Fathers and Their Children in the First Three Years of Life : An Anthropological Perspective [1 ed.] 9781623498085, 9781623498078

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Fathers and Their Children in the First Three Years of Life

Volume Twenty

Texas A&M University Anthropology Series Series Advisory Board

William Irons Conrad Kottak James F. O’Connell Harry J. Shafer Erik Trinkaus Michael R. Waters Patty Jo Watson

Fathers and Their Children in the First Three Years of Life An Anthropological Perspective

Frank L’Engle Williams

TEXAS A&M UNIVERSITY PRESS COLLEGE STATION

Copyright © 2019 by Frank L’Engle Williams All rights reserved First edition Library of Congress Cataloging-in-Publication Data Names: Williams, Frank L’Engle, 1966– author. Title: Fathers and their children in the first three years of life : an anthropological perspective / Frank L’Engle Williams. Other titles: Texas A & M University anthropology series ; no. 20. Description: First edition. | College Station : Texas A&M University Press, [2019] | Series: Texas A&M University Anthropology Series ; number 20 | Includes bibliographical references and index. Identifiers: LCCN 2019021690 | ISBN 9781623498078 (hardcover) | ISBN 9781623498085 (ebook) Subjects: LCSH: Patriarchy. | Fatherhood—History. | Father and infant. Classification: LCC GN479.6 .W44 2019 | DDC 306.874/2—dc23 LC record available at https://lccn.loc.gov/2019021690

It is with all my love and devotion that I dedicate this volume to my children, Jacob, Esther, and Yoni, who fundamentally transformed a man into a father and who deeply inspired me to consider writing a book about how infant care and carrying by parents during the first few years of life is at the very core of our collective humanity, past, present, and future.

Contents Acknowledgments  Chapter 1: How Long Have Fathers Carried and Cared for Their Infants? 

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Part 1: Life Cycle Chapter 2: The Birth of a Child and the “Birth” of a Socially Recognized Father 

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Chapter 3: Couvade and Hormonal Correlates of Paternity 

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Chapter 4: Postnatal Infant Development 

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Chapter 5: Reproductive Careers among Forager Males 

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Chapter 6: The Duration of Father Care Estimated from Skeletal Maturation and Decline 

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Part 2: Evidence of Father Care in Humans and Animals Chapter 7: Forager Fathers and Infants Cross-culturally 

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Chapter 8: Paternal Behavior in Nonhuman Primates and Other Animals 

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Part 3: Evolutionary Perspectives Chapter 9: The Evolution of Carrying Behavior 

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Chapter 10: Hyper-encephalization of Neonates 

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Chapter 11: Becoming Human 

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Epilogue The Role of Father Care: Past, Present, and Future 

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References 

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Index 

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Acknowledgments It is with much gratitude that I thank my editor, Thom Lemmons at Texas A&M University Press, for his support and encouragement throughout the publication process. This book was conceived and born in 2008–2009, when I was awarded a Research Initiation Grant from the Vice President for Research at Georgia State University. Support from this award to purchase rare ethnographic texts is gratefully acknowledged, as is the funding of two student assistants who helped launch the project, Tina Rezvani and Dani Bond. In 2019, completion of the book project was supported by a Tenured Scholarly Support Grant from the Vice President for Research and Economic Development at Georgia State University. Dr. Deborah Cunningham of Texas State University graciously allowed the use of her dissertation data for Figures 9.6 and 9.7. Dr. Cunningham provided fruitful discussions about the evolution of carrying behavior, which led to our paper with Dr. Lia Amaral on the forelimb skeleton of Australopithecus afarensis published in 2015 in Homo-Journal of Comparative Human Biology, and the conceptual development of Chapter 9. Dr. Francis Thackeray and Stephany Potze of the Ditsong Museum of Natural History kindly provided permission to photograph Sts 14 and Sts 5 (Figure 9.2). Encyclopædia Britannica generously allowed Figures 2.1 and 2.2 to be included with permission; Terese Winslow LLC Medical Illustration licensed the use of Figure 2.3 and retains the copyright; and Dr. Eric Wong of McMaster Pathophysiology Review kindly allowed the use of Figure 2.4, which was created by Cassandra Uy, Kate Gerster, and Jenna Rebelo. Figures 1.1, 3.1, and 7.1 fall under Creative Commons license. Oxford University Press generously allowed the reuse and modification of Figures 6.1, 6.3, 6.4, 6.5, 8.1, 8.3, 8.4, 9.1, 9.3, 10.2, 10.3, and 10.9 from my lab manual titled Exploring Biological Anthropology. I am indebted to the thorough reviews provided by Dr. James McKenna of Notre Dame University, Dr. Ellen Ingmanson of Bridgewater State University, and one anonymous reviewer. Their careful

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read of the text and subsequent comments, critiques, and additional references tremendously increased the relevance and value of the book for a wider audience. James McManus originally crafted the osteological photographs utilized in Chapters 6, 9, and 10; Jennifer Freidman photographed Figures 4.1 and 8.2 at the Duke University Lemur Forest for her honors thesis at Georgia State University; Caroline McGuire contributed additional ethongraphic evidence of father-infant procimity for her honors thesis at Georgia State University; Dr. Emanuela Guano kindly offered some brilliant ideas at a critical junction; and Tamar Williams provided Figures 4.2, 8.4, and 10.1, bibliographic sources, and inspiration to write this book. The primate phylogeny depicted in Figure 8.1 was modified from P. Dolhinow and A. Fuentes’s The Nonhuman Primates (Mayfield, 1999). Figure 10.7 was photographed at the Anatomical Museum at the University of Leiden with the permission of Dr. George Maat. Kimberly Myers and Rachel Paul generously proofread the manuscript, and their assistance is kindly acknowledged. The data utilized in Figures 6.2, 8.5, 10.4, 10.5, and 10.6 were collected during my dissertation research, and I am grateful to the curators who kindly allowed me the opportunity to examine the material in their care. I would like to offer my most profound thanks to Wilma Coleman L’Engle, who edited a previous version and who generously gave me the double gifts of life and good parenting, and to Edward DeCastro Williams, who inspired me to become a father.

Fathers and Their Children in the First Three Years of Life

1 How Long Have Fathers Carried and Cared for Their Infants?

How ancient is father care of human infants and young children, and why did it emerge? Is it possible that father care arose among the ancestors of modern humans and became essential for survival? Or is it a recent, though variable, development? Is father care an evolved trait of Homo sapiens, or is it a learned cultural behavior transmitted across generations in some societies but not others? It will be argued here that father care, specifically the proximate attention given to infants during the first three years of life, is not a recent development but rather an evolutionary and cultural phenomenon. The time frame of when this behavior arose in the human lineage is uncertain. Did males assist early human mothers some five to six million years ago (Ma) in Australopithecus or another ancient human genus (Figure 1.1)—when the foot changed from a grasping to a walking organ for two-legged locomotion, or bipedalism? Or were males recruited within the past 2 Ma when infant carrying and caretaking would have greatly benefitted slowly maturing, large-brained infants in the taxon Homo erectus? Certainly food sharing, some form of complex communication analogous to language, and sociocultural complexity would have enhanced pair-bonding or at least male social obligations. The initial imprinting of socially recognized fathers during the first few postnatal years may have sustained culturally sanctioned indirect care, such as provisioning and protection, of dependents for nearly two decades thereafter. In modern humans, this three-year window is critical to father-child bonding—which differs so intrinsically from the mother-child relationship. By increasing the survival of children in the past, present, and quite possibly the future, father care may be a driving force in the biological and cultural evolution of Homo sapiens.

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There is striking evidence that father care in humans was essential in the emergence of a prolonged human maturation schedule and the provisioning of dependents, unlike that seen in nonhuman primates or any other animal. Like so many things human, the variability of father care cross-culturally indicates it is a learned reproductive strategy based on familiarity, whereas in other vertebrate species, such as birds

Figure 1.1. Reconstruction of the Laetoli footprints, dated to 3.6 Ma, pay testament to the use of habitual bipedalism. Larger footprints are found in close proximity to smaller ones, and a childlike footprint is superimposed on those of the presumed adults. Whether these were made by a family group is suggestive but unknown. The smaller of the two adult Laetoli footprints show evidence of a figure carrying something on its left side, such as an infant. At the very least, the two adults are of different body weights, perhaps a male and female, and appear to have been walking next to one another, side by side (Hart and Sussman, 2005). Early humans such as Australopithecus afarensis, reconstructed here, or early Homo may have established pair-bonds between females and males to allow for cooperative breeding to take place. It is likely that some kind of cooperative breeding existed in A. afarensis to accommodate the increasingly large, relatively helpless infants who lacked a gripping foot (DeSilva, 2011).

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and wolves, paternal behavior has a strong genetic basis. In humans, cross-cultural accounts of socially recognized fatherhood provide ample evidence for the importance of paternal behavior to infant survival. Indirect paternal behavior such as provisioning and protection of children is practiced widely by humans, whereas direct paternal caretaking occurs less frequently (Marlowe, 2000). Father care is particularly pronounced in some foraging and small-scale societies in which fathers and infants are proximal for several hours per day. Father care in foragers ranges from 1.9 to 22 percent of the day (Marlowe, 2000) and, considering night cosleeping hours, would tally up to one half to two-thirds of a twenty-four-hour period. Among Hadza foragers of Tanzania, fathers carry their infants 5.6 percent of the time, and interaction with older infants and young children increases to 20 percent of daylight hours when fathers are in the camp (Marlowe, 2005). These activities include “carrying, holding, cleaning, feeding and pacifying infants” (Muller et al., 2009: 348) and peaks when infants reach about nine months of age (Marlowe, 2005). The goal of this book is to present an argument that father care throughout the first few years is adaptive within the context of the parental pair-bond and shapes how infants develop socially and biologically. The individual chapters grapple with a number of related questions. For instance, how do males become fathers? How do fathers become socially recognized in traditional societies, and how does this affect their biology? How do infants develop during the first three postnatal years? When do males become fathers during the life cycle, from ethnographic and osteological perspectives? What examples of paternal behavior exist in ethnographic accounts of foragers and smallscale societies, nonhuman primates, and other animals? What evidence exists in the fossil record for infant carrying, and how did it evolve? And finally, can the evolution of empathy—a quintessential aspect of father care—be reconstructed by comparing human developmental milestones during the first three years to cranial capacities of a human growth series and fossil hominins? Father care is likely to have arisen gradually during human evolution, as reflected in the protracted emergence of empathy during this critical three-year window, and was likely present within the behavioral repertories of early Homo, if not earlier. If ancient human males were recruited to help care for and carry infants, there may be life history and hormonal implications for fathers, such as an optimal reproductive age range for males. Osteological indi-

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cators of age provide additional evidence of an evolved reproductive life history of human males such that maturation and decline of the skeleton, while variable, proceed in a species-typical fashion across the life cycle. Meanwhile, testosterone levels decrease and prolactin levels increase among active fathers, suggesting proximate and evolutionary processes are at work (Gray, 2011; Gettler et al., 2012a; Bribiescas, 2016). If father care truly is an evolutionary trait of our species, then neolocal families today are reenacting and recreating this ancient set of parental practices. There may be important benefits of father care. For example, paternal involvement during infant brain growth may increase later social and cognitive potential, enhancing maturation, reproduction, and longevity (Lamb, 1997). Active involvement would entail carrying the infant.

Infant Carrying Carrying infants would have been a crucial aspect of parenting during human evolution. A simple pocket sling could have been utilized by females, males, or both, particularly during long stretches of bipedal locomotion, and could have allowed for additional items to be carried alongside the infant. Slings are often suggested to have been the first tool, invented by females out of necessity to care for an apelike biped that lacked the ability to grasp using its feet (Hrdy, 2009). Simple pocket slings are still available, and carrying devices generally increase the efficiency of manual infant transport by about 16 percent (Wall-Scheffler et al., 2007). The morphology of the forearm in humans bears the mark of infant carrying in the reduced lower to upper arm length in bipedal humans and 3 to 4 Ma Australopithecus compared to the arboreal apes, where the ulna and radius are elongated with respect to the upper arm. While a relatively long forearm might assist the biomechanical efficiency of arm swinging, it decreases the mechanical efficiency of infant carrying (Williams et al., 2015). Recruiting the forearm in infant carrying had high survival value, and so infants were likely held most of the time during the first two to three postnatal years and were probably carried between camps until the age of five years, similar to recent foragers (Hill and Hurtado, 1996).

