fox, D. M., and T. J. Ord. 2004. Sexual selection, natural selection and the evolution of dimorphic coloration and ornamentation in agamid lizards. Proc R Soc Lond B 271: 2249–2255. Stuart-Fox, D., A. Moussali., G. R. Johnston, and I. P. F. Owens. 2004. Evolution of colour variation in dragon lizards: Quantitative tests of the role of crypsis and local adaptation. Evolution 58: 1549–1559. Studd, M. V., and R. J. Robertson. 1985. Life span, competition, and delayed plumage maturation in male passerines: The breeding threshold hypothesis. Am Nat 126: 101–115. Temrin, H., and B. Sillen-Tullberg. 1994. The evolution of avian mating systems: A phylogenetic analysis of male and female polygamy and length of pair bond. Biol J Linn Soc 52: 121–149. Temrin, H., and B. Sillen-Tullberg. 1995. A phylogenetic analysis of the evolution of avian mating systems in relation to altricial and precocial young. Behav Ecol 6: 296–307. Verner, J., and M. F. Wilson. 1969. Mating systems, sexual dimorphism and the role of male North American passerines in the nesting cycle. Ornithol Monogr 9: 1–76. Vorobyev, M., and D. Osorio. 1998. Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265: 351–358. Vorobyev, M., D. Osorio, A. T. D. Bennett, N. J. Marshall, and I. C. Cuthill. 1998. Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183: 621–633. Wallace, A. R. 1889. Darwinism, second edition. London: Macmillan. Zahavi, A., and Zahavi, A. 1997. The Handicap Principle. Oxford: Oxford University Press. Zuk, M., R. Thornhill., J. D. Ligon, K. Johnson, S. Austad., et al. 1990. The role of male ornaments and courtship behaviour in female mate choice of Red Jungle Fowl. Am Nat 136: 459–473.

10 Adding Color to the Past: Ancestral-State Reconstruction of Coloration kevin e. oml and and christopher m. hofmann

Using Ancestral-State Reconstruction to Frame Questions Evolutionary studies of bird coloration have traditionally been hampered by an inability to know the history of the colors being studied—bird coloration generally does not fossilize. In recent years, advances in phylogenetic reconstructions have provided an unprecedented opportunity to infer the coloration of ancestral taxa. Using ancestral-state reconstruction (Cunningham et al. 1998), it is possible to use the characteristics of extant species to reconstruct likely colors and patterns of ancestral avian lineages. Ancestral character-state reconstruction—also known as character mapping, character tracing, or character optimization—generally involves two distinct steps. The first step is to obtain a reliable phylogeny of the group. Increasingly, this is a molecular phylogeny based on DNA sequences, which typically has the advantage of being independent of the characters of interest (but see de Queiroz 1996). The second step is to use that tree, along with the character states of extant species, to infer the characteristics at ancestral nodes (i.e., ancestral species)—in other words, to map the color characters onto the molecular tree. Ancestral-state reconstruction helps frame the questions that ornithologists can and should be asking about the species of birds they are studying. For

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kevin e. oml and & christopher m. hofmann example, a North American ornithologist may notice the bright orange breast of a male Baltimore Oriole (Icterus galbula), and she may begin to ask questions about its behavioral significance and the selective forces that favor such coloration. However, if she undertakes this study without considering the breast coloration of other orioles, including those in the tropics, without knowing which species are closely related, and without considering the possible history of this characteristic, she may miss interesting opportunities or make misleading assumptions. In particular, if she focuses on why the males are so bright compared to the females, she may be asking the wrong question. For example, if in related species both males and females are brightly colored, it may be more fruitful to ask why the breast plumage of females is so dull. For studies like this, it is useful to know whether the trait of interest recently evolved in the focal species, or whether it evolved a long time ago in a distant ancestor. This and other such examples are developed in the course of this chapter.

Reconstructing Color: An Example Consider the hypothetical phylogeny in Figure 10.1. It is comprised of ten bird species: eight ingroup species (e.g., the genus in question) as well as two outgroup species (e.g., in two genera closely related to the ingroup). If the focal species, species Z, is black, and we know that species Y is closely related and white, then we know that some change must have taken place between Y and Z. However, without knowing which other species are closely related, we cannot determine the color at the YZ ancestral node. That ancestor could have been black, so that Y represents a loss of black, or the ancestor could have been white so that Z represents a gain of black. If the phylogeny shows us that species W and X are related in the way shown by the topology, that provides strong information that the common ancestor of that clade was black, and that black has recently been lost in species Y. This preferred reconstruction only requires one change in the clade—assuming that an ancestral lineage in the WXYZ clade was always white would require three changes and is less parsimonious. The other clade in the genus has only one black species, so it is most parsimonious that the ABCD ancestor was white and that species B represents a recent gain of black coloration. The two outgroup genera are also white, which provides good evidence that the common ancestor of the genus was originally white. Thus, knowing the phylogeny enables us to infer the direction (polarity) of evolutionary change in our focal species pair and to determine where losses versus gains of the color of interest have likely occurred.

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419 O1 O2 A B C D W X Y Z

Figure 10.1. Ancestral-state reconstruction of coloration in a hypothetical bird genus (species A–D and W–Z) along with two outgroups (O1, O2). The common ancestor of the group is reconstructed as being white (based on unordered parsimony). Black coloration is reconstructed as evolving convergently twice: once in species B, and once in the common ancestor of the WXYZ clade, with a subsequent reversal to white in species Y. This reconstruction requires a total of three evolutionary changes and is the most parsimonious, in that other reconstructions require more evolutionary changes.

Knowing this phylogeny, we might decide that species Z is not the ideal species in which to study the evolution of black coloration. It is a member of a clade that probably evolved black coloration in its common ancestor, which could have occurred long ago in a different selective environment. We can also use molecular clocks (Avise 2004) to estimate how long ago black coloration may have evolved in the WXYZ clade—in other words, branch lengths on the phylogeny also provide useful information. Knowing why species Z may maintain black coloration is interesting and important, but for such a species, there is an increased chance that constraint or lack of selection against black coloration may be sufficient to explain its maintenance. In contrast, species B seems to represent a recent gain of black coloration, so it may be easier to measure the selective forces that led to its evolution. We can be even more confident that there must be strong recent selection pressure in the current environmental conditions if we know species A and B split very recently. Species B may be an easier and much more fruitful species in which to study the function of black coloration. Furthermore, in clade WXYZ, species Y seems to represent a

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Box 10.1. Methods of Ancestral-State Reconstruction and the Basal Fallacy One of the most powerful uses of phylogenies is to infer the characteristics of extinct ancestral taxa. This approach is especially crucial for such characters as coloration and behavior, which generally do not fossilize. For such characters, it is necessary to use indirect methods to infer what evolutionary changes have occurred in the past. The logic of parsimony and similar inference methods can be used to infer probable ancestral characteristics. Generally, the ancestral states that require the fewest evolutionary changes or fit best with the assumed model of evolution are preferred (Brooks and McLennan 1991; Cunningham et al. 1998). Here we provide more background on different methods of such character mapping, and address one of the most common misconceptions about how position on a tree may reflect ancestral character states. In the tree shown in Figure B10.1, we show four hypothetical bird species with their phylogeny. The most parsimonious ancestral state reconstruction is depicted on the tree branches. Because species A is in the “basal” position on the tree, it may seem like the common ancestor of the group must have been white (the “basal-as-primitive fallacy”; Crisp and Cook 2005). However, note that the parsimony reconstruction is equivocal for the ancestral node; based on simple parsimony, the common ancestor could have been black or white. There could have been a change to white on the branch leading to A, or a change to black on the branch leading to BCD—either reconstruction is equally parsimonious and would only require one change (parsimony reconstruction using unordered parsimony in MacClade; Maddison and Maddison 2000). Maximum likelihood reconstructions (Cunningham et al. 1998; Pagel 1999) are shown in pie diagrams next to the nodes. Note that maximum likelihood actually favors black as the most likely state at the ancestral node, especially when branch lengths are taken into account. A third possible method is to use Bayesian approaches (Huelsenbeck et al. 2003). Whether using parsimony, likelihood, or Bayesian methods, different assumptions can lead to different reconstructions, so careful attention to these methods and assumptions is critical (Omland 1997, 1999; Cunningham et al. 1998).

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Figure B10.1.

See Maddison and Maddison (1992) or Brooks and McLennan (1991) for more background on ancestral-state reconstruction and tree thinking. (The likelihood reconstruction was conducted assuming the symmetric transformation model with branch lengths as depicted, using Mesquite; Maddison and Maddison 2004.)

recent loss of black coloration, and we may be able to learn about black feathers from a different perspective by studying the loss of the trait. The reconstruction in Figure 10.1 is the most parsimonious; however, this reconstruction is an inference based on simple parsimony (i.e., “unordered”) and makes a number of explicit and implicit assumptions (Omland 1997, 1999; Cunningham et al. 1998). Other methods of ancestral-state reconstruction include weighted parsimony, maximum likelihood and Bayesian methods (see Box 10.1). Different assumptions and methods may result in different inferences and can provide estimates of the confidence that we should have in the reconstructions at any particular node. Being aware of assumptions,

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kevin e. oml and & christopher m. hofmann alternative methods, and ways of assessing reliability is important for understanding the implications of character mapping for studies of bird coloration. Ancestral-state reconstruction has been used to study a number of aspects of coloration in birds. In this chapter we review: (1) studies of the rate of change in individual color characters, (2) the apparent convergence of overall color patterns in several groups of birds, and (3) the repeated gain and loss of sexual dichromatism. In addition, we preview a new use of ancestral reconstruction— mapping complex spectral characters obtained from spectrometry.

Reconstructing Individual Color Patches One of the most basic applications of phylogenies to studies of avian color is to reconstruct the history of individual color patches. For example, one might be interested in whether black crowns were present or absent in the common ancestor of a group or how many times black crowns had evolved or been lost. Such studies have been conducted to address a number of different questions: (1) Are individual color patches subject to high rates of evolution? (2) Are individual color patches subject to homoplasy (convergence and reversal)? (3) What is the history of specific color patches of known functional significance? Rapid Plumage and Bare-Part Evolution Such sexually selected traits as bird plumage color are expected to evolve rapidly for several reasons, including the strength of sexual selection, the possible arbitrary nature of which signals are elaborated, and the possible interaction between sexual selection and speciation (e.g., Andersson 1994; Prum 1997; Omland and Lanyon 2000; Omland and Kondo in press). Additionally, some plumage characters are changed by point mutations in single genes (Theron et al. 2001; Mundy et al. 2004), so different rates of mutation and fixation also could be involved. Ornithologists have long recognized the repeated occurrence of similar patterns, such as wing bars and “black crowns,” in apparently distantly related taxa (Hoekstra and Price 2004), but only recently have such character states been rigorously mapped onto phylogenies. Several studies have used molecular phylogenies to reconstruct rapid changes in individual plumage characters (Johnson and Lanyon 2000; Weckstein 2003; Hill and McGraw 2004). Price and Pavelka (1996) mapped the presence or absence of melanin for three body patches that show pattern variation among Phylloscopus warblers and demonstrated the repeated gain and loss of plumage patches (especially crown stripes; Figure 10.2; Plate 29). Other studies have noted

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Figure 10.2. Phylogeny of warblers in the genus Phylloscopus, showing parsimonious reconstructions of wing-patch (W), crown-stripe (C), and rump-patch (R). Inferred changes are indicated on the tree as gains and losses of light, nonmelanized patches. Cettia fortipes is the outgroup. Some races of the species marked with an asterisk lack a crown stripe. There are several equally parsimonious reconstructions of wing-patch; regardless, repeated rapid changes are indicated. Redrawn from Price and Pavelka (1996).

rapid plumage evolution in light of a phylogeny or have discussed plumage data that are inconsistent with a molecular phylogeny, but have not shown explicit reconstructions of plumage characters (e.g., Christidis et al. 1988; Hackett and Rosenberg 1990; Joseph and Moritz 1993; Kusmierski et al. 1997; Burns 1998b; Crochet et al. 2000; Kimball et al. 2001; Ödeen and Björklund 2003; Lovette 2004; see also Box 10.2). Bare-part colors also show rapid changes when mapped onto phylogenies, although even fewer such studies have been done. For example, Johnson (1999) reconstructed bill coloration in Anas ducks and showed repeated gain and loss of colored bills (yellow or red, which he assumed contained carotenoids; see also Omland 1996). He showed that lineages that had lost dimorphic plumage