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Early Days There is a long history of interest in fatherhood as a social construct (Malinowski, 1927; Mead, 1955; Dahlberg, 1981; Hewlett, 1991, 1992; Marlowe, 2003; Gray and Anderson, 2010; Shwalb and Shwalb, 2015). For example, Malinowski (1927) posited that human cultures are grounded in the cooperation of socially recognized fathers as coparents, whereas Mead (1955) constructed fatherhood as a uniquely human cultural behavior that serves as a useful adaptation in human societies. Zihlman (1981) argued that in early hominins (Australopithecus), females selected more sociable males as reproductive partners, such that parenting was shared and male nurturing increased the survival of the young. The biology of fatherhood is understood by cultures in fundamentally different ways, and this interpretation of the biological by the social profoundly reflects the character of human societies. One way in which many cultures have brought the attention of a male to parental obligations are the elaborate birth rituals collectively referred to as “couvade” (Malinowski, 1927). In addition to the cultural underpinnings of father care, there are hormonal, physiological, psychological, and social changes that occur when males are culturally recognized as fathers. Indeed, the rapid change following the birth of a child is as instantaneous as it is profound for fathers. Fathers must first adapt to sleep interruptions upon the arrival of an infant. Throughout the breastfeeding duration of up to three years or more, cosleeping at night becomes segmented for both parents, although obviously more so for the mother. Small (1998) argues that segmented sleep is the normal human pattern based on ethnographic evidence of hunter-gatherers. She describes in detail the sleep patterns of the !Kung, who sleep incrementally with or without infants. Individuals will often awaken during the night, sit by the fire, then return to sleep. Segmented sleep is also reported in historical investigations of natural sleep rhythms prior to the advent of electricity and cheap fuel (Ekirch, 2005). During the “night season,” from shortly after dusk to dawn, individuals had a first sleep, which was deeper and restful for the first several hours, and a second sleep before morning, which was lighter and marked by dreaming; these two were separated by a wakeful state of variable duration (Ekirch, 2005). McKenna’s research on the sleep patterns of mother-infant dyads also helps explain why infants awaken often throughout the night (e.g., McKenna et al., 2007). Sears and Sears (2003), among others, posit that infants should

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be carried throughout the day, they should cosleep with their nursing mothers at night, and they should not be left to cry themselves to sleep. Effective father care and indulgent parenting decrease signs of infant distress.

Father Care The biological foundation of paternity, or the act of procreating as a male, can be distinguished from father care, the act of helping to raise a child, from infancy to adulthood. Father care includes satisfying the immediate needs of infants, as well as affiliative behavior toward them. Additionally, fathers who are caretakers exhibit a number of behaviors, including carrying infants, food sharing, showing tolerance during the feeding of infants in close proximity, and active protection from predators, extrinsic dangers, and other humans (Hewlett, 1992b: 3). If father care evolved from habitual pair-bonding between the parents, and included male proximity during pregnancy, coparenting and carrying neonates and infants, support of breastfeeding, adapting to the sleeping patterns of infants, and infant hygiene, one would expect to see evidence in the physiology, growth, and development in both fathers and infants. Indeed, there appears to be a synchrony in malefemale oxytocin levels and neural networks in response to the caretaking of infants that may be fundamental to the formation of families (Atzil et al., 2012). Ultimately, if male involvement in parenting were a crucial aspect of how humans evolved, it would have shaped the reproductive careers of males in terms of timing, duration, and hormone regulation. It would also affect infant language development, brain growth, socialization, and enculturation. Yet there is individual and intercultural variation in father care (Bribiescas et al., 2012). Some of this variation may be attributed to context-specific needs or facultative fatherhood that is modulated by the presence of others, including grandmothers, older children, kin, and nonkin, and by economic and ecological circumstances (Hrdy, 2009; Shwalb and Shwalb, 2015). How can this variation be reconciled with the idea that father care was instrumental during the evolution of the genus Homo?

Cooperative Parenting During human evolution, increasingly large infants would have required extensive load-bearing demands for survival (DeSilva, 2011). Additional help to the mother, such as from a socially recognized father, grandmother, other relatives, siblings, and nonkin, at some

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point became essential (Robson et al., 2006; Hill and Hurtado, 2009; Hrdy, 2009; DeSilva, 2011). Siblings have been particularly important in assisting with the care of younger members of the family. To provide one example, in Ngecha, Kenya, mothers routinely call upon an older daughter, or son if necessary, between the ages of six and ten years as a “child nurse” for the baby (Edwards et al., 2015). The child nurse then carries and cares for the infant, with adults nearby, for several hours to permit the mother to tend to food production and domestic activities. There is a universal need for human mothers to harness this additional help to supplement the expensive energetics of human reproduction (Morelli et al., 2014). The provisioning of this auxiliary caretaker allows for a doubling of brain size to occur during the first year of life and a relatively rapid rate of brain growth for the following two years. Human infants are virtually helpless during the first two to three postnatal years and completely dependent on caretakers until age seven (unsubstantiated myths of feral or street children aside; Bogin, 2006). Cooperative parenting between females and males enhances the survival of offspring and has been shown to characterize all human foragers (Hill and Hurtado, 2009; Hrdy, 2009).

Pair-bonding Did pair-bonding and intense father care coevolve, or did the intensity of father-infant proximity occur more gradually over time, independent of the emergence of the pair-bond (Figures 1.2 and 1.3)? Social organization is often tied to the mating system among primates (Lancaster and Lancaster, 1983; Lawler, 2009). For example, males and females that differ in body size and secondary sexual characteristics tend to form social groups that include multiple females and fewer or a single male, such as in gorillas and baboons. In contrast, there are much fewer body and canine size differences between males and females in nonhuman primates that form smaller social groups comprising a single female-male pair with offspring, such as in gibbons and owl monkeys. In other words, it is the female-male pair-bond that often creates the conditions necessary for father care to occur. There may be several reasons for the evolution of the pair-bond. Lovejoy (1981) suggests that monogamy emerged as a consequence of bipedalism and provisioning by males. Deacon (1997) posits that monogamy arose along with the evolution of language so that males and females could express their monogamy to other members of the social group. The relatively large size of the penis with respect to

Figure 1.2. Major events during human evolution as compared to the intensity of father care. The evolution of father care occurred rather recently, perhaps beginning with carrying behavior during the transition to bipedality some 6 to 4 Ma, and later intensifying with the advent of stone production about 3.3 Ma. When encephalization arose during the evolution of the genus Homo around 2 Ma (Leonard et al., 2007), father care became a behavioral adaptation of pair-bonded early humans. The evolution of complex language around 300,000 years ago ushered a still greater intensity and longer duration of father care of infants. The symbols are a = the order Primates evolves about 55 Ma; b = origin of monkeys (anthropoids) about 35 Ma; c = apes (hominoids) evolve around 19 Ma; d = earliest humanlike forms (hominins) evolve around 6 Ma; e = definitive evidence for bipedalism in hominins at around 4.4 Ma; f = earliest stone tools at 3.3 Ma; g = evolution of encephalization/selection for larger brain size between 2 to 1 Ma, intensifying around 400,000 years ago; h = emergence of modern human language between 300,000 and 70,000 years ago; i = evidence for the belief in an afterlife evidenced by the purposeful burial of Neandertals between 120,000 and 60,000 years ago; j = food production, such as agriculture and animal husbandry, develops around 11,000 years ago; k = first cities in Mesopotamia arise around 5,500 years ago.

Figure 1.3. Landmark events during the evolution of the human genus accompanied an increasing intensity of father care, scored as 1 (incipient father care) to 4 (father care as experience in H. sapiens foragers).. The symbols are a = earliest stone tools common between 3.3 and 2.6 Ma; b = evolution of encephalization and selection for larger brain size occurs between 2 to 1 Ma, intensifying around 400,000 years ago; c = evidence for use of fire at Swartkrans dated to around 1.5 Ma; d = gesticulation evolves and becomes a precursor to language use evidenced by symbolism between 300,000 and 70,000 years ago; e = belief in an afterlife demonstrated by the purposeful burial of Neandertals between 120,000 and 60,000 years ago; f = evidence of tailored clothing as shown by bone needles at around 40,000 to 35,000 years ago; g = cave art becomes more common after 25,000 years ago; h = food production emerges around 11,000 years ago; i = first cities occur at around 5,500 years ago; j = first states emerge at around 4,500 years ago; k = first empires arise at around 4,350 years ago with Sargon of Akkad; 1= globalization emerges around 500 years ago.

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body mass suggests female choice was instrumental in the evolution of the pair-bond (Morris, 1967). Stone tools have also been cited as a precursor to monogamy, arising in conjunction with canine reduction (Wolpoff, 1976). The pair-bond could have acted to reduce the upper canines, which are more socially relevant, followed by the lower ones. Both canines changed from a weapon to incisor-shaped, and erupted earlier to reduce their influence as a social marker of maturation in male hominins, such as in Ardipithecus ramidus, dated to ~6 to 4 Ma (Lovejoy, 2009). The pair-bond could have emerged directly after the human line departed with the ancestors of chimpanzees, and thus canine reduction and monomorphism, along with an exposed pendulous scrotum, uncomplicated penile morphology, and cryptic ovulation, may be among the most ancient characters of human evolution, arising in conjunction with bipedality (Lovejoy, 2009). The antiquity of the pair-bond or marriage is further evidenced by its widespread cross-cultural occurrence, and the union of the pair is demarcated by specific social customs and rituals (Hill and Hurtado, 2009). There are variations, such as in polygamous marriages, where the union between the man and each wife is considered a pair-bond. The evolutionary underpinnings of the pair-bond are given further support by the relatively small size of the human testes with respect to body weight, as well as the thinner vas deferens, the reduced seminal vesicles, rate of sperm production, sperm counts and motility, and poor ejaculate quality with respect to nonhuman primates typified by a multimale/multifemale social organization, such as chimpanzees (Lovejoy, 2009). The antiquity of the pair-bond is also evidenced by the hormonal biofeedback loops that modulate social relationships between parents and between parents and children (Ellison and Gray, 2009). The pair-bond may have arisen from the exigencies of raising infants that require intense supervision and physical strength for the first several postnatal years and the need to provision dependents during an elongated subadult phase (Lovejoy, 2009). It is unknown if father care within a pair-bond arose first or if extremely large and physically demanding infants initially evolved. Several authors have suggested that direct paternal care arose subsequent to the emergence of the human pair-bond (Lukas and Clutton-Brock, 2013; Gray and Crittenden, 2014). The culturally constructed set of socioeconomic responsibilities between a single male and female with offspring led to the emergence of the “father-husband,” which is unique in the animal kingdom (Lancaster and Lancaster, 1983: 43). As one of the few

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primates, and only catarrhine, without a baculum, or penis bone (Bribiescas et al., 2012), it is possible that this bone was lost during the evolution of the human pair-bond (Lovejoy, 2009). Females could have preferred reproductive and social male partners who could honestly advertise their intentions without skeletal support for penile erection. In primates where paternal care is observed, including tamarins, marmosets, baboons, macaques, and humans, females often choose to mate with males that demonstrate affiliative behavior toward infants (van Schaik and Paul, 1996).