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Box 10.2. Should Color Characters Be Used to Build Phylogenies? The colors of plumage and bare-parts in birds are among the most conspicuous and variable traits of many species and are frequently the basis for distinguishing different species of birds. An ongoing question in systematics is whether such characters should be used to build evolutionary trees. Are avian colors and patterns reliable phylogenetic characters? Although most of the studies reviewed in this chapter have taken the approach of reconstructing color characters onto molecular phylogenies, some researchers have used them as part of morphological phylogenies (Livezey 1991; Prum 1997; Chu 1998; Birdsley 2002). Bertelli et al. (2002) exclusively used integumentary characters for a phylogeny of tinamous, although this group is drab and only a few of the characters would likely be subject to sexual selection. If plumage characters evolve very rapidly, then they may be subject to high levels of homoplasy (convergence and reversal), especially if the number of color states seems to be limited (Omland and Lanyon 2000). Character types with higher levels of homoplasy may be less useful as phylogenetic characters (Felsenstein 1973), although all types of characters show some levels of homoplasy and phylogenetic methods can deal with some homoplasy. Furthermore, if color characters evolve very rapidly, they may retain little or no phylogenetically useful information even if homoplasy is low. Because color is so labile and because of the opportunities provided by both mitochondrial and nuclear genes, ornithologists should probably avoid heavy reliance on color characters for building trees (Omland and Lanyon 2000; Weckstein 2003). These points are especially true for elaborate and colorful aspects of plumage that are likely subject to sexual selection. We generally advocate the use of other phylogenetic data for building trees and mapping color onto those trees (although see de Queiroz 1996). Finally, caution is warranted even when just mapping color characters onto molecular phylogenies: characters that evolve rapidly and exhibit high levels of homoplasy will likely lead to less accurate ancestral-state reconstructions (Felsenstein 1973; Omland 1997). However, the often rapid evolution of elaborate color characters means that they are good for diagnosing species and subspecies (Omland and Lanyon

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2000) and perhaps for determining groups of very closely related species. In fact, many mtDNA trees are not sorted to monophyly for closely related bird species (Funk and Omland 2003), so color characters can be more reliable indicators of species boundaries than sequence data (but see Gill et al. 1993 and Omland et al. 2000 for counterexamples in drably plumaged groups). Color characters are also much more likely to be useful for defining species limits than sequences from nuclear genes, which tend to mutate slowly or retain ancestral polymorphism (Allen and Omland 2003). Nevertheless, caution is warranted even with species diagnosis, given that color traits can show phenotypic plasticity, as reviewed in Chapter 12, Volume 1. Color characters may be especially unreliable as characters for building trees if suites of color characters evolve in concert, so that overall appearance is subject to convergence (Omland and Lanyon 2000; Allen and Omland 2003). Although homoplasy in individual characters can often be overcome by adding more characters, this approach is not a viable solution if the characters show concerted homoplasy (e.g., McCracken et al. 1999). Characters that evolve in concert or that respond to selection to produce common patterns violate one of the fundamental assumptions of phylogenetic analysis— that of character independence (Swofford et al. 1996). This topic is also addressed in the main text on convergence in overall color patterns.

tended to evolve colored bills. Johnson’s findings are consistent with the “transference hypothesis,” which predicts that female preferences may be transferred from one ornament type to another (in this case, from plumage to bill color). Weckstein (2003) reconstructed the history of two fleshy ornaments and three feather ornaments in toucans, all of which showed high levels of homoplasy. Prum and Torres (2003) showed convergent evolution of avian skin coloration across a wide diversity of avian taxa (see also Randi et al. 2000). Several studies on mate choice within species have suggested that fleshy ornaments may generally be more reliable indicators of current condition than plumage color (e.g., Zuk et al. 1992; Omland 1996; Blount et al. 2003; Chapter 12, Volume 1). More studies that reconstruct the ancestral states of barepart color characters are needed to determine whether such properties might result in differences between plumage and fleshy ornaments in patterns and rates of macroevolution.

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kevin e. oml and & christopher m. hofmann In each of the above cases, rapid character evolution is a qualitative description indicating repeated gain or loss of character states among a relatively small number of species. The speed of color evolution can be evaluated more quantitatively, however, by comparing the number of individual color characters that have changed relative to the estimated time since speciation using molecular clock calibrations. For example, Kondo and Omland (2004) showed that Baltimore Orioles and Black-backed Orioles (Icterus abeillei) have accumulated 17 discrete plumage patch differences, even though they likely split from each other only about 200,000 years ago. These two taxa appear to be more closely related than virtually any pair of bird species studied to date, yet they differ dramatically in plumage color. Examples: Individual Plumage Patches Omland and Lanyon (2000) scored male plumage color for the entire feathered surface of all 25 recognized species of New World orioles (Icterus). Orioles have 44 discrete plumage areas that vary in coloration among species, and virtually the entire feathered surface of orioles can differ between any two species. Forty-two of these characters showed evidence of two or more changes on the molecular phylogeny. Some characters showed extremely high levels of convergence and/or reversal across the phylogeny. For example, the coloration of the lesser coverts was likely colored (yellow, orange, or chestnut) in the common oriole ancestor, but apparently changed to black seven different times across the genus (Figure 10.3). The study did not reveal any obvious tendency for characters on certain parts of the body to be more or less labile. It will be interesting to determine whether parts of the avian body involved in displays are more labile than areas that are obscured (e.g., head and wings versus vent and under-wing areas). Prum (1997) developed a phylogenetic hypothesis for manakins (Pipridae) based on plumage characters. Using this phylogeny, he argued that both plumage and behavioral characters show “explosive” diversity, with little evidence of constraint or convergent evolution. Prum (1997:668) argued that his results are “consistent with Fisherian and broad sensory bias mechanisms, but they are not consistent with the predictions of the indicator, direct selection, species isolation or sensory drive mechanisms.” Johnson and Lanyon (2000) reconstructed the presence or absence of a colored epaulet (shoulder patch) across the “grackles and allies” clade within the Icteridae. Their study is unique in that they reconstructed a particular plum-

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cayanensis cayanensis chrysocephalus cayanensis periporphyrus cayanensis pyrrhopterus auricapillus dominicensis dominicensis dominicensis portoricensis oberi laudabilis bonana dominicensis melanopsis dominicensis northropi spurius fuertesi spurius spurius dominicensis prosthemelas cucullatus igneus cucullatus nelsoni wagleri wagleri maculialatus jamacaii croconotus jamacaii strictifrons icterus ridgwayi graceannae pectoralis mesomelas salvinii mesomelas taczanowskii mesomelas mesomelas gularis tamaulipensis gularis yucatanensis gularis gularis nigrogularis nigrogularis nigrogularis trinitatis auratus leucopteryx leucopteryx bullockii bullockii bullockii parvus pustulatus formosus pustulatus sclateri abeillei galbula chrysater chrysater chrysater hondae graduacauda audubonii graduacauda graduacauda parisorum

Figure 10.3. Phylogeny of New World orioles (genus Icterus) showing the most parsimonious reconstruction of lesser covert coloration. This character shows a very high level of convergence in an individual plumage patch. The lesser coverts were originally scored as being either black or “carotenoid,” but the latter should have been scored as “colored,” as we now have evidence that several oriole species use phaeomelanins in their colored plumage (C. M. Hofmann, T. W. Cronin and K. E. Omland, unpubl. data). Redrawn from Omland and Lanyon (2000: Figure 3).

age patch known to be used in displays and showed repeated correlated changes with a particular environment or function. In particular, species that inhabit open marsh habitats, including the Red-winged Blackbird (Agelaius phoeniceus; Plate 11), were significantly more likely to have colored epaulets than were related species that do not nest in marshes—possibly due to more intense territorial interactions (Figure 10.4).

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absent Nesopsar nigerrimus Dives warszewiczi Lampropsar tanagrinus Macroagelaius subalaris Gymnomystax mexicanus Curaeus curaeus Amblyramphus holosericeus Gnorimopsar chopi Agelaius thilius Agelaius cyanopus Agelaius xanthophthalmus Oreopsar bolivianus Molothrus badius Agelaius ruficapillus Agelaius icterocephalus Xanthopsar flavus Pseudoleistes virescens Pseudoleistes guirahuro Euphagus cyanocephalus Euphagus carolinus Quiscalus quiscula Quiscalus lugubris Quiscalus niger Quiscalus mexicanus Quiscalus major Agelaius xanthomus Agelaius humeralis Agelaius tricolor Agelaius phoeniceus Molothrus rufoaxillaris Scaphidura oryzivora Molothrus aeneus Molothrus bonariensis Molothrus ater

Figure 10.4. Ancestral-state reconstruction of colorful epaulets in male blackbirds (family Icteridae) based on unordered parsimony. The four changes to colored epaulets all occur in lineages that are predominantly marsh nesting. The pigmentary basis of icterid epaulets has been tested in only one species (Red-winged Blackbird), in which epaulets contained a mix of melanins and carotenoids (McGraw et al. 2004). Redrawn from Johnson and Lanyon (2000).

As part of his extensive studies on the function of ornamental coloration in male House Finches (Carpodacus mexicanus; Plate 14), Hill (1994, 1996) reconstructed the size of the ventral carotenoid patch. He reconstructed a medium-sized patch as the ancestral state, with small and large patches being independently derived. He suggested that differing patch sizes were best explained as an evolutionary response to different levels of carotenoids in the

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environment, as females from all populations showed a preference for males with the largest patches. More such work using ancestral-state reconstruction is needed for individual color traits whose functional significance is known. Furthermore, little phylogenetic work has been done comparing character states with different hypothesized costs or behavioral functions. For instance, Eaton and Lanyon (2003) documented the wide range of avian taxa that show ultraviolet (UV) reflective plumage, but no studies have reconstructed the gain and loss of UV plumage colors. With regard to different pigment classes, it would be interesting to know whether carotenoids, melanins, and other bird pigments differ in their macroevolutionary lability. It will also be interesting to determine whether there is a tendency to lose or gain these different classes of pigments.

Convergence of Overall Plumage Patterns Overall plumage patterns created by suites of individual plumage characters, including both pattern and color elements, can also be studied using a phylogenetic approach. Several cases of overall plumage convergence have been documented in the context of molecular phylogenies (Joseph and Moritz 1993; Price and Pavelka 1996; Crochet et al. 2000; Omland and Lanyon 2000; Dumbacher and Fleischer 2001; Weibel and Moore 2002; Allen and Omland 2003; Weckstein 2003). Explanations for these cases of convergence range from genetic constraints to selection for interspecific mimicry. Overall Convergence in Orioles Work on New World orioles has uncovered repeated examples of convergence in complex plumage patterns (overall convergence: Omland and Lanyon 2000; see also Beecher 1950). The mitochondrial DNA (mtDNA) tree showed three distinct groups of orioles that have been designated clades A, B, and C (Figure 10.5). When looking at the overall patterns of orioles across this tree, two distinct “types” crop up repeatedly: those species with the Baltimore Type resemble the Baltimore Oriole, and those with the Altamira Type resemble the Altamira Oriole (Icterus gularis). The Baltimore Type occurs in two parts of Clade C and in Clade A. The Altamira Type shows convergence that is even more striking, with representatives in all three clades (Figure 10.5; Plate 32). These two plumage types represent the extremes of convergence; there are many species of orioles that exhibit other patterns. These overall convergent types

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Orchard Clade A

Hooded Clade B

Spot-breasted

Altamira

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Figure 10.5. Convergence in overall patterns in orioles (genus Icterus). Species outlined in black express the Baltimore Type pattern; species outlined in grey have the Altamira Type pattern. Phylogenetic tree based on mtDNA (Omland et al. 1999).

represent a combination of convergences, reversals, and retained ancestral states of the individual ornaments (Omland and Lanyon 2000). By correlating the number of plumage differences with the percentage of genetic divergence, we quantified the degree of plumage similarity across the entire genus Icterus (Figure 10.6). Data points in the lower right in Figure 10.6 depict the species pairs that show the most extreme examples of overall convergence. This approach shows that the amount of genetic divergence predicted the maximum number of plumage differences, although number of plumage

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between clades

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Figure 10.6. Pairwise plumage distance (calculated as the number of plumage patches that differ between taxa) as a function of genetic distance (uncorrected mitochondrial distance). Generally, the maximum amount of plumage divergence between species can be predicted based on sequence divergence, but the minimum amount of plumage divergence cannot be predicted from sequence divergence. Points labeled W, X, Y, and Z correspond to the most extreme examples of overall plumage convergence, including the species illustrated in Figure 10.5. Adapted from Omland and Lanyon (2000).

differences did not predict genetic divergence. By using such approaches, it is possible to quantify the amount of plumage change among different bird species; similar methods could be applied to a wide range of avian taxa and color traits. These results seem to suggest repeated convergence of plumage patterns. Another way of looking at these studies, however, is that there was disagreement in phylogenetic information between plumage characters and mtDNA data—it was conceivable that the plumage characters reflected evolutionary history and the mtDNA characters were misleading. To test these competing hypotheses, an independent gene was sequenced, the nuclear intron complex ODC 6/7. The nuclear data produced trees that showed the same three clades as did the mtDNA analysis (Allen and Omland 2003). Data from a second intron and additional individuals including outgroups further confirm the mtDNA tree and plumage convergence (K. E. Omland and C. M. Hofmann,

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kevin e. oml and & christopher m. hofmann unpubl. data). Thus, there is strong support for repeated convergence of the Baltimore and Altamira plumage types (see Hoekstra and Price 2004). What could explain the repeated evolution of these two complex color patterns? Possible explanations range from purely adaptive, driven by light environment (Endler and Théry 1996) or social selection (Moynihan 1968), to purely constrained, based on genetics or development (West-Eberhard 2003; see Hoekstra and Price 2004). If pattern convergence is due to light environment, we expect that species with the same plumage type would inhabit similar habitats (McNaught and Owens 2002); that is often not the case. For example, in the Baltimore Type, Baltimore and Orchard (Icterus spurius; Plate 30) orioles both inhabit forests and edge habitats of eastern North America, whereas Scott’s Oriole (I. parisorum) inhabits the deserts of southwestern North America. Selection for interspecific mimicry (Moynihan 1968; Dumbacher and Fleischer 2001) predicts that sympatric species should look similar, but the Altamira Type includes taxa that are both sympatric and allopatric with one another. There is no obvious environmental correlation or geographic trend that explains convergence in oriole color patterns (Omland and Lanyon 2000). In contrast, constraint appears to be a viable explanation for convergence in complex color patterns in orioles and other avian taxa, especially because individual plumage patches seem to have a limited number of colors that “blink” on and off (Price and Pavelka 1996; Omland and Lanyon 2000; see also Marshall et al. 1994; c.f. Prum 1997). Plumage Convergence in Other Bird Groups: Adaptive Explanations Other groups of birds—including woodpeckers (Weibel and Moore 2002), toucans (Weckstein 2003) and pitohuis (Dumbacher and Fleischer 2001)— seem to show convergence of overall patterns in sympatry. In these groups, adaptive explanations have been proposed that range from maintaining cohesion in mixed-species flocks (Moynihan 1968), to predator avoidance through flock confusion (Barnard 1979), to adaptation to common environments (Johnson and Lanyon 2000). Weckstein (2003) showed that distantly related pairs of Ramphastos toucan species have very similar overall plumage patterns in sympatry, which he attributed to any of the range of possible social or ecological explanations. Dumbacher and Fleischer (2001) showed convergence in plumage patterns between the Hooded Pitohui (Pitohui dichrous; Plate 3) and the Variable Pitohui (P. kirhocephalus; Plate 3), both of which can have high levels of toxin in their feathers. The authors argued that the best explanation

Adding Color to the Past

for convergence in these birds from New Guinea was Müllerian mimicry (Dumbacher and Fleischer 2001). They used ancestral-state reconstruction on phylogenetic trees based on mtDNA and two nuclear genes to show that races of the Variable Pitohui re-evolved the hooded pattern from an ancestor that lacked the hood and associated features (Figure 10.7). They used a statistical test developed by Templeton (1983) to argue that their evidence for convergent gain was statistically significant. However, their analysis is still based on the implicit assumption that the genetic and developmental basis of these patterns makes them equally possible to be lost or gained (Cunningham 1999; Omland 1999).

Repeated Gain and Loss of Sexual Dichromatism Dichromatism has been gained or lost repeatedly in many avian groups (Mayr 1963; Irwin 1994; Peterson 1996; Price 1996; Price and Birch 1996; Kusmierski et al. 1997; Omland 1997; Burns 1998a,b; Amundsen 2000) as well as in other taxa (reviewed in Wiens 2001). Understanding the causes of sexual dimorphism has been a major question in evolutionary biology since Darwin (1871). Most of this research has taken a microevolutionary perspective, focused on understanding why elaborate male ornaments have been favored by selection in the focal species (reviewed in Andersson 1994; Part 1 of this volume). Such a research program implicitly assumes that dimorphic species have evolved from a cryptic monomorphic ancestor. Considering this issue from a phylogenetic perspective, however, indicates that many possible historic pathways can lead to the gain or loss of sexual dimorphism (see Burns 1998a; Wiens 2001; Badyaev and Hill 2003; Figure 10.8). Sexual dimorphism is a composite character that results from differences in character states of the male and female (Coddington et al. 1997). Complete understanding of patterns of sexual dimorphism requires a comprehensive phylogenetic approach that includes ancestral reconstruction of both female and male characters (see also McLennan and Brooks 1993). There are four possible pathways leading to a change in dichromatism: gain in male coloration, loss of male coloration, gain in female coloration, and loss of female coloration (Figure 10.8). It is interesting to begin to evaluate the relative frequency of these transformations. Gain in male coloration is the situation implicitly assumed in many behavioral ecology studies of elaborate coloration. There are few examples, however, with strong evidence that one or more dichromatic species have evolved from monochromatic, dull ancestors

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Figure 10.7. Overall plumage convergence in pitohuis, likely attributable to Müllerian mimicry. The most parsimonious reconstruction of overall appearance is shown. Gray lines correspond to type 1 lineages (which express the focal hooded appearance), and black lines correspond to lineages not expressing the type 1 pattern. In addition, the pie diagrams show maximum-likelihood reconstructions of ancestral states, with the relative size of grey and black indicating the relative amount of support for the two states. The numbers above branches represent bootstrap support. Note that two nodes that are shown as unequivocal in parsimony reconstructions show a great deal of uncertainty when reconstructed using maximum likelihood (pie diagrams). Adapted from Dumbacher and Fleischer (2001).

Adding Color to the Past

435 Female change

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+D female male +D

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Figure 10.8. The four possible historical pathways to the gain and loss of sexual dichromatism. Male and female colors are shown then reconstructed using parsimony on a hypothetical four species phylogeny; +D indicates where dichromatism is gained, and –D indicates where it is lost. (a) The pathway often implicitly assumed in studies of sexual selection is a gain of dichromatism due to a gain of elaborate male coloration. However, a phylogenetic perspective (b) reveals that the reverse can happen and dichromatism can be lost. A phylogenetic perspective also reveals that changes in female coloration can lead to (c) gains and (d) losses of dichromatism.

(e.g., Northern Pintail [Anas acuta]; Johnson 1999; see below). Omland (1997) argued that loss of bright male coloration might be relatively common and highlighted the putative loss of elaborate color in the mallard clade (e.g., Black Duck [A. rubripes]; Avise et al. 1990; Omland 1997). Increasingly, researchers have pointed out that changes in female coloration may commonly lead to changes in dichromatism. Examples of gains in dichromatism due to a change in female coloration include Irwin (1994) and our own work within Icterus (unpublished data). Finally, Burns (1998b) provided an example of reduced sexual dichromatism in Piranga due to an increase in female coloration. Comprehensive surveys that quantify the relative frequencies of these four transformations are needed. This exercise could be challenging because of possible asymmetries in the relative ease of gains and losses of dichromatism (Omland 1997; see below), but it would be useful to direct more behavioral research toward the transformation types that are most common. Avian genera that inhabit both temperate and tropical zones provide a unique opportunity to investigate the gain and loss of sexual dichromatism.

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kevin e. oml and & christopher m. hofmann In many groups, there is a tendency for tropical resident species to be monochromatic and temperate migratory species to be dichromatic (Hamilton 1961; Cox 1985; Price 1996). In these birds, tropical species tend to have bright coloration in both females and males (monochromatic bright), whereas temperate species tend to have cryptically colored females and brightly colored males (dichromatic). Such patterns are found in a range of taxa, including New World warblers (Parulidae), tanagers (Thraupidae), and blackbirds (Icteridae; Hamilton 1961). For most groups, it unclear whether monochromatism or dichromatism represents the ancestral condition. Irwin (1994) presented evidence that monochromatic bright is the plesiomorphic condition in the family Icteridae; however, no published data test these ideas at lower phylogenetic levels in the family (see also Björklund 1990). In contrast, Burns (1998a) reconstructed the history of sexual dichromatism in the family Thraupidae and showed that dichromatism was the most parsimonious ancestral state in that taxon (Figure 10.9). Burns (1998b) also showed that strong dichromatism is ancestral within the genus Piranga at lower levels in that family. However, both Irwin (1994) and Burns (1998a,b) pointed out that changes in female coloration were often responsible for gains and losses of dichromatism, emphasizing the need for increased attention to female coloration in both phylogenetic and behavioral studies. One current focus of our research is to use a comprehensive phylogeny of New World orioles based on mtDNA and multiple nuclear introns to reconstruct gains and losses of dichromatism in Icterus and to attempt to understand causes of these changes by focusing on female behavior. Accounting for Different Kinds of Dichromatism and Monochromatism Many studies of sexual dichromatism in birds fail to account for the fact that dichromatism results from character complexes that involve both male and female coloration (e.g., Omland 1997). Dabbling ducks (Anas) and New World orioles exemplify two very different ways that monomorphism and dimorphism can occur. In the ducks, females of most species have “dull” mottled brown plumage (especially females of the widespread northern migratory species). In only a few tropical or southern species do females have some “bright” malelike patterning (e.g., Chiloe Wigeon [A. sibilatrix], White-cheeked Pintail [A. bahamensis]). Thus, in these ducks, female coloration is relatively conservative, and dichromatism is generally gained or lost by changes in male coloration. Males can be bright and elaborately patterned (e.g., Mallard [A. platyrhynchos;

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1 2 3 4 5 polymorphic equivocal

Spindalis Phaenicophilus Chlorospingus Nesospingus Piranga Chlorothraupis Habia Chlorophanes Heterospingus Chrysothlypis Hemithraupis Cnemoscopus Hemispingus Pyrrhocoma Thlypopsis Nephelornis Cypsnagra Ramphocelus Lanio Eucometis Tachyphonus Conothraupis Creurgops Nemosia Sericossypha Lamprospiza Mitrospingus Diglossa Oreomanes Xenodacnis Cyanerpes Dacnis Tersina Chlorornis Delothraupis Dubusia Anisognathus Buthraupis Calochaetes Chlorocrysa Tangara Schistoclamys Cissopis Neothraupis Iridosornis Thraupis Pipraeidea

Figure 10.9. Reconstruction of dichromatism in the family Thraupidae, showing dimorphism with colorful male and drab female (i.e., 3) as the most parsimonious ancestral state. Burns (1998a) coded the taxa as having five possible states: 1, monomorphic and drab; 2, monomorphic and colorful; 3, dimorphic with colorful male and drab female; 4, dimorphic with both sexes drab; and 5, dimorphic with both sexes colorful. Adapted from Burns (1998a).

Plate 15]), or males can be dull and female-like (e.g., Mottled Duck [A. fulvigula]). These duck species are generally either dimorphic or monomorphic dull. This group thus conforms to many of the implicit assumptions about how dichromatism is gained or lost, and it is reasonable to think about dichromatism coming and going with different strengths of sexual selection acting on males. It is also possible that levels of natural selection may vary among

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kevin e. oml and & christopher m. hofmann species and could account for the presence or absence of elaborate male plumage in spite of similar strengths of sexual selection acting on males. New World orioles, however, present almost the opposite situation. Males of all species have some sort of bright contrasting patterns and colors (Omland and Lanyon 2000). Although the specifics of which colors and patterns are expressed varies substantially, that males of all species express some form of bright plumage is very conserved. In contrast, female orioles range from bright (as elaborately colored as the males, e.g., Altamira Oriole), to dull (no hint of any saturated colors nor contrasting patterns, e.g., Orchard Oriole; Plate 30). Thus in these orioles, male brightness is conserved, and dichromatism is gained or lost by changes in female coloration. Orioles are either dichromatic or monochromatic bright. This genus thus does not conform well to frequent assumptions about how dichromatism evolves, and differences in dichromatism among oriole species cannot be simply explained by different strengths of sexual selection acting on males (see also Price and Birch 1996; Badyaev and Hill 2003). Dichromatism due to elaborate female coloration in polyandrous species is yet another type of dichromatism that requires an explanation. Many comparative studies have used dichromatism as an index of plumage color intensity—for example, to document a correlation between coloration and species richness (Barraclough et al. 1995; Owens et al. 1999; see also Panhuis et al. 2001). Other studies have used correlations between indices of dichromatism and different pigment classes to understand the evolution of coloration itself (e.g., Gray 1996; Owens and Hartley 1998; Chapter 9). Using dichromatism as an indicator of plumage brightness or strength of sexual selection needs to be approached with caution. A dichromatism index might work well in some groups in which many species are monomorphic dull and the most elaborately ornamented species are strongly dichromatic, such as dabbling ducks. However, using dichromatism as an index would presumably work poorly in New World orioles or other groups with monomorphic bright species (e.g., Trail 1990; Omland and Kondo, in press). Is There a Bias Toward Loss or Gain of Dichromatism? Many authors have suggested that there might be repeated instances of the loss of dichromatism in dabbling ducks, especially in the mallard lineage (e.g., Delacour and Mayr 1945; Sibley 1957; Livezey 1991). Mitochondrial DNA gene trees from Mallard and Black Ducks (Avise et al. 1990) show Black Ducks