Human Life History Provisioning by fully adult male hunters could have allowed for food sharing, pair-bonding, and social reciprocity to evolve (Lancaster and Lancaster, 1983). However, hunting (and other kinds of skills-intensive foraging in both sexes) takes several decades to master and peaks at thirty-five years (Kaplan et al., 2000; Gurven et al., 2006). The protracted period of learning may have provided “embodied capital” that was later relied upon to produce far more than needed for survival. This excess of resources allowed for high-quality foods to be consumed by weaned yet dependent offspring during maturation. Consistently available high-quality protein provided the fuel necessary for a large brain to evolve and concomitantly reduced rates of aging, leading to a decrease in rates of mortality and increased longevity. However, whether or not males provisioned their offspring during maturation does not answer whether fathers were social caregivers, which would have included carrying behavior. The grandmother hypothesis offers an alternative explanatory model to account for the extra calories needed by mothers with slowgrowing dependents. This hypothesis suggests the additional dietary resources were supplied by grandmothers, which in turn selected for postreproductive longevity in humans. The explanation is built upon observations of vigorous Hadza postmenopausal forager women with grandchildren (Hawkes et al., 1998; Hawkes and Paine, 2006). However, the average life span of humans in nonaffluent societies is about fiftyfive to sixty years (Hill and Hurtado, 1996). Patterns of demography in past skeletal populations, and observations of recent hunter-gatherers and subsistence farmers, suggest that the elderly are rare (Meindl and Lovejoy, 1989; cf. Konigsberg and Herrmann, 2006), although they are always present in forager societies (Hawkes, 2006). If humans did not reach advanced ages in a predictable fashion in the past, grandmothers

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would scarcely be able to care for their own children born at the terminus of their reproductive career prior to dying, and would not be regularly available to provision their grandchildren. Given the variability of mortality, and family size and composition over time, the grandmother hypothesis alone may not fully explain the extension of life history schedules for mobile pair-bonded families of foragers. Furthermore, there are tremendous differences in the degree to which grandparents are involved in caring for infants cross-culturally (Edwards et al., 2015). Even among Hadza foragers, males contribute direct father care to their infants about twice as often as grandmothers (Marlowe, 2005), and cross-culturally, fathers take care of infants as much as grandmothers and aunts (Huber and Breedlove, 2007). In the absence of grandmothers or aunts, fathers may have been reliable and accessible actors to provision and care for young children.

Language Father care may have played a critical role in the evolution of intelligence, providing additional opportunities for complex communication systems such as spoken language to emerge. Language is a distinctive human quality that relies on binary contrasts and symbolic associations to transmit a large density of information. Language captures complex relationships, as well as differentiations of time and space, using a network of arbitrary symbols that is mutually, by and large, intelligible to its speakers. It differs from animal communication by its flexibility and can be modified as needed, contingent on circumstance (Fuentes, 2014). Using language, information is transferred between generations and across individuals (Fuentes, 2014). Human neonates are more captivated by language than random sounds, and by the first year are more attuned to their own language than other ones (Fitneva and Matsui, 2015). Shortly after the second postnatal year has been completed, a rapid transformation in language occurs. Between 2 and 2.5 years, and often shortly after the second birthday during a period of 2 to 6 weeks, children begin talking in full sentences with the use of correct pronouns, direct and indirect objects, syntax, and semantics. The increasingly routine and automatic arrangement of phonemes into communicative contrivances allows for higherorder linguistic processing to occur, permitting word combinations and eventually sentences to be constructed (Greenfield, 1991; Moore, 2011). The development of language is consistent cross-culturally (Mead,

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1955), suggesting there may be some brain-size Rubicon that is crossed by two-year-olds, activating full-blown human language skills. In addition to a large, complex, humanlike brain, language involves other aspects of anatomy, including hyoid and larynx position, diaphragm size and strength, and cranial base flexion. In ancient humans, indications of symbolic thought, such as advances in stone tool technology, nonutilitarian artifacts, cave paintings, and portable art, can be taken as indirect evidence of language. Early stone tool production may be linked to the initial development of language because of the necessity of teaching techniques of knapping and providing information about the location of source materials. The increasing complexity of stone tool production over the past few million years is analogous to human language development in infancy, in that both represent “grammars of action” in which distinct ideas and motor sequences are progressively and hierarchically organized into a coherent, culturally constructed form (Greenfield, 1991; Moore, 2011: 15). Experimental evidence suggests that cultural transmission of how to create stone tools could only have occurred using language rather than imitation and emulation (Morgan et al., 2015). In essence, stone tool production is so sophisticated that it requires language and not mimicry to replicate. Inferences drawn from infant development identify critical language windows. Human language is preceded by walking during early postnatal ontogeny, and this is also true of what we know about human evolution—that bipedalism occurred about two million years before brain expansion, and presumably language, did (Figures 1.2 and 1.3). The evolution of language may have been tied to an increased sophistication of gestures that can be learned prior to spoken language during early postnatal development. Carrying infants may have facilitated the acquisition of language through storytelling, teaching, and other forms of socialization. Larger brains were probably integral to the neural circuitry and heightened memory necessary for language to operate.

Brain Size and Encephalization One of the primary physical distinctions between humans and other animals is the degree to which the brain is encephalized (Leonard et al., 2007). Encephalization, or the ratio of the observed versus the expected brain size of an animal given their body weight, is extreme in humans during the first three years of life, corresponding to the neonatal period

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and early infancy. Substantial differences in encephalization between humans and the great apes can be observed when cranial capacity per age, from gestation to adulthood, is compared; distinctions between humans and Old World monkeys are even more profound. Human cranial capacities can also be compared to early human forms, such as Australopithecus, Homo erectus, and Neandertals, to show evolutionary trends. The fact that the brain doubles in size during the first year and reaches 80 percent of adult values by three years of age suggests that the first three postnatal years are absolutely critical in terms of forming personality traits, cognitive potential, and social skills. When humans are born, their brains are disproportionately large compared to their bodies (Leonard et al., 2007; Kuzawa et al., 2014; Hublin et al., 2015). When fathers, and other group members, are proximate to infants during this period of hyper-encephalization, the brain grows in a social context. This may enhance the potential for high-level aptitude functions, including language, mathematics, and social skills. Research from psychology shows that the absence of fathers decreases reactions to novel stimuli in children and may prove detrimental to the later cognitive and social potential of adults (Whiting and Whiting, 1975; Williams and Radin, 1993; Thomas et al., 1996; Lamb, 1997; Veneizano, 2000, 2003; Atzil et al., 2012).

Cross-cultural Approaches If father care were an adaptation of the human species, we would expect to see a worldwide distribution of paternal behavior, which we do. However, this global presence of father care is highly fragmented. Many societies engage in status-seeking behaviors, which detract from male-infant proximity, a pattern that has only increased since the Neolithic revolution. These societies include industrial economies, warrior states, agriculturally based historic empires, and herders (Katz and Konner, 1981). A fragmented patchwork of societies remains in which father care for infants is observed during the first three postnatal years. Many of these societies are described as egalitarian forgers, small island fisher/foragers, and small-scale fisher/horticulturalists. For example, an ethnography titled Intimate Fathers by Barry S. Hewlett (1991) describes the frequency of father-infant proximity and paternal carrying among the Aka foragers of Central Africa. As demonstrated by the Aka, carrying by fathers increases the enculturation of infants

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(Hewlett, 1991). This small-scale society is also strongly egalitarian, with both sexes participating in the “net” hunt. Increased social status is conferred when a man has multiple brothers. However, having brothers involves mutual obligations, as well as competition with other men and their brothers. These activities decrease paternal behavior, drawing a father’s attention away from infants. Fathers who grew up with sisters are noted to be the most social and to carry infants more than 80 percent of daylight hours. Father care is found more often in foragers than in stratified and/or polygynous food producers. Hunter-gatherers often share several characteristics in common, including an emphasis on cooperative and collective hunting, gathering, and child-rearing within the group, as well as food and possession sharing between kin and nonkin (Narvaez et al., 2014). As a consequence of the intensity and intimacy of group living, extensive social learning characterizes adult-child, child-child, and adult-adult interactions. Hunter-gatherer groups are autonomous, rely on negotiation between group members for decision-making, show primarily positive relations with neighboring groups, and exhibit fluidity of group membership and small group size (twenty to fifty individuals, including immature members). Groups tend to be mobile and inhabit dwellings that are constructed with local materials within a few hours (Narvaez et al., 2014). Ethnographies of subsistence farmers demonstrate the degree to which food production required a very different way of life and world view. Perhaps most importantly, food production exacerbated the sexual division of labor and limited father-infant proximity. It is not necessary to idealize hunter-gatherer lifeways as some utopian past in which societies functioned optimally through equitable resource distribution and equality. In fact, forager societies suffer high infant and adult mortality. Among Batek foragers of the southern Malaysian peninsula, about 25 percent of neonates (inclusive of stillbirths) and infants during the first two years died prematurely, primarily from malaria and intestinal diseases (Endicott and Endicott, 2014). Furthermore, Aka forager adolescents could recount on average twentyfour personal experiences with deceased relatives and others (Hewlett and Lamb, 2000), and 20 percent of Efe children under eighteen years of age had experienced the loss of a parent (Morelli et al., 2014). Given this context, there is tremendous variation in father-infant relations in both foragers and food-producing societies. In agricultural and industrial societies, there may be more variation within cultures than

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between them with respect to fathering styles (Gray and Anderson, 2010; Shwalb and Shwalb, 2015). It is possible that some of the variation in fatherhood can be attributed to ecological, demographic, economic, cultural, and familial factors (Hewlett, 1991, 1992), or that it is situation-contingent and arises when it benefits the interests of fathers and mothers (Hrdy, 2009). One commonality, however, is that positive father involvement with infants arises from individual idiosyncrasies and circumstances, but is framed within a sociocultural context. Ethnographies detailing hunter-gatherer societies are particularly important reservoirs of information concerning human patterns of behavior in the absence of food production. The Aka foragers mentioned previously present one example of a hunter-gatherer economy with egalitarian social relations and positive father-infant proximity. Indeed, Aka infant-toting fathers often engage in social encounters with other male caretakers (Hewlett, 1991). There are several other foraging societies similar to the Aka, such as the Batek (Malaysia), Agta (Philippines), Hadza (Tanzania), and to a lesser extent, the !Kung (southern Africa), Ache (Paraguay), and Hiwi (Venezuela). Among Batek foragers, fathers were traditionally involved in caretaking, second only to the mother, including carrying behavior, socializing, and elimination communication (Endicott, 1992). Among forager–food producers in lowland rainforest tribes, such as the Bari Indians of Venezuela, several social fathers are often recognized, and infants with more “fathers” have a better chance of survival than those with fewer (Beckerman and Valentine, 2002). This is also true of the Ache (Hill and Hurtado, 1996) and other South American tribes (Hrdy, 2009). However, in masculinized cultures such as the Yanomanö of the Amazon basin, where patriarchy prevails, fathers act differentially to the sexes (Chagnon, 1977), although much variation exists between villages (Hames, 1992). The fact that father care varies so greatly in human families suggests two things. First, father care is a learned behavior, passed down (or not) by tradition. Second, traditions that lack or limit father care are those that are dominated by the accumulation of social power and material wealth; these societies are also inherently nonegalitarian and prone to warfare. If father-infant proximity and cooperative breeding were essential factors during human evolution, how did such a system of parental care arise? Furthermore, in what context did father care first emerge? Konner (2010) suggests early hominin parental care included “(1) touch, being held or kept near others constantly; (2) caregiver prompt and

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appropriate responses to fusses, cries, and needs; (3) breastfeeding on demand frequently (2 to 3 times/hour initially) and on average 2 to 5 years; and (4) cosleeping close to caregivers” (Konner, 2010: 314). When mothers gave birth to additional children, became ill or incapacitated, or were unable to cope with a difficult infant, could fathers have intermittently played a role in helping care for the children? Alternatively, could the affectionate relationships arising between females and males have been extended to include their offspring, with dual obligations and responsibilities? Could sociable fathers have been among multiple group members that helped mothers care for infants (Hrdy, 2009)? All of these patterns of infant care parallel those characterizing many small-scale societies, such as Batek hunter-gatherer parents (Endicott and Endicott, 2014).

Windows into the Past It is often suggested that there are five windows into the past, however imperfect. The fossil record remains the most compelling of these windows by evidencing the physical remains of past life-forms. Humanlike fossils, whether they are cousins or lineal relatives, approximate the ancestral condition of Homo sapiens. A second window into the past is the archeological record. Human behavior is represented in the tools produced, resources exploited, context of the remains, whether retouching of tools is present, the sources of raw materials, and the duration of activity (Lebègue et al., 2010). These remains record the social and economic activities of humans, allowing for the reconstruction of past behavior. A third window is primate behavioral ecology. The dietary, reproductive, developmental, and social worlds of nonhuman primates, particularly the great apes, offer provocative examples of behaviors that may have been exhibited by the last common ancestor of apes and humans. Nonhuman primates are the closest living relatives of humans, and they generally live in complex social groups. Primates exhibit relatively large brains, an emphasis on the visual system, and a tendency to explore the world using the hands rather than the face. Although they are not living fossils, they offer a glimpse into the ecological and social dynamics perhaps encountered by early human forms. A fourth window into the past is the reproductive biology and social organization of contemporary foragers. Although these peoples are not frozen in time, they still obtain dietary resources, much as all humans did prior to the advent of food production ten thousand years

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ago (Figure 1.3). Foragers are characterized by delayed sexual and skeletal maturation compared to agriculturalists and tend to live in small, mobile groups of kin and nonkin. A fifth, less often articulated window into the past is the human maturation schedule from conception to around the age of seven years. It has long been known that Haeckel’s biogenetic law is untenable (Gould, 1977). In other words, ontogeny does not recapitulate phylogeny. Ernst Haeckel believed that the stages of development of a descendant represent ancestral adults. Stephen J. Gould (1977) posited that the juvenilized morphology of the human adult head and face, compared to nonhuman primates, stems from the slowing of shape change with respect to growth and maturation. Females could have favored males with more gracile faces, which may have arisen from a reduction in the development of male craniofacial features, particularly if these neotenic males exhibited higher levels of positive paternal behavior (Jolly, 1985). The trajectory of human development may partially represent some of the major steps in human evolution. From the brink of conception to a walking, talking child, humans traverse important evolutionary milestones. It must be remembered that this is an imperfect window. For example, infants cannot climb trees, but given the shoulder morphology of humans, ancient humans ancestors were certainly preceded by tree-living forms. However, we should not throw out the proverbial baby with the bath water. There may be other vestiges of the human evolutionary past manifested during the first three postnatal years. One of these might be the emergence of empathy, or “feeling-withothers” (Morelli, 2015: 156). Empathy may allow for the coordination of neural networks involved in coparenting and, in turn, the mimicking of a partner’s physiological state by males (Atzil et al., 2012). Empathy is one of the social emotions—the others being shame, guilt, and contempt (Friedlmeier et al., 2015). These emotions are learned in different ways cross-culturally. However, between twelve and eighteen months, empathy is learned by infants as part of enculturation, alongside the increasing control of emotions, which develops during the first three postnatal years (Friedlmeier et al., 2015). Could the acquisition of empathy in infants provide an indication of when empathetic behaviors—and perhaps father care—arose during human evolution? Nonhuman primate mothers are in close proximity to their infants and young juveniles, and it is likely that humans evolved in a simi-

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lar fashion. In contrast, human infants in many cultures must learn self-soothing techniques to survive the lack of empathy, which entails a lack of physical contact and close proximity of immediate caretakers. Carrying of infants by fathers and mothers provides a strong foundation for later parent-child relationships, and influences the hormonal profile and self-perception of male caretakers (Gettler et al., 2011a, b). As in the New Guinea village of Busama, “the love of the father for their children” was partly borne from proximity and direct care, which furthered the emotional attachment between generations (Hogbin, 1963: 20).

1 Life Cycle

2 The Birth of a Child and the “Birth” of a Socially Recognized Father

Reproduction remains a quintessential foundation of paternal behavior. Fatherhood can occur in the absence of direct male reproductive involvement in cases of adoption and remarriage. However, in all instances, infants are conceived, undergo gestation, and are born. Distinct female and male contributions toward creating infants correspond to differences in reproductive life histories.

Sex Differentiation Males differ from females in primary and secondary sexual characteristics. Physical differences related to reproduction are established chromosomally at the moment of conception. Sex differences initially form during embryological and fetal development and are amplified during adolescence. Females exhibit an XX configuration of sex chromosomes, whereas males have an XY combination for the twenty-third pair. Aneuploidy (having an abnormal number of chromosomes in a pair) is more common in the twenty-third pair than in most autosomes (Snow and McGaha, 2003). Nevertheless, variation in sex chromosome configuration occurs only rarely. In the twenty-third pair of male chromosomes, the Y chromosome is shorter than its counterpart, which leads to a greater expression of sex-linked genetic traits carried on the X chromosome, like hemophilia and red–green color-blindness. In other words, the Y chromosome contains so little information that anything present on the X chromosome is usually expressed (Arnold, 2004). However, the Y chromosome does contain vital information for the development of male primary and secondary sex characteristics. About two months after conception, the Müllerian and Wolffian ducts are found in both female and male fetuses. When the Y chromo-

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some is present, these are modified by a massive bath of testosterone. In XY individuals, Sertoli cells of the gonads begin to initiate a withering of the Müllerian ducts. Meanwhile, the Wolffian ducts, through the action of testosterone, develop into the sperm and ejaculatory ducts and seminal vesicles, which eventually results in the development of the testicles, vas deferens, prostate, and penis. The wash of testosterone may actually alter the neural circuitry developing rapidly during the first trimester (Cahill, 2006). The formation of the primary sex organs of males is completed late in the first trimester of pregnancy (Snow and McGaha, 2003). Primordial male germ cells and Sertoli cells in the seminiferous tubules of the developing testes also take form during the first trimester. Further expressions of testosterone during gestation prime the cells responsible for later sperm production after puberty. In females, the Müllerian ducts develop into the analogues of their male counterparts. In the absence of substantial testosterone production, the clitoris, vaginal canal, cervix, uterus, fallopian tubes, and ovaries develop and the Wolffian ducts disintegrate. During the second and third trimester, substantial egg production ensues in the ovaries via meiosis, equaling about 400,000 to 800,000 eggs. These eggs remain in a rudimentary state for eight to sixteen years before sexual maturation.

Puberty, Adolescence, and Sexual Maturation The velocity of growth is relatively slow during childhood, from three years of age to puberty (Bogin, 1999, 2006; Gurven and Walker, 2006). Growth of the primary sex organs follows the trajectory of other postcranial elements until puberty, which commences in males between the ages of twelve to sixteen years, with a median age of thirteen years, and usually between ten to fifteen years in females. Puberty—which marks the initiation of sexual maturation—is short, lasting only a few weeks, but its occurrence fundamentally changes the hormonal and physiological systems that continue to mature thereafter (Bogin, 2006). In both males and females, the nipples swell in response to rising levels of sex hormones at the onset of puberty, but in females, the swelling of the nipples continues as the mammary glands expand. In males, the development of secondary sexual characteristics, such as facial and body hair, begins to occur alongside the enlargement of the penis, scrotum, testes, and internal reproductive organs when testosterone and other androgens are produced in increasingly greater quantities after puberty. During adolescence, the hypothalamus becomes increasingly acclimatized to circulating androgens (Bribiescas and Elli-

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son, 2008). This leads to greater hormone production and subsequently to changes in voice pitch, enlargement of the skeletomuscular system, and enhancement of secondary sexual characteristics (Bribiescas and Ellison, 2008). After maturation, males cycle on a circadian rhythm with respect to the ebb and flow of testosterone and other androgen levels. These peaks and valleys of testosterone production in cells of the testes are directed by the hypothalamus-pituitary axis, and serve to initiate and regulate spermatogenesis. At least twenty million sperm per ejaculate are needed to be fertile, which may take many months to years after puberty to be able to produce. It is at this point when males reach sexual maturation. Sexual maturation can precede adulthood by four or more years. Adulthood occurs after sexual maturation in both males and females. Since adulthood is socially defined, it varies for each culture. However, adult status normally coincides with full dental and skeletal maturation. At puberty in females, fatty tissues develop around the areolas of the nipples, which enlarge, as do the mammary ducts and lobules. Either before or after the enlargement of breast tissue in females, the endometrium, comprising the inner layers of the uterus, is shed. This first shedding of the uterus, known as menarche, prepares the reproductive system of females to begin the first menstruation cycle, in which a buildup and breakdown of the endometrium occurs on a monthly or twenty-eight-day cycle, corresponding to the rise and fall of estrogen and progesterone levels, among other reproductive hormones. Menarche usually occurs between eleven and fifteen years, although much variation is present (Jones and Lopez, 2006). Menstruation is controlled by the hypothalamus-pituitary axis, which regulates secretions of estradiol and other estrogens in the ovaries during the follicular phase when the endometrium is thickened. This is followed by a peak in progesterone after ovulation, known as the luteal phase, when the uterine wall continues to become enriched in anticipation of receiving a developing conceptus for implantation, followed by a menstruation phase, in which the endometrium contracts and is shed for three to seven days. The initiation of cycling is accompanied by pubic and axillary hair growth, fat deposits in the hips and upper chest, growth and development of the reproductive organs, and sweat and sebaceous glands. Eventually, ovulation begins to occur toward the middle of the menstrual cycle when females approach sexual maturation, although adulthood may occur five to six or more years thereafter.

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Puberty is usually followed by an adolescent growth spurt in which both females and males grow considerably in limb bone and trunk length. In females, the growth spurt terminates between thirteen and sixteen years, whereas in males, it begins later and lasts much longer, with much individual variation. In the late teens and early twenties, from sixteen to twenty-four years, most limb bones begin to ossify, although growth in some males can continue to the middle of the third decade (Steele and Bramblett, 1988). Facial robusticity—including jaw, cheek, and brow amplification—continues to develop in all males until about twenty-five years of age, but amplification of these facial structures decreases markedly in females by twenty years or beforehand. The clavicle does not complete its maturation until twenty-nine or thirty years (Steele and Bramblett, 1988), which allows a miniscule increase in shoulder breadth in males toward the end of the third postnatal decade. Forager males such as the Ache often become fathers between the ages of twenty-four years and forty-eight years, and the prime years of paternity are between thirty-five and forty-five years (Hill and Hurtado, 1996). Socially recognized fatherhood thus comes many years after sexual maturation. The prime reproductive years for female foragers range from nineteen to thirty-seven years but can extend from eighteen years, or younger, to forty-eight years (Hill and Hurtado, 1996). Females among the Ache and other foragers are often infertile until nineteen years. In agricultural populations and others with high caloric diets, fertility can occur much earlier (Frisancho, 1993).