Adding Color to the Past

genetically nested within Mallards, which Avise et al. attributed most likely to recent speciation and loss of dichromatism in the former. Omland (1997) reconstructed the history of dichromatism in the genus Anas and showed how different assumptions about the relative ease of gain or loss of dichromatism could lead to very different conclusions (Figure 10.10a). He reviewed seven lines of evidence that dichromatism in these ducks would be more likely to be lost than gained, including the genetic nature of dichromatism in ducks and biases toward the loss of any complex character (Omland 1997). An alternative hypothesis is that a monomorphic mallard colonized North America and speciated into several lineages, and only later did the dimorphic “greenheaded” Mallard colonize North America (Palmer 1976; McCracken et al. 2001; see also Johnson 1999; Kulikova et al. 2004; Figure 10.10b). In New World orioles and other groups in which there are not monochromatic dull species, it is less obvious why there might be a bias toward the repeated loss of dichromatism. In these species, there is no widely expressed base plumage. In Anas ducks, juveniles, females, and eclipse-plumaged males of most species all express predominantly mottled brown plumage (Omland 1997). However, in New World orioles, although juveniles of most species express relatively unpatterned plumage, there is no generally expressed female coloration, and no adult males ever express dull coloration. Thus, there is no obvious default plumage that might easily reappear in evolutionary transitions. All of these issues are amenable to empirical testing, especially by focusing on the genetic and developmental basis of plumage coloration (e.g., Theron et al. 2001; Mundy et al. 2004). Testing for any bias using only phylogenetic approaches is problematic, however, because most researchers start by assuming equal gain-loss probabilities and can be led astray if there is a strong biological bias for the repeated gain or repeated loss of a character state (Omland 1997; Cunningham 1999; Shultz and Churchill 1999). Unfortunately, determining whether gains or losses ought to be weighted more heavily, and if so, by how much, is difficult. Furthermore, the more rapidly character states can evolve, the less certainty we have in the ancestral reconstructions for any node or for the whole tree. All aspects of bird coloration—from overall dimorphism to individual plumage patches—can evolve rapidly and show high levels of homoplasy (Omland 1997; Omland and Lanyon 2000). The evolutionary history of such rapidly evolving characters may be difficult to reconstruct accurately (see Felsenstein 1973), especially for older radiations with long branches separating species. To obtain accurate ancestral reconstructions for such characteristics, detailed

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Ancestor Cairina moschata Cairina scutulata Pteronetta hartlaubi Aix sponsa Aix galericulata Chenonetta jubata Nettapus auritus Nettapus coromandelianus Nettapus pulchellus Amazonetta brasiliensis Callonetta leucophrys Lophonetta specularioides Speculanas specularis Anas capensis A. strepera A. falcata Wigeons A. sibilatrix A. penelope A. americana A. sparsa A. platyrhynchos A. wyvilliana A. laysanensis A. oustaleti A. fulvigula A. diazi Mallards A. rubripes A. undulata A. melleri A. luzonica A. superciliosa A. poecilorhyncha A. zonorhyncha A. discors A. cyanoptera A. smithii Blue-wings A. platalea A. clypeata A. rhynchotis A. bernieri A. gibberifrons Austral A. albogularis A. castanea Teal A. chlorotis A. aucklandica A. erythrorhyncha A. bahamensis A. flavirostris A. andium Pintails A. acuta A. eatoni A. georgica A. crecca A. carolinensis A. formosa A. querquedula Green-wings A. versicolor A. puna A. hottentota

Figure 10.10. (a) Reconstruction of dichromatism in the ducks (from Omland 1997), when losses of dichromatism occur five times more readily than gains. The phylogeny is Livezey’s (1991) morphological tree. Numbers refer to ancestral branches for main Anas groups and the Anas common ancestor, as discussed in the original paper. Adapted from Omland (1997). (b) Reconstruction of dichromatism in Anas ducks from Johnson (1999). This reconstruction uses simple unordered parsimony, which makes the implicit assumption that gains and losses of dichromatism are equally likely. The phylogeny is a molecular tree from Johnson and Sorenson (1998). Adapted from Johnson (1999). Note that both (a) Omland’s and (b) Johnson’s reconstructions show repeated evolutionary changes between dichromatism and monochromatism. Therefore, both reconstructions should imply a high degree of uncertainty about the states at many ancestral nodes.

b

Plumage dimorphism unordered monomorphic dimorphic equivocal

Figure 10.10. continued

Lophonetta specularioides Tachyeres pteneres Amazonetta brasiliensis Speculanas specularis Anas formosa A. querquedula A. versicolor A. hottentota A. platalea A. cyanoptera A. discors A. smithii A. clypeata A. rhynchotis A. strepera A. falcata A. penelope A. americana A. sibilatrix A. chlorotis A. capensis A. bahamensis A. erythrorhyncha A. georgica A. acuta A. castanea A. gibberifrons A. bernieri A. crecca A. carolinensis A. flavirostris A. sparsa A. undulata A. melleri A. platyrhynchos 2 A. rubripes A. fulvigula A. superciliosa A. laysanensis A. luzonica A. zonorhyncha A. poecilorhyncha A. platyrhynchos 1

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kevin e. oml and & christopher m. hofmann studies are needed of very closely related species using well-corroborated species trees. In our lab, we are evaluating strategies for testing mtDNA trees at the species level. Well-corroborated trees and accurate ancestral-state reconstructions are critical for a more complete understanding of color evolution in birds. We have used the terms “dull” and “bright” following the previous usage of these terms (e.g., Omland 1997; Badyaev and Hill 2003; see also Burns 1998a), but such terminology may not be as precise as would be ideal. There are many other related terms that also have their own uses and limitations (e.g., bright, colorful, conspicuous, patterned, elaborate, brilliant, ornamented, exaggerated; dull, drab, cryptic, inconspicuous, unpatterned). Although, “dull” and “bright” work quite well in ducks and orioles (because most species have sexes that can be binned into one of the extreme categories), many other groups are not so easily dichotomized. For example, Burns (1998a) used a much more complex scheme including five categories to reconstruct the history of dichromatism in the Thraupidae (Figure 10.9). The problem is that “dull” and “bright” are typically used without explicit analysis of the visual sensitivities of the birds (Chapter 1, Volume 1), without objective quantitative measures of color or pattern (Chapter 2, Volume 1), and without explicit consideration of the light environment and background coloration (Chapter 4, Volume 1). Furthermore, most studies of dichromatism have failed to address whether the dichromatism is caused by differences in pigmentary or structural colors. We believe that the continued usage of such terms can facilitate communication, but we strongly emphasize the need for awareness of the limitations of these terms. Furthermore, along with other authors of these volumes, we argue for further quantification of each of these aspects of color and vision. It is possible that quantification and new spectral analyses discussed below will eventually lead to completely new perspectives and terminology. Delayed Plumage Maturation The study of delayed plumage maturation (DPM; see also Chapters 2 and 3) could also benefit from the use of ancestral-state reconstruction. As with the related issue of sexual dichromatism, a phylogenetic perspective indicates that there are many possible pathways to the evolutionary gain and loss of DPM. Björklund (1991) used early phylogenies of nine-primaried oscines to reconstruct the history of DPM, and he suggested that delayed maturation was actually the ancestral state for many North American birds. Furthermore, his phylogenetic and mechanistic approach led him to suggest that delayed male

Adding Color to the Past

maturation might be caused by selection for neoteny in females. At a lower taxonomic level, Hill (1996) used a composite phylogeny to reconstruct DPM and carotenoid patch size for subspecies of the House Finch. He showed that DPM was a derived state that seemed to be associated with increased costliness of male ornamentation. Rigorous phylogenetic approaches to this topic are needed in genera that vary in such characters as molt timing and coloration that contribute to DPM.

Reconstructing Spectral Color Data Reflectance spectrometry is a relatively new tool in avian color research (Chapter 2, Volume 1); quantitative spectral data have yet to be employed in studies that use ancestral-state reconstruction. These methods can provide reflectance data for the full sensitivity range of avian visual systems (i.e., well into the UV for many birds; Chapter 1, Volume 1). Spectrometers allow researchers to quantify objective measures of avian color and are being used increasingly in a wide range of color studies (see reviews throughout this volume). This increase in quantitative ability, however, raises interesting new issues regarding ancestral-state reconstruction. Avian coloration is a composite character produced by a variety of proximate mechanisms (Badyaev et al. 2001; Saks et al. 2003), and a single reflectance spectrum contains information about multiple perceptual aspects of color (including hue, chroma, and brightness; Endler 1990). These factors, as well as the assumptions and methods of character mapping, need to be carefully considered when reconstructing color evolution. Here we address three ways that color data can be reconstructed: (1) discrete unordered, (2) discrete ordered, and (3) continuous. Researchers should choose which of these reconstruction methods to use based on the observed variability in spectral data and knowledge of the mechanistic basis of the colors being measured. Ancestral-state reconstructions often treat color as a discrete unordered qualitative character: for example, black, white, or colored (Omland and Lanyon 2000) and red or yellow (Hill and McGraw 2004). Other, more quantitative aspects of color may also be reconstructed as discrete characters. Figure 10.11 illustrates a hypothetical example for which spectra only occur in discrete intervals at 500 nm (short), 550 nm (medium) and 600 nm (long)— corresponding approximately to the human perception of yellow, orange, and red hues. (For a similar example using sound spectrograms, see Price and Lanyon 2002). Ideally, something would be known about the pigments or

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Figure 10.11. A hypothetical set of color measurements for which spectral location might be reconstructed as a discrete character. In this example, spectra occur in three discrete groups with reflectance midpoints at short (500 nm), middle (550 nm), and long (600 nm) wavelengths.

mechanisms used to produce these colors. If it was known that these spectra are produced by three different pigments or by different mechanisms (e.g., pigments versus structure) and intermediates are not found, then these spectral data should be reconstructed as a discrete unordered character. Figure 10.12 reconstructs the data from Figure 10.11 onto a hypothetical phylogeny using simple parsimony. Reconstructing spectra in this way assumes that going from the short to the long wavelengths does not require going through the middle wavelength (e.g., if a single metabolic step could convert a yellow pigment to an orange or a red; Brush 1990, McGraw et al. 2003). However, if going from a short wavelength to a long wavelength requires going through a middle wavelength (e.g., if orange pigments are formed as intermediates between yellow and red ones), then these spectral data should be reconstructed as a discrete ordered character. In Figure 10.13, the same data are reconstructed onto the same tree, but as an ordered character, which changes the reconstruction: the ancestor at node B now has an equivocal ancestral state. In this case, going from a long wavelength to a short wavelength requires two steps. It is equally likely that the ancestor at node A had a middlewavelength color with a change to short wavelength occurring in the branch to Taxon 6 (with the second change from middle to long occurring in the

Adding Color to the Past

445 Taxon 1

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Figure 10.12. Reconstruction of the spectra illustrated in Figure 10.11 as discrete unordered characters. Two nodes, A and B, are highlighted. Node A is reconstructed as having a middlewavelength reflectance midpoint. Node B is reconstructed as having a long-wavelength reflectance midpoint that was subsequently lost by Taxon 6.

branch to Taxon 5). These two figures illustrate how different assumptions about character evolution can alter the reconstruction of ancestral states. When aspects of color seem likely to evolve in a continuous manner, these characters should be reconstructed using continuous methods. Again, this choice could be based on observed variability or knowledge of the proximate mechanisms underlying color production. For example, preliminary data from New World orioles suggest continuous variability among yellows, oranges, and reds of many species in the genus Icterus (C. M. Hofmann, T. W. Cronin, and K. E. Omland, unpubl. data). When reconstructing a continuous character, the assumption is made that all intermediates are possible and that going from one state to another requires evolving through these intermediates (Martins 1999). A full range of intermediates could occur if color is produced by a mixture of pigments for which varying the concentration of one pigment relative to another shifts the hue toward longer or shorter wavelengths.