Spermatozoa Production in Males In traditional cultures, the male biological contribution to offspring has been difficult, but not intractable, to ascertain (Malinowski, 1927; Beckerman and Valentine, 2002). Observations of domestic animals have long convinced humans that male and female essential qualities are involved in reproduction, but the exact contribution was unknown until the middle of the nineteenth century. Even contemporary subsistence farmers may believe that several fathers are necessary for conception to occur (Mace and Sear, 2008). This belief benefits the survival outcomes of infants “fathered” by multiple males. The modern fertility industry, including in vitro fertilization, has demonstrated that, without a doubt, sperm is needed for conception to occur. The millions of spermatozoa that compete with one another are enveloped within a nutrient-filled medium produced by the male

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reproductive tract. The number of spermatozoa empirically demonstrated in a normal ejaculate of an adult male can easily exceed 250 million, and ranges from 40 to 500 million (Jones and Lopez, 2006). This staggering number suggests that the competition is intense, since normally only a single spermatid will fertilize an ovum. About one thousand spermatozoa per second are created in mature males. Each male germ cell takes about three to four months to mature into a spermatozoa. A gonadotropin-releasing hormone from the hypothalamus stimulates the production in the pituitary gland of the folliclestimulating and luteinizing hormone (Jones and Lopez, 2006). These prime the Sertoli and Leydig cells in the seminiferous tubules of the testes of sexually mature males to assist the development of male germ cells through the action of androgens, such as testosterone. Sertoli cells, which stop increasing in number at puberty, nurture male germ cells. Some male germ cells become specialized spermatogonia that undergo spermatogenesis. Spermatogenesis involves meiosis, or reduction division, reducing into half the original number of chromosomes, such that four spermatids are produced from a single male germ cell. The spermatids then mature into spermatozoa. During this process, they undergo a shape transformation, including the formation of a head that contains twenty-three chromosomes (haploid) and is surrounded by a nuclear membrane, a middle-section that provides energy from mitochondrial metabolism, and a tail that allows for propulsion. Along the circumference of the testes lies a protective barrier that prevents large immune cells from attacking the genetically foreign spermatids. The spermatids are “foreign” because they are haploid in chromosome number and therefore different from the typical cells of the human body, containing a diploid number of chromosomes (n = 46). The mature spermatozoa eventually leave the testes via the propulsive action of cilia and enter the epididymis, an organ found behind each of the testes (Figure 2.1). The epididymis is a long but tightly coiled tube where spermatozoa continue the final stages of maturation. They are then transported through the action of cilia and muscle pulses of the vas deferens to a broadened area called the ampulla, where spermatozoa are stored and where the seminal gland connects to the vas deferens. The vas deferens then joins the ejaculatory duct, which passes through the prostate gland to the urethra. The prostate, seminal vesicles, and Cowper’s gland contribute nutrient-filled, viscous fluids that allow the spermatozoa greater mobility and motility. Most of the fluid in semen

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is contributed by the seminal vesicles, followed by the prostate gland. Cowper’s gland is the main contributor to preejaculatory semen, which also contains a small number of spermatozoa.

Ova and Follicle Production in Females Toward the middle of the follicular phase of a female menstruation cycle, follicle-stimulating and luteinizing hormones secreted by the pituitary gland result in the further development of cohorts of immature ova, each surrounded by a follicle or sack, within an ovary of a sexually mature female. The follicles are composed of granulosa cells and aid in the maturation and protection of the oocyte, and produce hormones that influence female reproduction (Jones and Lopez, 2006). These immature ova undergo the first meiotic division but are in an arrested state within the follicle, resulting in two unequal cells. One is the polar body, which eventually disintegrates, while the secondary oocyte continues to develop within the follicle. The secondary oocyte remains arrested in the second meiotic division, and the final stages of meiosis are only completed when a sperm cell enters the plasma of the ovum. After a number of selection phases (Baker and Spears, 1999), about twenty maturing, or tertiary, follicles develop simultaneously in the ovaries, about half per ovary (Jones and Lopez, 2006). These stimulated follicles (more specifically, the granulosa cells of the follicle) begin to secrete estradiol, which reduces the effect of circulating folliclestimulating and luteinizing hormones, and stimulates the initial thickening of the endometrial lining of the uterus (Figure 2.2). Rising levels of estradiol result in the secretion of gonadotropin-releasing hormone by the hypothalamus (Baker and Spears, 1999). This leads to a surge in the production of luteinizing hormone, and eventually to a bursting of a single follicle sack, called ovulation. The released oocyte exits the ovary amid follicular fluid and enters the fallopian tube via the oviduct infundibulum. The oviduct contains cilia along the edges of fimbriae, or narrow finger-shaped appendages, which direct the oocyte toward the uterus (Jones and Lopez, 2006). At the same time, the corpus luteum forms from the remains of the emptied follicle and begins to produce progesterone and limited amounts of estradiol to stimulate a further thickening of the endometrial lining of the uterine wall, and functions later during the first trimester of pregnancy. A mature ovum lives for about twenty-four hours.

Figure 2.1. Male reproductive anatomy. Reprinted with permission from Encyclopædia Britannica, copyright © 2012 Encyclopædia Britannica, Inc.

Figure 2.2. Female reproductive anatomy. Reprinted with permission from Encyclopædia Britannica, copyright © 2013 Encyclopædia Britannica, Inc.

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Sexual Reproduction During sexual intercourse, spermatozoa are ejaculated by an erect penis at the cervix, which lies at the terminus of the vaginal canal. Ejaculation is a two-step process. During penile erection, the ejaculatory center of the spinal cord signals the bulbocavernosus muscle, located at the base of the penile shaft, to contract, along with muscles of the testes, epididymis, vas deferens, ejaculatory duct, and urethra, as well as the prostate and Cowper’s glands, and the seminal vesicles (Jones and Lopez, 2006). The contractions force semen, which includes sperm cells and associated fluids, into the urethral bulb, which is blocked from the bladder by a sphincter muscle. The push of semen into the urethral bulb is sensed by males as the euphoric sensation that ejaculation is imminent. During the second phase, semen is expelled through the external urethra orifice via muscular contractions of the penis and bulbocavernosus muscle. Most of the semen is expulsed during the first four of these contractions. Subsequent contractions are not as forceful and expel lesser amounts of semen (Jones and Lopez, 2006). If a woman is ovulating, the mucus lining of her cervix is thin and contains nutrients essential for the survival of sperm cells. The spermatozoa mature over a period of seven hours, reaching the capacity to fertilize an ovum (Moore and Persaud, 1998). The movement of sperm can be rapid at ovulation, reaching the uterus in less than half an hour after the deposition of sperm ejaculate. Vaginal contractions caused by female orgasm can facilitate sperm transport through the cervix and into the uterus. However, fertilization can occur in the absence of female orgasm. Elaborate folds and fibers within the cervix create tiny tubules that sperm must traverse, nearly single-file, to reach the uterus (Jones and Lopez, 2006). Most sperm cells live for about twenty-four hours, although some can live up to five days in the reproductive tract of females, as long as ovulation has not occurred. If sperm deposition during sexual intercourse occurs before ovulation, sperm can live in the cervix until the follicle bursts. Upon ovulation, the cervix thins further, and uterine contractions pull the spermatozoa previously held in the cervix toward the fallopian tubes, effectively allowing a female to fertilize herself with sperm deposited up to five days previously (Jones and Lopez, 2006). Once ovulation has occurred, sperm only have twelve to twenty-four hours to reach the ovum. Uterine contractions assist in sperm transport while white blood cells, released upon the presence of sperm in the uterus, collect incapacitated spermatozoa. Only several

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thousand sperm are able to pass from the uterus to the fallopian tubes, and some choose the wrong one. The fastest and healthiest sperm reach the egg first, most often at the widest part of the fallopian tubes closest to the ovaries, called the ampullary–isthmic junction of the oviduct (Jones and Lopez, 2006). Along the way, millions die or get sidetracked, but eventually up to a few hundred spermatozoa surround the ovum, each desperately attempting to be accommodated. But in most conceptions, the egg only admits a single sperm cell, probably the most biochemically attractive to abut the cell wall. The sperm has to be received by the ovum, first by traversing a cloud of follicular cells surrounding the egg and then by pushing through the outer cell matrix, called the zona pellucida. Once a biochemical connection occurs with the egg, enzymes on the sperm head disintegrate the cell wall of the ovum, while the tail frantically propels it further inside the zona pellucida, eventually allowing the nucleus to be released into the plasma of the ovum. Thereafter, an immediate biochemical barrier denies entrance to other spermatozoa. The genetic material of the received sperm cell is immediately brought toward the nucleus of the ovum, as the nuclear wall of the sperm degrades further. However, before fusion of the ovum-sperm nuclei

Figure 2.3. Development of the preimplantation blastocyst in humans, reprinted with permission, copyright © 2001 Terese Winslow LLC.

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occurs, the egg nucleus undergoes the final stages of meiosis, in which a tiny polar body is shed (Jones and Lopez, 2006). In essence, the ovum is haploid for less than a half hour, which means it largely evades immune system detection until conception. Once ovum-sperm nuclei are fused, the zygote, or ovum-sperm combination, is transformed, and a number of systemic changes occur as it traverses the fallopian tube (Figure 2.3).

Human Embryology The zygote, which is about the size of this dot (.), begins cell division by thirty-six hours after conception, resulting in two daughter cells (Snow and McGaha, 2003; Jones and Lopez, 2006). After seventy-two hours, the zygote is about twelve to sixteen cells and exhibits the shape of a raspberry. The knobby appearance of this cell mass has led to its description as a morula (or “mulberry” in Latin), which enters the uterus after four days postconception. Cell division proceeds, and eventually the morula comprises a cluster of about fifty-eight cells (Snow and McGaha, 2003). At about this time, this cluster begins to form an internal cavity called a blastocyst, in which specialized cells group together on one of the internal sides, eventually becoming the embryo and associated structures, known as the embryonic disk. The blastocyst is mobile within the uterus for two or three days subsequent to initial formation and slightly larger than the original ovum before conception. At about six days postfertilization, the blastocyst undergoes implantation as biochemical communication occurs among both parties. This intricate choreography of biochemical signals between the blastocyst and the mother’s uterine endometrium must be successful for implantation to take place. Otherwise, both are shed during the next menses. At the site of contact, newly differentiated outer blastocyst layers secrete enzymes that disintegrate the outer layer of uterine tissues (Figure 2.4). As this occurs, the blastocyst is “hatched” by the shedding of the zona pellucida from the action of enzymes secreted by uterine tissues. The secretion of digestive enzymes by the blastocyst lasts for about four days, then abruptly halts, and the implantation site heals with a scar three to four days thereafter, or two weeks postconception, sometimes with a bit of bleeding. Implantation often occurs in the upper uterus. The blastocyst is now completely enveloped within the uterine wall as specialized trophoblast cells further invade the maternal tissues, eventually forming the basis of the umbilicus. The outermost of these trophoblast-derived cell layers burrow still deeper into the uterine

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Figure 2.4. Embryonic and placental development. Reprinted with permission of McMaster Pathophysiology Review.

tissue, and these eventually completely surround the developing conceptus. The external layers of these trophoblast-derived cells are the precursors of the outer wall of the placenta (Jones and Lopez, 2006). The blastocyst, once it becomes attached, continues to differentiate more rapidly into cell layers and is nourished by pockets of maternal blood within the endometrium (Figure 2.4). After the second postconception week, subsequent to implantation, a transition occurs in which the new organism begins to develop as a multicellular entity. Development is a major difference between onecelled and multicelled organisms, and allows for greater modulation by the external world. Development involves a differentiation of tissues. Cells that are close to one another, or proximal, begin to differentiate in the same way to become organs, limbs, and nerves. In other words, cells that are generally undifferentiated become specialized cells of particular organs because of the position they occupy in the developing embryo. In this way, the embryo becomes clusters of specialized cells that form the foundation of all major bodily systems (Bogin, 1999). The embryonic period lasts from the end of the second week through the end of the eighth week after conception. During this time, the cell mass within the blastocyst forms a disk-shaped structure that becomes the embryo, sandwiched between the yolk sac and the amniotic cavity.

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Ultimately, the embryo develops three disks of cells (Bogin, 1999). One of these, the ectoderm, which is the thickest, eventually becomes the nervous system. The ectoderm also forms the basal cell lines of the epidermis of the skin, hair, fingernails, and tooth enamel, all of which later migrate during embryonic development. The endoderm develops into the digestive and reproductive organs and circulatory system, while the mesoderm forms the basis of the musculoskeletal system. Eventually, the ectoderm spreads into a sheath. The neural tube forms from the folding over and sealing of the ectoderm, while the spinal cord develops from the lower portion of the fold. The central nervous system begins as a suffuse bundle of nerves centered at the fore-end. Three pronounced areas of the fore-end become visible, corresponding to the forebrain, the midbrain, and the hindbrain. This cluster of rapidly developing neural circuitry—the beginning of the brain—assumes dominance over the extension of the middle tissue of the tubelike structure, which the spinal cord still partially reflects. Neurons begin to rapidly form in the walls of the neural tubes, but not necessarily in the place where they will eventually reside; thus some neurons travel to other locations within the developing brain. The circulatory system first develops at the start of the third week postconception, with the rhythmic contractions of a primitive U-shaped heart tube that shuffles the blood of the embryo to and from the umbilical cord and placenta using a rudimentary network of veins and arteries (Moore and Persaud, 1998). Meanwhile, pockets of nutrient-rich blood from the uterus are made available, and these will eventually abut the growing capillaries of the embryo. After three weeks postconception, a chorion develops and envelops the embryo. The placenta forms where the spongelike chorion attaches to specialized tissues along the uterine wall. Within the chorion and adjacent to the embryo, an amniotic cavity develops, later becoming a saclike structure that acts as a lung and stores waste. Eventually the amniotic wall fuses with the chorion. The amniotic sac holds a salty fluid that eventually surrounds the developing embryo and later fetus. On the other side of the embryo, within the chorion, is the primary yolk sac. Unlike the yolk sac in reptiles and birds, the yolk sac does not provide nutrients directly to the developing embryo but functions to transmit nutrients between the developing placenta and the embryo. The human yolk sac provides blood cells and fulfills some of the roles of the developing liver, which becomes operational at six weeks postconception (Moore and Persaud, 1998).

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Eventually the yolk sac is resorbed while the amniotic cavity enlarges, completely enveloping the embryo and later fetus. The amnion becomes the outer layer of tissue, which effectively seals the developing embryo from pathogens. The amniotic fluid functions to protect the embryo from sudden changes in temperature and movement, and the repositioning of the mother. Additionally, the amniotic fluid allows the embryo to move about freely and prevents adhesion to the amnion (Snow and McGaha, 2003). An allantois, a vestige of a reptilian past, also forms, and eventually becomes part of the umbilicus (Jones and Lopez, 2006). During the fourth week, a prominent tail become visible, as well as superficial limb bud swellings, the forelimbs preceding the hind limbs. Precursors of the milk teeth, or deciduous dentition, also begin to form during this period, as do the preliminary urinary organs, and the beginnings of the optic nerve. By the fifth week, synapses that connect neurons together into extensive neural networks begin to form in the spinal cord (Snow and McGaha, 2003). By the sixth week, the midface begins to develop between the forebrain nodule and the heart, while placodes, or circular darkened areas of specialized cells, can be observed. These correspond to the external openings of the skull, including the eyes, ears, and nose. A primordial gonadal streak has formed by the sixth week, and eventually becomes the precursor of the testes for males and ovaries for females during the seventh and eighth weeks (Lamb et al., 2002). By the eighth week, the Müllerian and Wolffian ducts are present in both males and females. In males, the primordial testes begin to secret testosterone as well as a Müllerian inhibiting substance, which enhances the development of the Wolffian ducts into the penis, testes, vas deferens, prostate, and adjoining canals. In females—who never receive the wash of testosterone—the Müllerian ducts continue to develop into the ovaries, fallopian tubes, uterus, cervix, vaginal canal, and clitoris while the Wolffian ducts disintegrate. Specialized cells within the developing ovary begin to increase up to several hundred thousand immature ovary cells, which, as mentioned previously, normally lay dormant for well over a decade. At the end of the second prenatal month, specialized cells in the developing testes are primed to become sperm-producing cells some thirteen to seventeen years later. Between the latter two-thirds of the prenatal period, testosterone affects the two main glands of the central nervous system, the hypothalamus and pituitary glands, to suppress the cyclical reproductive pattern characteristic of females (Lamb et al., 2002; De Vries,

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2004). In males, a flood of testosterone at puberty further suppresses the cyclical characteristics of female reproductive physiology. Synapses can be observed in the central nervous system during the seventh week, and by the eighth week, the central nervous system has grown to comprise about one half of the embryo. Also during the eighth week, the tail largely disappears. Somites begin to form along the exterior of the developing spinal cord, and these serve as reservoirs of embryonic bone cells from which the cartilaginous skeleton arises, with true bone cells arising at about nine weeks postconception. At nine weeks, all of the internal organs are formed, although in a rudimentary state, and the skeletal system is fully differentiated into cranial, vertebral, trunk, and limb bones, although the joints are merely swollen extensions near the ends of limb bones. Bones of the skull are relatively well-formed by the end of the first trimester, which lasts for about thirteen weeks after conception. At this time, the human resemblance is clearly visible, albeit with a trunk length of three centimeters, and is called a fetus, meaning “young one” (Snow and McGaha, 2003). A fetus has all of its organs and limbs in place, and a secure attachment to a food source, the placenta. While not a miniature human, the developing embryo/fetus begins a trajectory that resembles the body plan of all vertebrates, and includes a heart, brain, musculoskeletal system, and organs of digestion and body regulation, arranged along a vertebral column with a head distinct from the trunk from which the limbs extend.

Fetal Development During the second trimester, the fetus rapidly gains weight. After three months postconception, the fetus is the size of a plum, while at the end of six months, it is the size of a grapefruit, often curled up in “fetal position” during sleep, or moving its legs and arms spontaneously during short periods of wakefulness. This rapid weight gain is facilitated by an enriched placenta that becomes substantially larger at the end of the first trimester, thus relieving females from directly supplying the nutrient and elemental needs of the fetus from her own organs of metabolism. The organs of the fetal body are well developed at this time, but become increasingly more complex and functional. Relative head size decreases as trunk and leg length increase as a function of bone cell proliferation and weight gain. During the middle of the second trimester, fetal movement can be felt by the mother, known as “quickening” (Snow and McGaha, 2003). Meanwhile, a tremendous growth in num-

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ber of neurons occurs, along with the production of a fatty layer, or myelination, of these neurons by neuroglia cells. The fetus is covered with vernix caseosa, a thick paste-like layer that prevents the chapping of the skin from constant contact with amniotic fluid. Late in the second trimester, at about four months postconception, the fetus sports a furry coat of fine hairs known as lanugo that remains until just before birth or (rarely) shortly thereafter. During the third trimester, the placenta is as large as a liver. The placenta increases its efficiency of oxygen and nutrient transport and removal of fetal wastes, allowing the fetus to increase from three to four pounds to six to nine pounds or beyond during the last three months of gestation, essentially doubling its weight. The brain grows tremendously during this period in complexity and integration, and becomes about a third of the body weight. As the fetus increases in weight, it begins to respond to the social world of its mother through hearing the inflexion and tone of her voice and those around her. Regular periods of sleep and wakefulness occur, and the fetus can develop a habitual position while resting. Stretching, yawning, swallowing, thumb sucking, and grasping also take place, and the eyes become functional. During the third trimester, the cerebral cortex takes form along the exterior of the brain. In the last few weeks of gestation, the fetus acquires a layer of fat and some antibodies toward a variety of infectious diseases. Meanwhile, the placenta becomes increasingly less efficient in providing nutrients. Toward the end of the third trimester, the lack of space in the womb usually restricts the infant to the lower portion of the abdomen in a head-down position, with its face pointing posteriorly. At this time, the fetal head descends lower into the pelvis. If late-term fetuses are in an unusual position, they can be turned by a medical professional or health care specialist to avoid complications during birth. Gestation, from conception to birth, takes about 266 to 270 days in humans, or about 38 weeks (Jones and Lopez, 2006; Robson et al., 2006). This is similar to orangutan gestation, which lasts for about 260 days, and gorillas, in which gestation requires approximately 255 days. In bonobos and chimpanzees, gestation is shorter (244 days and 225 days, respectively; Robson et al., 2006). Pregnancy duration in apes has been remarkably conserved, despite the much larger brain size of human neonates compared to those of orangutans, gorillas, and chimps. However, only gorilla males maintain close contact with pregnant females of their group and may be the only ape to experience, however remotely,

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the kind of gestational fatherhood typical of pair-bonded human males with partners undergoing the gestation of a zygote, followed by a conceptus, embryo, and eventually a fetus.

Gestational Fatherhood Fathers can only live vicariously through their pregnant partner’s experience, particularly during the third trimester when fathers can actually see infant movement. Recognition of the upcoming birth event is inevitable, yet the inability to physically experience the pregnancy hinders a complete understanding of the physical, social, and emotional changes taking place in the mother. Women confronting birth recognize their dual nature of being human but also being an animal (Jolly, 1985). Males cannot approximate the physiological sensation of birth, the closest analogue of which may be expelling sperm during ejaculation (Mead, 1955). When a pregnancy reaches forty weeks since the last menses, intercourse may act to hasten birth through agitation of the cervix and vaginal walls, and prime the reproductive system of females to expel the fetus. Alternatively or concomitantly, semen may induce a hormonal reaction in females that results in labor. However, whether or not sexual intercourse occurs, birth is eminent.

Stages of Birth The basic reproductive biology of humans follows most closely the profiles of the nonhuman primates compared to those in other mammals. At birth, the newborn effectively becomes a new social entity within the group. The response to the newborn varies, but the birth process itself is remarkably conservative throughout the order Primates, which includes apes, monkeys, and prosimians. There are three phases of birth among primates. First, horizontal contractions force the neonate to descend. Next, longitudinal contractions expel the neonate from the vaginal canal. Expelling the placenta is the third phase (Jolly, 1985). In humans, labor lasts for as short as one to two hours and as long as twenty to twenty-four hours. Every birth process is unique and depends on a variety of factors, including the disposition of the mother, the expertise of the birth attendants, the neonatal position, and the health of the infant. Most women are able to fit the neonatal head through the pelvic inlet despite the past thirty years of increasingly larger numbers of Caesarian births.

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Birth is initiated when the needs of the infant outstrip the ability of the placenta to provide the nutrition and oxygen essential for further growth (Ellison, 2001). Although the exact triggering mechanism remains enigmatic, the birth process begins with the onset of labor and the commencement of contractions of the uterine walls. These uterine contractions proceed in intensity and often last eight or more hours. Labor can be longer for first-time, or primiparous, mothers, often lasting sixteen to seventeen hours (Lamb et al., 2002). At first, the contractions last about half a minute and can be up to thirty minutes apart. By the time the infant is expelled, contractions can be just a few minutes apart, are more pronounced, and can last from one to two minutes. Once the cervix is ten centimeters, women enter the transition phase and can begin pushing, or can soon thereafter expect an involuntary response to expel the fetus (Snow and McGaha, 2003). The fetal head first becomes lodged within the true bony pelvis. During labor, the uterus retreats back into the abdomen by becoming thicker superiorly and thinner and elongated inferiorly. Nevertheless, the fetus is surrounded by a thickened uterine wall that contains the amitotic fluid and is separated from the vaginal canal by a thick mucus plug. Once the cervix begins to dilate, the mucus plug will either efface or be expelled. A rupture in the uterine wall will allow the amniotic fluid to escape. Once the fetus is no longer protected by the amniotic fluid, it becomes more vulnerable to the outside world, and birth becomes eminent. Expulsion of the fetus requires complete cervical dilation, pushing of the diaphragm, and contraction of the abdominal muscles, and lasts between twenty minutes and two hours. Head rotation occurs during passage through the bony pelvis, followed by shoulder rotation.