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Figure 10.13. Reconstruction of the spectra illustrated in Figure 10.11 as a discrete ordered character. Node A is still reconstructed as having a middle-wavelength reflectance midpoint, but it is equally parsimonious to reconstruct node B as having a long- or middle-wavelength reflectance midpoint. In this case, the change from a long- to short-wavelength reflectance midpoint requires two steps, and it is equally parsimonious that two single step changes occurred (a change from a middle- to a long-wavelength reflectance midpoint on the branch to Taxon 5 and a change from a middle- to a short-wavelength reflectance midpoint on the branch to Taxon 6) or that a single two-step change occurred (a change from a long to a short wavelength on the branch to Taxon 6).

Figure 10.14 reconstructs the same spectral data from Figure 10.11 as a continuous character. In this case, the reconstructed ancestral state at node A is 540 nm and node B is 557 nm. However, the original spectral data do not fit the assumptions of continuous character evolution, and as a result, most ancestral nodes are reconstructed with values very different from any of the extant taxa. The original data suggest that it may be possible to go from 500 nm to 550 nm in a single step (e.g., by oxidizing a pigment; Brush 1990), so that reconstructing color as a continuous character as in Figure 10.14 is likely misleading for this hypothetical example. We emphasize that, although reflectance spectra allow any color to be measured in a continuous manner, there are many cases in which reconstructing the

Adding Color to the Past

447 Taxon 1

Taxon 2 508

Taxon 3

516

A Taxon 4

540

Taxon 5

553

570 short (500 nm) middle (550 nm) long (600 nm)

Taxon 6

B 557

Taxon 7

Figure 10.14. Reconstruction of the spectra illustrated in Figure 10.11 as a continuous character. Node A is reconstructed as having a reflectance midpoint of 540 nm. Node B is reconstructed at 557 nm. Note that the reconstructed reflectance midpoints at the ancestral nodes are not expressed in any of the extant taxa. Reconstructed using squared change parsimony. All spectral character mapping done using MacClade (Maddison and Maddison 2000).

characters as continuous would be inappropriate. An obvious example would be when two distinct classes of pigments are present, such as a reddish brown phaeomelanin and a yellow carotenoid. Although their colors can be scored on a continuous scale, they are produced by two very different mechanisms, and reconstructing them as continuous would likely lead to false conclusions. Careful “tree thinking” and attention to the assumptions of ancestral-state reconstruction are likely to yield important and new insights when applied to spectral data.

Summary Ancestral-state reconstruction provides a method to study the evolutionary history of avian color, by allowing the researcher to infer the color of ancestral lineages. In addition, a phylogenetic approach provides valuable perspective

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when framing virtually any question related to bird color. This chapter examined how character mapping has been used to investigate individual plumage patches, overall plumage patterns, and sexual dichromatism. Throughout this chapter, we emphasized that different assumptions about character evolution— such as equal gains and losses or character state continuity—may alter phylogenetic reconstructions. Finally, we outlined a framework for determining how spectral data can be reconstructed and addressed some of the challenges presented by these new quantitative data on bird color. In each of these areas, many important questions remain. As more species-level phylogenies become available, ancestral-state reconstruction will play an increasing role in our understanding of avian color evolution.

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II Acknowledgments Contributors Species Index Subject Index

Acknowledgments

For his tremendous help and support in all phases of this project, we give special thanks to Bob Montgomerie. More than anyone else, Bob helped us scale back our preliminary ideas for a review of the colors of all vertebrates to a more focused book on birds. Bob also took charge of the enormous task of redrawing every black and white illustration in this book and overseeing the legends for all figures. Noah Strycker drew the black and white vignettes that make the graphs and charts of the book much more attractive. Members of the Hill lab gave sound advice on the topics to include in the book. Two anonymous referees commented on an earlier version of the book. We thank the chapter authors for sticking to deadlines, for accepting sometimes heavyhanded editing, and for serving as reviewers and the quality control for all of the chapters in the two volumes. During book preparation, Geoffrey Hill was supported by National Science Foundation grants DEB0077804 and IBN0235778 and Kevin McGraw was supported by the College of Liberal Arts and Sciences and the School of Life Sciences at Arizona State University, Tempe.

Chapter 1 First and foremost, I recognize the intellectual stimulation and support of my friends and colleagues Juan José Negro and Julio Blas. Sam Kelly provided invaluable technical help. I am grateful to the Natural Sciences and Engineering Research Council of Canada for supporting my research over the years.

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Chapter 2 Thanks very much to Peter Buston, Bernie Crespi, Emily DuVal, Geoff Hill, Dov Lank, Mark Hauber, Kevin McGraw, Bob Montgomerie, Patrik Nosil, Anders Ödeen, Elizabeth Tibbetts, and the “FAB” Evolution Group (Simon Fraser University) for extremely helpful discussion and comments on the manuscript, to the curators of the vertebrate collections at Cornell University, Ithaca, and the University of British Columbia, Vancouver, for access to their specimens, and to Mark Hipfner and the 2003 field crew at Triangle Island, British Columbia, for help scoring murre eggs.

Chapter 3 I am most grateful to Geoffrey Hill, Kevin McGraw, Lluïsa Arroyo, and Joan Saldaña for critically reading the manuscript. I also thank Joan Saldaña for writing the text of the model displayed in the boxes and Olaf Leimar for his comments on its content. Pedro Cordero provided the House Sparrow data in Figure 3.8. This work was supported by research project BOS2003-09589 from the Spanish Research Council, Ministerio de Ciencia y Tecnología.

Chapter 4 Bob Montgomerie, Trond Amundsen, Kevin McGraw, and members of the Hill Lab read and provided comments on this chapter. While this chapter was being written, I was supported by National Science Foundation grants DEB007804, IBN0235778, and IBN9722971.

Chapter 5 I thank Rufus Johnstone, Nick Davies, and Martin Fowlie for discussions; Geoff Hill and an anonymous reviewer for comments on an earlier chapter draft; Bruce Lyon and Justin Schuetz for generously providing photographs to illustrate the chapter; and Claire Spottiswoode for her help with phylogenies. I was supported by a Royal Society University Research Fellowship and co-funded by Biotechnology and Biological Sciences Research Council grant S/S12981.

Chapter 6 We thank Staffan Andersson, Rob Brooks, Geoff Hill, John Hunt, Val Olsen, Ian Owens, Tim Parker, and Ben Sheldon for useful discussions or comments

Acknowledgments

on earlier versions. Simon Griffith has until recently been supported by Fellowships from the Natural Environment Research Council and the Royal Society (UK). Sarah Pryke is currently supported by a New South Global Postdoctoral Fellowship.

Chapter 7 We have benefited from discussions about female ornaments in birds with a large number of colleagues, especially Elisabet Forsgren, Bo Hansen, Arild Johnsen, Jan Terje Lifjeld, Roy Mangersnes, Percy Rohde, and Per Terje Smiseth. We thank Geoff Hill and Becky Kilner for constructive comments on a previous version of the manuscript, Geoff Hill and Kevin McGraw for editorial assistance and patience during the preparation of the chapter, and the Research Council of Norway for financial support of our studies of female coloration.

Chapter 8 I thank Jason Wolf, Tobias Uller, Allen Moore, Gunter Wagner, Joanna Masel, Renee Duckworth, Joachim Hermisson, Rick Prum, and Michael Whitlock for discussions; Kevin Oh, Dana Seaman, Rebecca Young, and the participants in the “Concepts in Developmental Evolution” seminar at the University of Arizona, Tucson, for thorough comments on the manuscript; and Geoff Hill and Kevin McGraw for the invitation to contribute to this volume. This work was partially supported by National Science Foundation grants and the University of Arizona.

Chapter 9 I thank Malte Andersson, Kate Arnold, Alex Badyaev, Peter Bennett, Sonya Clegg, Simon Griffith, Nathan Hart, Ian Hartley, Fran Hausmann, Geoff Hill, Becky Kilner, Justin Marshall, Melinda McNaught, Val Olson, Daniel Osorio, Ally Phillimore, and Devi Stuart-Fox for discussion, comments, and collaboration.

Chapter 10 We thank Geoff Hill and Kevin McGraw for the invitation to contribute to this book. Tom Cronin has provided valuable guidance regarding spectral

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Acknowledgments

analysis and color in general. Kevin Omland is supported by National Science Foundation grant DEB-0347083. Spring Ligi and Ian Tracy helped compile references. Geoff Hill, Elizabeth Humphries, Rebecca Kimball, Scott Lanyon, Megan Porter, Jordan Price, and Sonja Scheffer provided helpful comments on the manuscript.

Contributors

trond amundsen Department of Biology Norwegian University of Science and Technology NO 7491 Trondheim Norway [email protected]

alexander v. badyaev Department of Ecology and Evolutionary Biology University of Arizona Tucson, Arizona 85721-0088 USA [email protected]

gary r. bortolot ti Department of Biology University of Saskatchewan 112 Science Place Saskatoon, Saskatchewan S7N 5E2 Canada [email protected]

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james dale Department of Biological Sciences Simon Fraser University 8888 University Drive Burnaby, British Columbia V5A 1S6 Canada [email protected]

simon c. griffith School of Biological, Earth and Environmental Sciences University of New South Wales Sydney 2052, New South Wales Australia [email protected]

geoffrey e. hill Department of Biological Sciences 331 Funchess Hall Auburn University Auburn, Alabama 36849 USA [email protected]

christopher m. hofmann Department of Biological Science University of Maryland—Baltimore County Baltimore, Maryland 21250 USA [email protected]

rebecca m. kilner Department of Zoology University of Cambridge Downing Street Cambridge CB2 3EJ United Kingdom [email protected]

Contributors

kevin j. m c graw School of Life Sciences Arizona State University Tempe, Arizona 85287-4501 USA [email protected]

kevin e. oml and Department of Biological Science University of Maryland—Baltimore County Baltimore, Maryland 21250 USA [email protected]

ian p. f. owens Division of Biology and Natural Environment Research Council Centre for Population Biology Imperial College London Silwood Park Ascot, Berkshire SL5 7PY United Kingdom [email protected]

henrik pärn Department of Biology Norwegian University of Science and Technology NO 7491 Trondheim Norway [email protected]

sarah r. pryke School of Biological, Earth and Environmental Sciences University of New South Wales Sydney 2052, New South Wales Australia [email protected]

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Contributors

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juan carlos senar U. A. Ecología Evolutiva y de la Conducta, C.S.I.C. Museu Ciències Naturals P. Picasso s/n Parc Ciutadella 08003 Barcelona Spain [email protected]

Species Index

Acanthiza chrysorrhoa. See Yellow-rumped Thornbill Acanthiza reguloides. See Buff-rumped Thornbill Accipiter bicolor. See Bicolored Hawk Accipiter nisus. See Sparrowhawk Acrocephalus scirpaceus. See Reed Warbler Actitis macularia. See Spotted Sandpiper Aechmophorus occidentalis. See Western Grebe Aethia cristatella. See Crested Auklet Aethia pusilla. See Least Auklet African Penguin, 90 Agelaius phoeniceus. See Red-winged Blackbird Agelaius tricolor. See Tricolored Blackbird Ajaja ajaja. See Roseate Spoonbill Alectoris rufa. See Red-legged Partridge Alpine Accentor, 325 Altamira Oriole, 429 Amandava subflava. See Goldbreast American Avocet, 24 American Bittern, 16 American Coot, 210, 217, 219 American Crow, 36, 74 American Goldfinch, 48, 104, 140, 146, 155, 163, 250, 253, 314, 318 American Kestrel, 26 American Redstart, 93, 121, 257 Amethyst-throated Sunangel, 308 Anas acuta. See Northern Pintail Anas bahamensis. See White-cheeked Pintail Anas fulvigula. See Mottled Duck Anas platyrhynchos. See Mallard Anas rubripes. See Black Duck Anas sibilatrix. See Chiloe Wigeon Anous stolidus. See Brown Noddy Aplomado Falcon, 12 Aptenodytes patagonicus. See King Penguin

465

Aratinga cyanogenus. See Blue-crowned Conure Arctic Skua. See Parasitic Jaeger Arctic Tern, 69, 205 Arenaria interpres. See Ruddy Turnstone Arenaria melanocephala. See Black Turnstone Aurora Finch, 212 Baltimore Oriole, 120, 418, 426, 429, 432 Bananaquit, 359 Bank Swallow, 208 Barn Owl, 163, 247, 296, 301–302, 305, 316, 322, 405 Barn Swallow, 47, 142, 144, 166–167, 175, 177, 296, 298, 316, 318, 405 Bar-tailed Godwit, 300, 301 Bat Falcon, 12 Bearded Reedling. See Bearded Tit Bearded Tit, 211, 318 Beautiful Sunbird, 201 Bicolored Hawk, 29 Black Duck, 435, 438 Black Redstart, 121 Black Swan, 296, 316 Black Tern, 205 Black Turnstone, 24 Black-backed Oriole, 426 Black-billed Magpie, 212, 298, 300 Black-capped Chickadee, 90, 98, 104, 144, 178 Black-headed Grosbeak, 121, 239 Blue Grosbeak, 144, 172, 238, 239, 240, 246 Blue Jay, 70 Blue Tit, 13, 47, 91, 142, 144, 169, 173, 174, 215–217, 234, 241, 298, 301, 314, 316 Blue-crowned Conure, 11 Blue-footed Booby, 146, 182, 316, 322