Birth of a North American Infant Human birth is a momentous event. The slight difference between the size of the neonatal head and the birth canal is particularly evident after the head passes through the cervix but has yet to emerge into the external world. With each push, the head batters against the perineum rather than the more anterior location of the vaginal canal. The continued massaging and application of lubricant to the vaginal orifice first permits the upper part of the back of the head to surface; then, slowly, the entire back of the head emerges, known as crowning, followed by the upper and lower face. As the mother pushes, the back of the head

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emerges then retreats back as the contraction subsides, in a “two steps forward, one step back” fashion (Snow and McGaha, 2003: 43). Women are instructed to push, but push effectively. In a supine position tilted almost to a sitting position, two birth attendants (for example, a doula and the expecting father) can push onto the bended right and left legs, respectively, at each contraction. Once the head has emerged and the neck is visible, the birth attendant can pull a shoulder forward and grab the upper arm and hand out. The baby’s body and other limbs can then successfully slide out. Once the umbilical cord has finished pulsating, it is fastened with two clamps. The birth attendant, or father, can cut between them with surgical scissors, effectively separating the mother and baby. The remaining umbilicus and clamp can be gently tugged to dislodge the placenta, which takes ten to twenty minutes or longer to detach from the uterine wall. The physician inspects the placenta and then quickly skirts it into a plastic receiving bag, along with the bulk of the blood and umbilical fluid. The baby’s arms are held and then let go to check its reflexes—this first test speaks volumes and rules out a whole array of the most compromising congenital abnormalities. Thereafter, the baby is wiped clean. By not washing the baby, the smell of the mother is preserved for subsequent maternal recognition and bonding. There are two options during the first few moments after an uncomplicated natural birth. The infant can be placed either under a heat lamp or on the skin of a living person to maintain as much of a constant body temperature as possible. Recently parous mothers, who have just given birth, must still deliver the placenta. The neonate can be placed on the father’s naked chest and abdomen, which becomes available by removing the father’s shirt, while a blanket can be kept over the two to maintain warmth. This provides a social way for a neonate to spend its first few moments of independent life, permits an initial bonding between the father and child, and stimulates the production of prolactin in the new father, which is an evolved response for paternal caretaking behaviors in primates and other animals (Gettler et al., 2012a). Infants show a preference for humanlike facial patterns soon after birth (Hrdy, 2016). Alternatively, the mother can bond initially with the infant; in this scenario, the neonate is placed on the ventral surface of the mother. The umbilical cord need not be severed immediately, and the baby can receive about 25 percent more blood if it is not cut until it stops beating after a few minutes. There is tremendous variation in umbilical cord length, with males usually having longer ones than females, and they

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generally are about twenty inches long (Morris, 1992). However, the umbilical cord is normally long enough so that the infant can remain attached to the mother for the first several minutes after parturition, while keeping warm from the mother’s body heat to recover from the trauma of birth (Morris, 1992). This provides time for mother-infant bonding to take place. Neonates are awake for only a few hours following the birth event. After the placenta is delivered to prevent infection, blood clots and tissue must be expelled from the uterus by intensive massaging of the abdominal region. Breastfeeding can commence within the first thirty minutes after birth. For the first few weeks, breastfeeding takes place multiple times per hour when the neonate is awake, followed by progressively longer periods contingent on infant needs, the availability of the breastfeeding mother, and the support of the recognized father and/or family. This differs from birth among the Efe foragers, in which all of the members of the mother’s hut, including children and other relatives, hold the baby; then the baby is taken outside of the hut to meet the other members of the camp, and about an hour or so later, the mother finally gets to hold her baby (Morelli and Tronick, 1987). Another lactating relative and/or friend will also nurse the baby during the first few days postpartum while the mother’s milk production increases (Morelli et al., 2014). Breast milk provides important immunities, as well as live cells, amino acids essential for development, and other contents not found in formula substitutes (Sellen, 2006). Additionally, breast milk positively enhances infant temperament, improves hormone regulation, and is rich in fatty acids utilized in the myelination of nerve cells during neurodevelopment (Dettmer et al., 2014). Breastfeeding promotes attachment between the infant and mother and enhances sociality (Sellen, 2006; McKenna, 2014). Moreover, the benefits of having received maternal breast milk continue into the juvenile, subadult, and adult life-cycle stages (Dettmer et al., 2014). In contrast to the shorter duration and reduced intensity of breastfeeding often found in Western cultures, among foragers and food producers in non-Westernized societies, infants are likely to be intensively breastfed for the first several years after the birth. Newly born full-term babies are covered with a waxy coating consisting of a combination of oily secretions from hair follicles and excess skin flakes, called vernix caseosa (Morris, 1992). Hair follicles begin to produce a greater intensity of oil a few months before birth, suggest-

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ing that it serves to lubricate the parturition, and perhaps without it, a natural birth is unable to occur. The coating also helps the neonate adjust to the temperature difference between the womb and the external world (Morris, 1992). The vernix may also assist in protecting the neonate against extrinsic pathogens and peels away after two to three days if the baby is not washed beforehand.

Birth in a Papua New Guinea Village As reported from fieldwork conducted by Ian Hogbin in the midtwentieth century subsistence village of Busama off the eastern coast of the island of Papua New Guinea, fathers dug a hole in the floorboards of the house in anticipation of receiving the placenta. The expecting father was accompanied by the father and brothers of his wife and his close associates, but was unable to relax or eat until he heard word of a successful birth. According to Hogbin (1963: 56), “Not until a messenger arrives at sunrise with word that he was the father of a healthy daughter and that his wife, though worn out, was well, did he compose himself. He then lay down and was soon fast asleep.” Upon the beginning of labor, Hogbin (1963: 56) relates that “the midwives take off the parturient woman’s calico dress, an expensive item, and replace it with a grass skirt. Thereafter, one of them kindles a fire to provide warmth and better illumination. They then make the woman lie down, and they take turns massaging her back and abdomen with a steady downwards pressure.” When delivery of the baby is imminent, “the woman crouches near a hole in the floor with her knees bent. One of the midwives supports her back, and a second continues the frontal massage till the child’s head appears, when she holds her hands ready. If the placenta comes out immediately afterwards the cord is cut with a razor blade so as to leave several inches” (Hogbin, 1963: 56–57). There are a number of rituals performed by the mother with the remaining end of the umbilical cord after it desiccates and falls off of the baby. Meanwhile, “the baby’s naval is smeared with a mixture of ashes and saliva” for several days after the birth (Hogbin, 1963: 57). Immediately after the passage of the placenta, “the woman’s mother now bathes both her and the infant with warm water” (Hogbin, 1963: 57). When the woman is strong enough, the baby is placed under her arm, although the baby is nursed by other women relatives until her milk comes, and “the father is also called upon to share the nursing when his wife gives birth to twins” (Hogbin, 1963: 57). A father was

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not given much opportunity to visit with his infant during the first two weeks, but by six months “he holds it for any length of time” (Hogbin, 1963: 58).

Birth Practices among the Batek of the Southern Malaysian Peninsula Batek birth practices were described to Endicott and Endicott by camp members, who reported that “unless labor began unexpectedly, Batek babies were born in special lean-to shelters set in the forest away from camp” (Endicott and Endicott, 2014: 110–11). The shelter was described as having “a floor of split bamboo, sticks, or bark and some sticks struck diagonally through the floor for the expectant mother to learn against” (Endicott and Endicott, 2014: 111). The expecting mother “sat with her knees drawn up and a cloth covering her abdomen and thighs” (Endicott and Endicott, 2014: 111). The Batek practiced assisted birth, whereby a “midwife, usually an experienced older woman, and a few other women assisted” (Endicott and Endicott, 2014: 111). During labor, “the midwife massaged the mother’s abdomen” ultimately receiving “the baby in her hands when the mother pushed it out” (Endicott and Endicott, 2014: 111). Directly following the birth, “the midwife placed the baby between the mother’s feet and then bathed the mother and baby with cool water to prevent fever” (Endicott and Endicott, 2014: 111). After cutting “the umbilical cord with a splinter of bamboo,” the midwife “wrapped the baby in a cloth, and placed it at the mother’s breast” (Endicott and Endicott, 2014: 111). Upon recovery from the experience such that the mother was “strong enough to walk, she returned to her family shelter in camp” (Endicott and Endicott, 2014: 111). Thereafter the mother would return to the birth shelter for three or perhaps four days “to keep a fire burning beside the placenta, which was left covered by a pandanus leaf mat” to ward off the possibility that either her or her baby would fall ill with a fever (Endicott and Endicott, 2014: 111). Similar to most small-scale societies, Batek forager mothers breastfeed and cosleep until the child is three to four years, although if another pregnancy occurs before this time, she must wean, as lactation is compromised. Upon the eruption of the teeth, breastfeeding is supplemented by softer foods of the local diet, and eventually solid foods are introduced (Endicott and Endicott, 2014).

3 Couvade and Hormonal Correlates of Paternity A number of early ethnographers, such as Sir Edward Burnett Tyler (1865) and Bronislaw Malinowski (1927), mention couvade as central to understanding the role of fathers in societies. For example, Malinowski (1927: 215–16) suggests: Even the apparently absurd idea of couvade presents to us a deep meaning and a necessary function. It is of high biological value for the human family to consist of both father and mother; if the traditional customs and rules are there to establish a social situation of close moral proximity between father and child, if all such customs aim at drawing a man’s attention to his offspring, then the couvade which makes man simulate the birth-pangs and illness of maternity is of great value and provides the necessary stimulus and expression for paternal tendencies. The couvade and all the customs of its type serve to accentuate the principle of legitimacy, the child’s need of a father.

Since males are not biologically necessary for the birth process to occur, their presence can be seen as a strictly cultural practice. Many cultures around the world have strong traditions or rituals of male-infant involvement after birth, or have magic or religious practices, termed couvade, to help cement the societal role of fathers and their commitment to the neonate (Coelho, 1949; Broude, 1998). Couvade can take many forms, being mild or extreme measures such as confining a prospective father to bed. In parts of Scotland, “married man’s toothache” was invoked to lay a man to rest, whereas in continental Europe it was termed “man childbed,” wherein recent fathers would “lie-in” for varying lengths of time to contemplate the responsibility of a recognized father-infant relationship. Lying-in refers to the male being prostrate,

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periodically resting with the infant, for varying hours, days, or weeks, depending on the culture. Couvade can involve father participation in the gestation, birth, and immediate postnatal process in a physical sense through psychosomatic symptoms, dramatic empathetic performances, food taboos, avoidance of certain objects (such as knives), being bedridden, starvation, and other various ways of expressing partnership with the pairbond during the pre- and postpartum process. Prenatal couvade is associated with bonding with the spouse, whereas postnatal couvade recognizes the unique relationship between the father and infant. Cultures differ with respect to the role of fathers during labor and birth. In some cultures, males play an intimate role, and in others, males are excluded entirely. However, most cultures lie between these two extremes. For example, among the Ache, the primary father will go hunting during the labor of his wife—particularly first-time fathers (Hill and Hurtado, 1996). Upon returning, fathers will feign disinterest in the outcome of the birth process. Thereafter, Ache fathers become active caregivers, although not to the extent observed in other cultures, such as among the Aka, Agta, and Batek (Hewlett, 1991; Endicott, 1992). Couvade is mentioned by classical authors and ancient travelers, such as Marco Polo, and has been observed primarily in South America, the Caribbean, parts of Africa, Europe, South and Southeast Asia, and the archipelago, but apparently not in greater Australasia, at least according to Warren Royal Dawson (1929). Myths and recordings of couvade exist in Cyprus, Ireland, the Basque country, Corsica, and the Balearic Islands. Strabo reports couvade in the Iberian Peninsula and among the Celts of Thrace and Scythia (Dawson, 1929). The custom apparently persisted in parts of the Pyrenees, such as Navarre and Bearn, and along coastal areas of France, in the nineteenth century. The custom was known into the twentieth century in Oxfordshire, Cheshire, and Yorkshire, the northeast of Scotland and other areas of the British Isles. In Africa, it has been reported among the Bagesu on the northeast of Lake Victoria, along the White Nile, in the south of Sudan, and among the Dinkas (Dawson, 1929). In the eighteenth century, couvade was reported at Kasanje in the Congo, and the practice may have persisted into the twentieth century among the Boloki and other tribes of the Congo basin. Ancient writers recorded couvade customs among the Tibareni along the southern shores of the Black Sea. It has been observed historically