Species Index

466 Bluethroat, 144, 148, 169, 185, 247, 257, 261, 262, 284, 295, 296, 300, 302, 303, 305, 308, 312, 315, 316, 320, 321, 323, 324 Bobolink, 20, 257 Bombycilla cedrorum. See Cedar Waxwing Botaurus lentiginosus. See American Bittern Brachyramphus marmoratus. See Marbled Murrelet Bridled Tern, 205 Brown Noddy, 205–206 Brown Songlark, 212 Brown-headed Cowbird, 48 Bucephala clangula. See Common Goldeneye Budgerigar, 142, 146, 169, 179, 180, 316, 319 Buff-rumped Thornbill, 202 Bullock’s Oriole, 234, 235, 257 Burrowing Parrot, 146, 180, 296, 304, 316 Buteo albonotatus. See Zone-tailed Hawk Buteo buteo. See Common Buzzard Buteo jamaicensis. See Red-tailed Hawk Cactus Finch, 140, 163 Calandra Lark, 202 Capuchinbird, 300, 308, 310 Cardinalis cardinalis. See Northern Cardinal Cardinalis sinuatus. See Pyrrhuloxia Carduelis chloris. See Eurasian Greenfinch Carduelis sinica. See Oriental Greenfinch Carduelis spinus. See Eurasian Siskin Carduelis tristis. See American Goldfinch Carpodacus erythrinus. See Common Rosefinch[AQ1] Carpodacus mexicanus. See House Finch Caspian Tern, 204–207 Cathartes aura. See Turkey Vulture Catoptrophorus semipalmatus. See Willet Cedar Waxwing, 121, 296, 299, 361 Centropus phasianus. See Pheasant Coucal Cercotrichas galactotes. See Rufous Bush Chat Chaffinch, 16, 21–22, 91, 93, 98 Chalcites lucidus. See Shining Bronze-cuckoo Charadrius alexandrinus. See Kentish Plover Charadrius morinellus. See Eurasian Dotterel Charadrius vociferus. See Killdeer Chasiempis sandwichensis. See Elepaio Chen caerulescens. See Snow Goose Chestnut-sided Warbler, 142, 167 Chiloe Wigeon, 436 Chiroxiphia linearis. See Long-tailed Manakin Chlidonias hybridus. See Whiskered Tern Chlidonias leucopterus. See White-winged Tern Chlidonias niger. See Black Tern Chloebia gouldiae. See Gouldian Finch

Ciconia ciconia. See White Stork Cinclorhamphus cruralis. See Brown Songlark Cinclus cinclus. See White-throated Dipper Cirl Bunting, 251 Coal Tit, 91 Coccothraustes vespertinus. See Evening Grosbeak Coereba flaveola. See Bananaquit Clamator glandarius. See Great-spotted Cuckoo Cliff Swallow, 63, 208 Colaptes auratus. See Northern Flicker Collared Flycatcher, 47, 56, 90, 108, 140, 177–178, 238, 244, 246, 256, 257, 258, 264, 265, 266, 397 Columba livia. See Rock Pigeon Common Buzzard, 146, 184, 316 Common Canary, 203, 210, 219, 221 Common Cuckoo, 202, 224 Common Eider, 204 Common Goldeneye, 296 Common Hawk-cuckoo, 29 Common Moorhen, 210 Common Murre, 64–65 Common Raven, 11, 220 Common Redpoll, 104, 362 Common Rosefinch, 140, 362 Common Shelduck, 148, 186, 296, 316 Common Tern, 205–207 Common Yellowthroat, 93, 140, 163, 164, 256, 257 Corn Bunting, 91 Corvus brachyrhynchos. See American Crow Corvus corax. See Common Raven Corvus ossifragus. See Fish Crow Crested Auklet, 287, 298, 309, 311, 318, 321 Crested Caracara, 12 Crested Lark, 211 Cuculus canorus. See Common Cuckoo Cuculus poliocephalus. See Little Cuckoo Cuculus saturatus. See Oriental Cuckoo Cuculus varius. See Common Hawk-cuckoo Cyanocitta cristata. See Blue Jay Cyanoliseus patagonus. See Burrowing Parrot Cygnus atratus. See Black Swan Cygnus olor. See Mute Swan Dark-eyed Junco, 91, 93, 94, 98, 104, 140, 177, 218, 307, 309, 318, 319 Dendroica pennsylvanica. See Chestnut-sided Warbler Dendroica chrysoparia. See Golden-cheeked Warbler Dendroica coronata. See Yellow-rumped Warbler Dendroica petechia. See Yellow Warbler

Species Index Dolichonyx oryzivorous. See Bobolink Domestic Chicken. See Red Junglefowl Double-bar Finch, 146, 152 Dunnock, 211, 220–221, 223 Eastern Bluebird, 47, 142, 144, 167, 173–174, 247, 257, 298, 301, 305, 318 Eastern Kingbird, 24 Eastern Swamphen, 23 Eclectus Parrot, 216, 285 Eclectus roratus. See Eclectus Parrot Egretta garzetta. See Little Egret Egretta thula. See Snowy Egret Elepaio, 120 Emberiza calandra. See Corn Bunting Emberiza cirlus. See Cirl Bunting Emberiza citrinella. See Yellowhammer Emberiza schoeniclus. See Reed Bunting Empidonax traillii. See Willow Flycatcher Erithacus rubecula. See Robin Erythrura psittacea. See Red-throated Parrotfinch Eudocimus albus. See White Ibis Eudocimus ruber. See Scarlet Ibis Eulampis jugularis. See Purple-throated Carib Euplectes ardens. See Red-collared Widowbird Euplectes axillaris. See Red-shouldered Widowbird Eurasian Blackbird, 22, 146, 181, 202–203, 218, 252, 253 Eurasian Bullfinch, 362 Eurasian Coot, 209 Eurasian Dotterel, 285, 300, 308, 310, 316, 322 Eurasian Golden Oriole, 11 Eurasian Greenfinch, 47, 91, 104, 250, 253, 301 Eurasian Kestrel, 14, 117, 120, 142, 167, 246 Eurasian Siskin, 43, 46, 47, 91, 92, 93, 96, 97, 98, 100, 104, 105, 107, 109, 110, 111, 112, 113, 121, 140, 155, 163 European Bee-eater, 216–217 European Serin, 104, 252 European Shag, 287, 298, 318 European Starling, 9, 142, 144, 169, 172, 203, 298, 306, 307, 309, 310, 316 Eurypyga helias. See Sunbittern Evening Grosbeak, 104 Falco cherrug. See Saker Falcon Falco columbarius. See Merlin Falco deiroleucus. See Orange-breasted Falcon Falco femoralis. See Aplomado Falcon Falco mexicanus. See Prairie Falcon Falco naumanni. See Lesser Kestrel Falco peregrinus. See Peregrine Falcon

467 Falco punctatus. See Mauritius Kestrel Falco rufigularis. See Bat Falcon Falco sparverius. See American Kestrel Falco tinnunculus. See Eurasian Kestrel Falco vespertinus. See Red-footed Falcon Ficedula albicollis. See Collared Flycatcher Ficedula hypoleuca. See Pied Flycatcher Ficedula semitorquata. See Semi-collared Flycatcher Fish Crow, 74 Fregata magnificens. See Magnificent Frigatebird Fregata minor. See Great Frigatebird Fringilla coelebs. See Chaffinch Fulica americana. See American Coot Fulica atra. See Eurasian Coot Fulmarus glacialis. See Northern Fulmar Galerida cristata. See Crested Lark Gallinago media. See Great Snipe Gallinula chloropus. See Common Moorhen Gallus gallus. See Red Junglefowl Gasterosteus aculeatus. See Three-spined Stickleback Gelochelidon nilotica. See Gull-billed Tern Geospiza fortis. See Medium Ground Finch Geospiza scandens. See Cactus Finch Geothylpis trichas. See Common Yellowthroat Glaucidium gnoma. See Northern Pygmy-owl Goldbreast, 216 Golden-cheeked Warbler, 13 Gorgeous Bush-shrike, 201 Gouldian Finch, 146, 184, 185, 214, 314, 318, 319 Great Crested Grebe, 218, 283 Great Frigatebird, 146, 182 Great Kiskadee, 13 Great Snipe, 144, 177 Great Tit, 14, 91, 93, 95, 98, 99, 104, 112, 140, 162, 186, 210, 222–223, 238–239, 251, 254, 296, 300, 301, 304, 307, 308, 322 Greater Bird-of-Paradise, 396 Greater Flamingo, 11 Greater Golden Plover, 239 Greater Honeyguide, 66 Greater Painted-snipe, 256, 285 Great-spotted Cuckoo, 212 Gull-billed Tern, 205 Guppy, 150, 176 Gymnorhinus cyanocephalus. See Pinyon Jay Harpagus diodon. See Rufous-thighed Kite Harris’ Sparrow, 62, 91, 93, 98, 99, 103, 104, 307, 309 Heliangelus exortis. See Tourmaline Sunangel

Species Index

468 Heliangelus viola. See Amethyst-throated Sunangel Hemichromis bimaculatus. See Rainbow Darter Hirundo rustica. See Barn Swallow Hooded Pitohui, 28, 432 Hooded Warbler, 309 Hooded Vulture, 12 House Finch, 43, 46, 47, 91, 93, 98, 104, 121, 122, 153–154, 157, 165, 176, 186, 234, 243, 246, 250, 253, 268, 284, 285, 298, 300, 301, 303, 304, 307, 314, 315, 318, 322, 363, 428, 443 House Sparrow, 47, 91, 93, 98, 103, 104, 105, 106, 108, 109, 110, 112, 140, 142, 158, 160–162, 165, 234, 235, 238, 239, 247, 252, 253, 255, 256, 257, 264, 265, 268, 287 Humboldt Penguin, 24 Icterus abeillei. See Black-backed Oriole Icterus bullockii. See Bullock’s Oriole Icterus galbula. See Baltimore Oriole Icterus gularis. See Altamira Oriole Icterus parisorum. See Scott’s Oriole Icterus spurius. See Orchard Oriole Inca Tern, 287, 296, 300, 301, 304 Indian Peafowl, 6, 25, 59, 396 Indicator indicator. See Greater Honeyguide Indigo Bunting, 119, 120, 257 Javan Munia, 315, 318 Juan Fernandez Firecrown, 286 Junco hyemalis. See Dark-eyed Junco Kentish Plover, 90, 142, 163 Killdeer, 66–67 King Penguin, 146, 179–180 Lagonosticta senegala. See Red-billed Firefinch Lagopus lagopus. See Willow Ptarmigan Lagopus muta. See Rock Ptarmigan Lanius ludovicianus. See Loggerhead Shrike Larosterna inca. See Inca Tern Lazuli Bunting, 51, 53, 120 Least Auklet, 90, 93, 98, 287, 296, 300, 304, 308, 311, 315, 316 Lesser Crested Tern, 205 Lesser Kestrel, 12, 296, 299, 300, 304 Limosa lapponica. See Bar-tailed Godwit Little Cuckoo, 213 Little Egret, 11 Little Tern, 205 Loddigesia mirabilis. See Marvelous Spatuletail

Loggerhead Shrike, 13 Lonchura leucogastroides. See Javan Munia Long-tailed Finch, 52 Long-tailed Manakin, 120 Loxia leucoptera. See White-winged Crossbill Luscinia svecica. See Bluethroat Magellanic Penguin, 296, 316 Magnificent Frigatebird, 201 Mallard, 142, 144, 146, 166, 172, 181, 250, 253, 380, 436, 438–439 Malurus cyaneus. See Superb Fairy-wren Malurus melanocephalus. See Red-backed Fairy-wren Marbled Murrelet, 69 Marvelous Spatuletail, 201 Mauritius Kestrel, 12 Medium Ground Finch, 121, 142, 163 Megadyptes antipodes. See Yellow-eyed Penguin Melanocorypha calandra. See Calandra Lark Meleagris gallopavo. See Wild Turkey Melopsittacus undulatus. See Budgerigar Melospiza melodia. See Song Sparrow Merganetta armata. See Torrent Duck Merlin, 21 Merops apiaster. See European Bee-eater Mimus polyglottos. See Northern Mockingbird Molothrus ater. See Brown-headed Cowbird Monteiro’s Hornbill, 241–242 Mottled Duck, 437 Mountain Sheep, 101 Mute Swan, 120 Necrosyrtes monachus. See Hooded Vulture Nectarinia johnstoni. See Scarlet-tufted Malachite Sunbird Nectarinia pulchella. See Beautiful Sunbird Neochmia modesta. See Plum-headed Finch Northern Cardinal, 43, 46, 47, 91, 93, 140, 142, 156, 163, 238, 239, 246, 284, 285, 287, 288, 298, 300, 303, 315, 322 Northern Flicker, 51–52, 316 Northern Fulmar, 316 Northern Mockingbird, 24 Northern Pintail, 144, 146, 172, 178, 435 Northern Pygmy-owl, 27 Numenius phaeopus. See Whimbrel Numida meleagris. See Helmeted Guineafowl Orange-breasted Bunting, 120 Orange-breasted Falcon, 12 Orchard Oriole, 120, 142, 167, 432

Species Index Oriental Cuckoo, 213, 224 Oriental Greenfinch, 104 Oriolus oriolus. See Eurasian Golden Oriole Osprey, 9 Ovis canadensis. See Mountain Sheep Painted Bunting, 119, 120 Pandion haliaetus. See Osprey Panurus biarmicus. See Bearded Tit Paradisaea apoda. See Greater Bird-of-Paradise Parasitic Jaeger, 146, 183, 296, 314, 316, 359, 405 Parus ater. See Coal Tit Parus caeruleus. See Blue Tit Parus major. See Great Tit Parus montanus. See Willow Tit Passer domesticus. See House Sparrow Passerina amoena. See Lazuli Bunting Passerina caerulea. See Blue Grosbeak Passerina ciris. See Painted Bunting Passerina cyanea. See Indigo Bunting Passerina leclancher. See Orange-breasted Bunting Pavo cristatus. See Indian Peafowl Pekin Robin. See Red-billed Leiothrix Peregrine Falcon, 25 Perissocephalus tricolor. See Capuchinbird Petrochelidon pyrrhonota. See Cliff Swallow Petronia petronia. See Rock Petronia Phaethon rubricauda. See Red-tailed Tropicbird Phalacrocorax aristotelis. See European Shag Phalacrocorax guimardi. See Red-legged Shag Phalaropus lobatus. See Red-necked Phalarope Pharomacrus mocinno. See Resplendent Quetzal Phasianus colchicus. See Ring-necked Pheasant Pheasant Coucal, 204 Pheucticus melanocephalus. See Black-headed Grosbeak Philomachus pugnax. See Ruff Phoenicopterus ruber. See Greater Flamingo Phoenicurus ochruros. See Black Redstart Phylloscopus inornatus. See Yellow-browed Leaf Warbler Pica pica. See Black-billed Magpie Pied Flycatcher, 17, 21–22, 56, 117, 121, 140, 144, 146, 158–168, 177–178, 238, 240, 246, 251, 253, 296, 301, 310, 397 Pied-billed Grebe, 217–218 Pinyon Jay, 144, 298, 299, 308, 312, 316, 327 Pitangus sulphuratus. See Great Kiskadee Pitohui dichrous. See Hooded Pitohui Pitohui kirhocephalus. See Variable Pitohui Pitta superba. See Superb Pitta

469 Ploceus cucullatus. See Village Weaver Plum-headed Finch, 211 Pluvialis apricaria. See Greater Golden Plover Podiceps cristatus. See Great-creasted Grebe Podilymbus occipitalis. See Silvery Grebe Podilymbus podiceps. See Pied-billed Grebe Poecile atricapillus. See Black-capped Chickadee Poephila acuticauda. See Long-tailed Finch Polyborus plancus. See Crested Caracara Porphyrio porphyrio. See Eastern Swamphen Prairie Falcon, 12 Progne subis. See Purple Martin Prunella collaris. See Alpine Accentor Prunella modularis. See Dunnock Ptilonorhynchus violaceous. See Satin Bowerbird Purple Martin, 120, 257 Purple-throated Carib, 308 Pyrrhula pyrrhula. See Eurasian Bullfinch Pyrrhuloxia, 368 Pytilia phoenicoptera. See Aurora Finch Quelea quelea. See Red-billed Quelea Rainbow Darter, 138 Recurvirostra americana. See American Avocet Red Junglefowl, 10, 142, 149, 165–166, 204, 243, 296, 307, 308, 316, 322, 353, 406 Red-backed Fairy-wren, 121, 140, 155 Red-billed Firefinch, 214, 216 Red-billed Leiothrix, 142, 169 Red-billed Quelea, 44, 45, 61, 72–73 Red-collared Widowbird, 90, 93, 95, 111, 140, 157, 238, 241 Red-footed Falcon, 12 Red-legged Partridge, 13 Red-legged Shag, 63 Red-necked Phalarope, 90, 144, 146, 172, 181 Red-shouldered Widowbird, 90, 93, 140, 157, 238 Red-tailed Hawk, 17 Red-tailed Tropicbird, 287, 298, 318 Red-throated Parrotfinch, 214 Red-winged Blackbird, 16, 90, 93, 140, 149, 170, 237, 238, 250, 253, 257, 298, 300, 307, 309, 318, 397, 427–428 Reed Bunting, 220 Reed Warbler, 202, 210–211, 221, 223 Resplendent Quetzal, 201 Ring-necked Pheasant, 90, 144, 146, 172, 181 Riparia riparia. See Bank Swallow Robin, 221, 223 Rock Petronia, 286, 298, 300, 316, 322

Species Index

470 Rock Pigeon, 25, 316 Rock Ptarmigan, 17, 68 Roseate Spoonbill, 11 Roseate Tern, 205 Rostratula benghalensis. See Greater Painted-snipe Royal Tern, 63–64, 205–207 Ruddy Turnstone, 63 Ruff, 36, 53–54, 61, 72, 74, 108, 260 Rufous Bush Chat, 148, 186 Rufous-thighed Kite, 29 Saker Falcon, 12 Sandwich Tern, 14, 205 Satin Bowerbird, 252 Scarlet Ibis, 11 Scarlet-tufted Malachite Sunbird, 90, 237, 238, 312 Scissor-tailed Flycatcher, 318 Scott’s Oriole, 432 Semi-collared Flycatcher, 56 Sephanoides fernandensis. See Juan Fernandez Firecrown Serinus canaria. See Common Canary Serinus serinus. See European Serin Setophaga ruticilla. See American Redstart Shining Bronze-cuckoo, 202 Sialia sialis. See Eastern Bluebird Silvery Grebe, 218 Snow Goose, 71, 146, 183, 316, 359, 405 Snowy Egret, 67 Spheniscus demersus. See African Penguin Spheniscus magellanicus. See Magellanic Penguin Somateria mollissima. See Common Eider Song Sparrow, 11 Southern Emu-wren, 216 Sparrowhawk, 21 Spheniscus humboldti. See Humboldt Penguin Spotted Sandpiper, 326 Stercorarius parasiticus. See Parasitic Jeager Sterna albifrons. See Little Tern Sterna anaethetus. See Bridled Tern Sterna bengalensis. See Lesser Crested Tern Sterna bergii. See Swift Tern Sterna caspia. See Caspian Tern Sterna dougallii. See Roseate Tern Sterna hirundo. See Common Tern Sterna maxima. See Royal Tern Sterna paradisaea. See Arctic Tern Sterna repressa. See White-cheeked Tern Sterna sandvicensis. See Sandwich Tern Stipiturus malachurus. See Southern Emu-wren Strix aluco. See Tawny Owl Sturnus vulgaris. See European Starling

Sula nebouxii. See Blue-footed Booby Sunbittern, 25 Superb Fairy-wren, 144, 175 Superb Pitta, 201 Swift Tern, 205 Tachycineta bicolor. See Tree Swallow Tadorna tadorna. See Common Shelduck Taeniopygia bichenovii. See Double-bar Finch Taeniopygia guttata. See Zebra Finch Tawny Owl, 138, 150 Telophorus quadricolor. See Gorgeous Bush-shrike Three-spined Stickleback, 138, 150 Tockus monteiri. See Monteiro’s Hornbill Torrent Duck, 285 Tourmaline Sunangel, 308 Tree Swallow, 120, 296, 300, 308 Tricolored Blackbird, 397 Turdus merula. See Eurasian Blackbird Turkey Vulture, 29 Tyrannus forficatus. See Scissor-tailed Flycatcher Tyrannus tyrannus. See Eastern Kingbird Tyto alba. See Barn Owl Uria aalge. See Common Murre Variable Pitohui, 28, 432–433 Vidua chalybeata. See Village Indigobird Village Indigobird, 214, 216 Village Weaver, 140, 151 Western Grebe, 210 Whimbrel, 13 Whiskered Tern, 205 White Ibis, 11 White Stork, 11 White-cheeked Pintail, 436 White-cheeked Tern, 205 White-crowned Sparrow, 91, 93, 98, 99, 103, 104, 239, 257, 307, 309 White-throated Dipper, 90 White-throated Sparrow, 53–54, 146, 184, 298, 307, 309, 312, 318 White-winged Crossbill, 104 White-winged Tern, 205 Wild Turkey, 12, 149 Willet, 24 Willow Flycatcher, 13 Willow Ptarmigan, 9 Willow Tit, 91, 93, 98 Wilsonia citrina. See Hooded Warbler

Species Index

471

Xanthocephalus xanthocephalus. See Yellow-headed Blackbird

Yellow-rumped Thornbill, 203 Yellow-rumped Warbler, 14

Yellow Warbler, 47, 90, 93, 108, 142, 167, 246, 256, 257 Yellow-browed Leaf Warbler, 93, 140, 157 Yellow-eyed Penguin, 47, 146, 180, 296, 299, 300, 304, 316 Yellowhammer, 140, 155, 156, 246, 251, 256, 257 Yellow-headed Blackbird, 62, 90, 170

Zebra Finch, 47, 60, 144, 146, 148, 151, 169, 181, 185, 202, 212, 243, 247, 252, 253, 293, 298, 304, 315, 318, 319, 406 Zone-tailed Hawk, 29 Zonotrichia albicollis. See White-throated Sparrow Zonotrichia leucophrys. See White-crowned Sparrow Zonotrichia querula. See Harris’ Sparrow

Subject Index

Abrasion resistance from feather pigments, 7–11, 71 Age effect on female quality, 295 effect on ornamental coloration, 39, 92, 159, 160, 163, 180, 234–235, 361, 364 related to paternity, 256–257 signaled by coloration, 37, 40, 52, 97–99, 103, 104, 111, 113, 123, 167, 295–300, 330, 351, 356 Aggression, 28, 52–53, 62, 87–123, 237, 307 Alternative strategies, 50–54, 384, 386 Amplifiers, 38, 40, 46–48, 175, 187, 287 Ancestral-state reconstruction, 417–426, 428–429, 433–434, 436–437, 439–447 Aposematic coloration in adults, 22–23, 68 in nestlings, 224 selection on, 70–71, 405–406 Assortative mating, 49, 53, 55–58, 139, 140–149, 156, 167, 173, 180, 183, 184, 185, 186, 313, 314, 315, 316–319, 323, 330 Bare-part coloration in adults, 7, 406–407 change in, 12, 217–221 comparative studies of, 423–425 mate choice for, 151–152, 180–182 in nestlings, 202–227, 407–408 Bayesian methods, 420–421 Begging as a correlate of nestling mouth color, 218–224, 226–227, 407 as a signal of identity, 62 Benefits of mate choice for color displays courtship feeding, 241–243 direct, 236–249, 253

473

fertilization, 243–244 genetic compatibility, 258–260 good genes, 256–258 immunocompetence, 260–263 indirect, 254–262 nest defense, 248 parasite avoidance, 248–249, 253 parental care, 244–248 related to condition, 263–265 related to dominance, 236–241 related to extra-pair mating, 256–258, 261–262 signaled by carotenoids versus melanins, 268–269 Brood parasitism, 62, 213–214 Carotenoid coloration benefits signaled by, 268–269 comparative analyses of, 402–404, 406–407, 423–425, 427–429 condition dependence of, 48 frequency distribution of, 47 mate choice for, 153–158, 163–165, 316–319 versus melanin coloration as a signal, 234, 268–269, 294–295, 355 plasticity in expression of, 353, 364 use in status signaling, 95, 101, 109, 237 Carotenoid pigments in bare parts, 406 dietary limitations for coloration by, 403–404, 407, 428–429 in egg yolk, 224 feather strengthening by, 9–10 in nestling mouths, 221, 224 protection from bacterial degradation by, 10 related to female quality, 296–299, 301 UV protection from, 10

Subject Index

474 Coefficient of variation (CV), 44–45 Comparative analyses, 4, 5, 7, 17, 18, 21, 57, 62, 63, 69, 119, 122, 209, 282, 290, 292 380–382, 386, 388, 392, 394, 396–397, 399, 403, 405–408, 417 Condition dependence of coloration, 38–39, 48–50, 58, 61. See also Honest signaling “Conspiratorial whispers,” 208 Countershading, 9, 20, 204 Cryptic coloration, 4, 6, 13–21, 24–29, 66, 68–69, 106, 204–205, 208, 280, 290, 291, 326, 391–394, 402, 409, 433, 436, 442 Delayed plumage maturation, 37–38, 52–53, 99, 113, 116–122, 234, 295, 382, 394–397, 409, 442–443 Disassortative mating. See Assortative mating Disruptive coloration, 20, 21, 29, 160, 204 Disruptive selection on color, 38, 46, 206, 405–406 Dominance interactions. See Status signaling Egg coloration as a signal of individual identity, 62–64 Evolution of development of color displays, 349–353 via directional selection on color traits, 38, 46, 49 via disruptive selection on color traits, 38, 46, 206, 405–406 of modularity of color traits, 353 Extra-pair mating female benefits from, 256–258, 261–262 as an index of mate choice, 139, 140–148, 154, 155, 160, 161, 164, 167, 169, 172, 173, 175, 323 related to coloration in comparative studies, 383–385 related to signals of strategy, 52–53 Female coloration approaches in studies of, 314, 348–349 body size and condition related to, 300–301 categorization of, 281, 283–286 competition for food related to, 306–307, 310 differential allocation related to, 322 effects of age on, 295, 300 effects of hormones on, 324 genetic correlation hypothesis for, 289, 290–293 history of the study of, 289–290 immunocompetence related to, 301–302 as an indicator of quality, 294–295 male mate choice for, 313–323

maternal care related to, 302–303 offspring quality related to, 305 overview of studies of, 280–281 reproductive success related to, 303–304 sex roles related to, 326–327 signaling readiness to mate, 325 signaling status, 305–312 survival related to, 304–305 types of expression of, 286–289 use in competition for food, 306–307, 310 use in competition for mates, 310–312 use in species recognition, 325 used to conceal sexual identity, 325 Fisherian runaway selection, 38, 40, 48–50, 73, 211, 254–255, 426 Frequency-dependent selection on color, 22, 38, 46, 50, 60–61, 70 Genetic compatibility, 38, 39, 40, 54–59, 258–260 Genetic determination of color, 38–42, 48–50, 53, 55, 57, 59–61, 63, 66, 69–71, 349–369, 405, 422, 429, 432, 439 Geographic variation in color, 37, 40–41, 49–50, 55, 71, 205–206 Gloger’s rule, 11–12 Hamilton-Zuk hypothesis, 249, 260–262, 388–391 Handicap model of sexual selection, 254–255 Homoplasy, 422, 424–427, 439 Honest signaling by badge size versus color quality, 234 by carotenoid versus melanin coloration, 234, 268–269, 294–295, 355 by feather versus bare-part coloration, 182 by female coloration, 294–295 of social status, 97, 101–111 theory of, 137 Hormones, 100, 102, 107, 109, 123, 156, 281, 283, 324, 357, 360 Identity contrasted with status signaling, 88 signaled by color, 60–65, 69–71, 207 Immunocompetence as a benefit of mate choice, 249–253, 260–264 as a component of female quality, 295 Handicap Hypothesis of, 107–109, 123, 182, 249, 253 related to female coloration, 301–302 summary of studies of related to color, 250–252 Intersexual signaling. See Mate choice Intrasexual signaling. See Status signaling

Subject Index Iridescence, 48, 168, 172, 173, 175, 286, 292, 298, 316, 396 Iris coloration, 13, 16 Keratin, 9, 357 Kinship signaling by color, 59–60, 63, 207–208 Lighting effects on coloration, in adults, 18–20, 38, 41, 66, 68–69, 360, 362, 398–402, 406, 409, 432 in nestlings, 204–205, 209, 222–223, 407 Major histocompatibility complex (MHC), 38, 58 Mate choice, 74, 137–189 for achromatic brightness, 176–178 approaches to testing, 139, 148–149, 170–171 for badge size versus color quality, 139, 153, 176 for bare-part coloration, 151–152, 180–182 based on age, 235 benefits of choice for ornamental coloration, 233–269 for carotenoid coloration, 153–158 for colored leg bands, 151–152 cryptic, 260 for eumelanin versus carotenoid displays, 163–165 for eumelanin coloration, 158–165 for fluorescence, 178–179 for genetic compatibility, 57–58 history of the study of, 87, 137–138, 150–152 male choice for female coloration, 313–323 mapped on a phylogeny, 429 for penguin pigments, 179–180 for phaeomelanin coloration, 165–168 for polymorphic color traits, 182–185 for porphyrin coloration, 180 for psittacofulvin coloration, 180 in relation to signal content of coloration, 138–139 for structural coloration, 168–169, 172–175 studies of in fish, 137–138, 150–151, 326 summary of studies of, 140–149 for symmetry, 139, 185–186 for tail length versus color, 241–242 for turacin coloration, 180 for ultraviolet coloration, 168–171 for white coloration, 176–178 Mating system, 383–386, 392, 394, 396, 403 Maximum likelihood reconstructions, 420–421, 434 Melanin coloration comparative analyses of, 402–404, 422–423, 427–429 condition dependence of, 48

475 countershading by, 9, 20 eumelanin as a criterion in mate choice, 158–165 frequency distribution of, 47 genetic control of, 206 as an identity signal, 63 of nestling mouths, 211 of nestling skin, 202–203 phaeomelanin as a criterion in mate choice, 165–168 sex-linked color mutation, 202 as a signal amplifier, 48 as a signal of presence, 66–67 use in status signaling, 100–101, 107, 109 Melanin pigments in eye-stripes, 12–13 feather strengthening, 8–9 photoprotection, 9–10, 202 protection from bacterial degradation, 10–11 Melanocortin-1 receptor (MC1R), 206, 351–352, 354, 355, 359, 361 Mimicry, 28–29, 117, 118, 121, 295, 429, 432–434 Modularity evolution of, 356–357 of melanin verus carotenoid production, 357–359, 360–363 persistence through evolutionary time, 356 in production of color displays, 353–369 scenarios for selection on, 363–365 of within-feather pigmentation, 356 Mouth flush, 201, 218–221 Multiple ornaments, 72–74 Nest location, 392–393 Nestling bare-part coloration evolution of, 209–211, 213–215, 224–227, 407–408 function of, 212–213, 221 of the mouth, 218–222 parasite-host mimicry in, 212–215 parent-offspring communication through, 210–211, 220–224, 226–227 of rictal flanges, 221–222 role of blood flow in, 217–220 role in controlling water loss, 203 role in enhancing conspicuousness, 212, 222–223 role in identity signaling, 212 role in thermoregulation, 223 sex differences, 212 of skin, 202–203, 217–218 ultraviolet reflectance by, 203, 217, 223 Nestling plumage coloration in altricial species, 202–204 developmental control of, 202

Subject Index

476 Nestling plumage coloration (continued ) evolution of, 209–211, 226–227 parent-offspring communication through, 203, 210, 217, 222–224, 226–227 in precocial species, 204–209 role in camouflage, 204–205, 208 role in countershading, 204 role in disruptive coloration, 204 role in identity signaling, 207–208 role in sibling competition, 210 role in thermoregulation, 204–206, 208 sexual dichromatism in, 215–217 Neutral function of coloration, 6–7, 71 Nonoptical properties of coloration, 7–16, 71 Parasites avoidance of as a direct benefit, 248–249, 253 comparative tests of good genes for resistance to, 388–391 Parental care, 244–248, 383, 386, 392, 409 Parsimony, 418–421, 423, 427–428, 434–437, 440, 444, 446–447 Patterns of coloration in comparative analyses, 409–410, 429–433 developmental basis of, 7 of eggs, 64–65 evolution of, 350–368 on the head, 12 signal function of, 36, 37, 52, 54, 63, 64, 66, 68, 69, 70, 72 of young, 204, 207, 208, 209, 211–216 Perception of color, 46–48 Photoprotective role of color, 9–10, 71 Plumage polymorphisms, 6, 17, 18, 54, 61, 69–71, 146, 182–185, 204–206, 307, 312, 314, 318, 351, 353, 355, 356, 357, 359, 361, 363, 383, 405–406 Predator distraction, 25–26 Presence signaling, 65–71 Prey startling, 24–25 Psittacofulvin pigmentation of female plumage, 288, 298, 315, 318 mate choice for, 179–180 protection from bacterial degradation by, 10–11 signaling by, 269 Publication bias, 328 Pursuit deterrence hypothesis, 23 Quality signaling, 39–40, 42–43, 46. See also Honest signaling Receiver psychology, 5, 70, 210, 212–213, 215 Reflectance spectrophotometry, 397–400, 404, 422, 443–447

Sensory bias, 66, 211, 218, 223, 350, 367, 426 Sex recognition, 38, 50, 63 Sexual dichromatism, 18, 27, 37, 50, 66, 70–72, 215–217, 282, 290, 382–394, 397, 403, 406, 409, 422, 433–442 Sexual selection. See also Mate choice, Status signaling on coloration, 3, 6, 16–18, 23, 48–49, 137–186, 211, 215–216, 383, 385, 390, 391, 394, 402, 404–406, 409, 422, 424, 435, 437–438 contrasted with social selection, 87, 109–111, 305–306 signified by monomorphism, 282 Social selection contrasted with sexual selection, 87, 109–111, 305–306 overview of, 306 Speciation, 422, 426, 439 Species recognition by color, 55, 57, 397–398, 409 Stabilizing selection on color, 38, 66 Status signaling, 46, 52, 88–89, 92–107 approaches to testing, 89, 92, 94–97 badge size versus color quality in, 101 between age classes, 97–99, 113, 116–122 between sexes, 97–99 effect of prior experience on, 100 effect on benefits to female choice for coloration, 236–241 as an evolutionary stable strategy, 46, 52, 53, 108–109 by female coloration, 305–312 of fighting ability, 88 frequency distribution of badges for, 43, 46, 111–113 incongruence hypothesis for, 102–105 matrix model for, 111–112, 114–116, 117 overview of, 87 physiological costs of, 106–107, 237 predation as a cost of, 106 reliability of, 101–108 role of carotenoids in, 95, 101, 109, 237 role of melanin in, 100–101, 107, 109, 237 role of structural coloration in, 100–101, 109, 237 skeptical recipient hypothesis for, 102 social control hypothesis for, 103–105, 109, 111 summary of studies of, 90–91, 93 Strategy signaling by color, 46, 50–54, 69 Structural coloration in comparative tests of function, 403, 404, 409, 442, 444 condition dependence of, 42, 48, 269, 296–300 degradation of, 10–11 of females, 288–289 frequency distribution of, 47

Subject Index mate choice for, 144, 145, 168–169, 172–175, 314–315, 316–319 signaling immunocompetence, 250–252, 302 signaling resources, 238–239, 246–247 use in status signaling, 90–91, 100–101, 123, 237 in young birds, 203 Territory as a benefit of mate choice, 236–241, 245 defense of, 38, 53, 60–63, 71, 427 quality related to status signaling, 99–100 Thermoregulatory role of plumage, 8, 11–12, 71 Ultraviolet coloration comparative studies of the function of, 402, 404–405, 429 as a criterion in mate choice, 142–145, 168–175, 178–179, 316–319 in nestlings, 203, 216–217, 223 as a signal of social status, 91, 101 Ultraviolet radiation protection from, 9–10, 29 Unprofitable prey hypothesis, 21–23 Variability in color, 36–75, 380, 394, 400–401, 407, 409

477 Vision in birds, 4, 391, 397, 443 Vision-enhancing role of coloration, 12–13 White plumage as an amplifier, 287 bacterial degradation of, 10, 11 condition dependence of, 42 as a criterion in mate choice, 144–145, 176–178, 183 as cryptic coloration, 4, 8, 18, 69 as default coloration, 6–7 as disruptive coloration, 20 as a “flock-cohesion” signal, 24 as a “foraging-recruitment” signal, 6–8, 24, 66, 122 frequency distribution of, 47 as a mechanism to startle predators, 25 as a pursuit deterrent, 23 related to female condition, 296, 298, 307 related to offspring condition, 258 related to resource investment, 238, 239, 246 as a signal of immunocompetence, 250, 251, 252 as a signal of status, 101 as a strategy signal, 53–54 tensile strength of, 9 of young, 201, 202, 204, 205, 206, 208, 209, 211, 316–319

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