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in India, and some castes still maintain proverbs related to lying-in behavior of recent fathers, including basketmakers, such as the Pomla and the Koravar. The Erekulas in the South of India traditionally maintained a custom whereby upon the commencement of labor, the husband retreated to bed where he was to remain until the baby was brought to him, and thereafter he was not permitted to leave the bed for two weeks (Dawson, 1929). A similar custom existed among the Koramas into the twentieth century. Among the Paraiyan, the husband was practically starved for seven days following the beginning of labor, only receiving some fruits and tubers. The Nayadis of Cochin traditionally practiced couvade customs, wherein the husband washed his abdomen and prayed during labor and delivery. Customs related to the recognition of fathers have also been reported from central and northern India, such as the Miri of Brahmaputra Valley, the Assam and Tangkhuls, the Hindus of northern India, the Deshasht Brahmans of Mumbai, and among the Sonjhara caste of central India. Marco Polo reported couvade in Zardandau in Chinese Turkestan (Dawson, 1929). A common theme of many central and South Asian couvade customs is that at the onset of labor, the recognized father, or husband, goes to bed and remains there for forty days alongside the new infant. This bonding perhaps forms the basis of later child-father relationships, and more decidedly ensures that fathers would remain social actors and providers for their socially recognized descendants until their maturation nearly two decades later. Couvade in many of its classical manifestations has been reported in the Ainu of Japan and in Kamchatka. It has been observed in several locations in the Southeast Asian archipelago. In an inland tribe on Great Nicobar, on Car Nicobar and on the southern islands, it is likened to hatching an egg, whereby the socially recognized father must not leave bed for five days after the birth of his infant; he is treated as an invalid, and may not even bathe for two to five days, depending on the location. It is generally assumed that the infant’s health depends on the father observing couvade, and is often accompanied by food restrictions, fasting, and the cutting of lashes that are repaired after the custom has been completed. In Busama on the eastern coast of New Guinea, upon the birth of a child, the new fathers, like the mothers, were reported to avoid salt. Additionally, the new father “abstains from eating saltwater fish” and “even when the father is allowed salt-water fish he does not eat those with large scales—they might give the child a skin disease—nor

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those with protruding eyes—they might cause it to develop a squint” (Hogbin, 1963: 60). In this case, as in others, cultural contrivances were employed to ensure that new fathers were kept away from the dangers of sea fishing, particularly deep sea fishing. In addition to couvade, food restrictions on both parents until the infant could walk were traditionally required in various groups in the Malaysian Peninsula, such as the Orang Benu-wa of Malacca and the Boeginese and Macassarese in Johor on the Madek River, as well as on the islands off the coast of Sumatra. Couvade was reported from the Philippine Islands in the Bontok area and other parts of central Northern Luzon. In the Tagals of Luzon, both parents were required to follow certain food taboos. The Macusis of Guiana practiced couvade customs that involved both the parents being confined together with the new infant for almost a week. The parents were not allowed to work or bathe and were required to eat only cassava. The new father was not permitted to scratch himself, for fear of symbolically injuring the infant. In the Mentawi Islands, husbands could not work or even leave their houses for two months after the birth of the infant. In the Land Dyaks of Borneo, socially recognized fathers were not permitted to work with sharp instruments and were to refrain from violence, lest he damage the new infant. He subsisted on a diet of rice and salt during his seclusion, which traditionally lasted for several days. Reports from the seventeenth century by Schouten suggest that among some groups, like the Alfoeros of Boero, the husband falls infirm upon the birth of his infant, while the wife shortly thereafter resumed her normal activities and tenderly cared for the prostrate man. On the island of Timor Laut, the father traditionally cared for and carried the new infant around while the mother resumed her domestic chores after bathing. At San Christobol and other locations in the Solomon Islands of Melanesia, a father traditionally refrained from heavy labor for two to three weeks after the birth of his infant, and in some places, fathers were confined to bed for several weeks. Any physical excursion on Leper’s Island by the father was thought to be a danger to the newborn, including travel. On the Bank Islands, fathers were restricted from work for five days and could not engage in extreme physical labor for one hundred days. In New Ireland, an expectant father, once labor began, sympathetically took on the sensations associated with delivery by lying in bed, while simulating imaginary birth pains until the infant was born.

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In various foraging societies of precontact California, couvade was practiced by new fathers who would lie down and show extreme weakness for three to four days while the women went about their normal routines shortly after parturition. In central California, the soon-to-be father would lay in bed, groaning with the ache of sympathetic birth pain until the infant was born. He was then nursed back to health by his wife. Among the Lagunero and Ahomana of indigenous New Mexico, new fathers were confined to their homes and restricted to a vegetarian diet for about a week. The Caribs of the West Indies are widely noted for their elaborate couvade customs, surviving into the present day. Traditionally, a new father would take to bed after the birth of the infant, where he was visited by friends and relatives, as when ill. Thereafter, new fathers were expected to fast during the first five days and show restricted caloric regiments for forty days after the birth of their infant. The Arawaks of Suriname have also been observed practicing couvade (Farabee, 1918), as have various societies in Amazonian Brazil, such as the Bakari, the Petivares, societies along the Rio Yupura, the Passem, the Juri, the Mundzucu, and the Tupe. Along the border of northeast Brazil and British Guiana, the Tarumas and other tribes practiced the ancient traditions of couvade (Figure 3.1; Farabee, 1918). Among the Jivaro of Ecuador and Piojes of Putumayo, a father was required to sympathetically enact the birth outside the home; then, after the birth, he was in so weakened a condition that he was confined to bed to recover from the shock of assuming the social role of fatherhood. Among the Abipones between Santa Fe and St. Iago in South America, a new father went to bed in privacy for several days upon the birth of his infant. Both the father and the children observed couvade by resting and fasting among the Chiriguanos of Paraguay (Dawson, 1929). A common theme in these customs is the apparent or imposed weakness and infirmity of expectant fathers that remove, by sympathetic actions and vocalizations, the pain and suffering of childbirth. Many societies have been reported to provide excess to the fathers, lavishing complements and visiting, while the mothers are seen to continue their domestic chores within a day or so, even to the extent of providing particular favorite or elaborate meals to the bedridden new father. However, this may be a difference between the real and ideal. Clearly the reduction in caloric intake would provide leisure time to spend with the newborns and would encourage the presence of the father for

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Figure 3.1. Tarumas (outer) and Mapidan (middle) individuals are shown in this photo taken circa 1918 along the border of northeast Brazil and British Guiana, where a number of tribes practiced the traditional custom of couvade. After the child’s birth, the father would be confined to his hammock for the first postnatal month. During that time, he would be given prepared foods, while avoiding the hot sun and hard labor. For two years thereafter, the father would refrain from hunting poisonous snakes or dangerous animals, for fear that the spiritual bond between father and infant would be perturbed and in so doing would harm the latter (Farabee, 1918). Through couvade, fathers became proximate to the fact of birth and formed a bond with the infant and mother, increasing the likelihood of infant survival through provisioning and direct paternal care. Image from Farabee (1918), plate 1.

an extended period of time. The forbidden nature of touching pointed objects, such as hunting instruments, may have restricting males from leaving on outings that could involve bodily danger (Dawson, 1929), because females who have just given birth need support for the infant from the father.

Explanations of Couvade The term couvade is derived from the French verb couver, to brood or nest, and was first used by Tyler in the nineteenth century (Brennan et al., 2007). A number of reasons have been offered to explain couvade

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as it was originally practiced. Diffusionists considered the presence of couvade in so many cultures separated spatially and temporally to be evidence for the inheritance of the custom from a common human ancestor, rather than by independent invention alone. However, a diffusionist interpretation did not explain the presence of cultures practicing couvade next to those that did not. Others such as Bronislaw Malinowski point to a functional interpretation (Munroe et al., 1973); in a species where biparental care is highly valuable for the reproductive success and long-term survival of offspring, couvade attracts the attention of socially recognized fathers and primes them to assume the role of caregiver. The magical or religious practices that accompany the birth of a child help provide legitimacy to the offspring as the recognized descendant of the father. In some instances, men follow the same dietary restrictions imposed by cultures on pregnant or postpartum women and thus can symbolically unite with and even draw away the pain experienced by the new mother (Dawson, 1929). Some find couvade to be an expression of duty from a father to his family (Coelho, 1949). Others suggest that couvade is widespread for the same reasons that other rituals are widespread; they allow for more control of an uncertain situation (Munroe et al., 1973; Munroe and Munroe, 1989). Couvade is partitioned into two phenomena by Broude (1988), who suggests that much of what is called couvade is actually magico-religious rather than psychosomatic. Many of the magico-religious practices are believed to protect the infant from harm or encourage growth. Broude (1988) found that couvade is positively associated with father salience. High and moderate levels of father presence were associated with couvade, whereas father absence was not. The onset of fatherhood is a life-changing experience, marked for its profound meaning and transformative effect during the life history of human males. The process of becoming a gestational father is a developmental crisis (Clinton, 1986). Fundamental changes in social identity must occur without the physical symptoms demarcating the passing of this life history event. Anxiety can often accompany gestational fatherhood, and in severe cases can interfere with empathy for the spouse and later bonding with neonates. Yet there is no formal recognition of the pressures of fatherhood in many cultures; these cultures lack the acknowledgement of this transformation that many traditional societies demarcate with couvade practices.

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Couvade Syndrome In the psychological literature, “couvade syndrome” is a behavioral pattern whereby expecting fathers form an attachment to the fetus by exhibiting some of the signs of pregnancy, such as vomiting, nausea, bloating, weight gain, muscle aches, toothaches, anxiety, lethargy, upper respiratory and sleeping difficulties, heartburn, leg cramps, and other symptoms (Valentine, 1982; Brennan et al., 2007). Couvade syndrome differs from traditional forms of couvade because the former is idiosyncratic rather than a typical cultural behavior. Couvade provides an attachment within the family and awareness of the responsibilities expected of socially recognized fathers, whereas couvade syndrome is an internalized state of extreme empathy by gestational fathers. The manifestation of the symptoms of pregnancy by expecting fathers occurs in industrialized nations and elsewhere. Between 11 and 97 percent of all expecting fathers may exhibit some symptoms of pregnancy in countries as diverse as Russia (35 percent), China (68 percent), Thailand (61 percent), and the United States, estimated by some at 11 percent and others at 97 percent (Brennan et al., 2007). The severity of the symptoms is variable and often goes unreported. There also seems to be no difference between gestational fathers experiencing a first “birth” and those who are already parents. Couvade syndrome is difficult to account for because of the broad range in type and severity of symptoms. Medical professionals have considerable difficulty linking the husband’s self-reported symptoms to a partner’s pregnancy (Brennan et al., 2007). Couvade symptoms reported by the mother must also be taken into account. Browner (1983) found that women who relied economically and emotionally on their husbands were more likely to report couvade syndrome than their less dependent counterparts. Although the relationships to age, class, ethnicity, and other demographic factors are disputed, the time span of couvade syndrome is fairly well documented as U shaped, where the symptoms are most heavily expressed during the first and third trimester and end at birth or early in the postpartum period (Brennan et al., 2007). However, J. F. Clinton (1987), from interviews with more than thirty-nine gestational fathers, did not find a difference between trimesters. Among thirty-nine possible couvade syndrome symptoms, 7 to 12.4 percent of cases were reported per trimester. One of the most profound symptoms at six weeks postpartum is depression. The symptoms usually lasted 1 to 2.5 days.

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Hormonal Correlates of Paternity Gestational fathers may take cues, hormonally or socially, from their partner’s pregnancy experience. An increase in prolactin and decrease in testosterone may signal basic changes in the hormonal profile of gestational fathers (Gettler et al., 2012a), as it does in birds and other vertebrates (Wingfield and Goldsmith, 1990). Altered hormonal profiles are experienced by males who have close emotional contact with their pregnant partners, and depend on how extensively males are present to observe and hormonally mimic pregnancy symptoms (Storey et al., 2000). Prolactin is one of the primary hormones that stimulates and maintains lactation in mammalian females and is intimately involved in the evolution of caretaking among vertebrates. Prolactin secretion counteracts the effects of dopamine, a hormone needed for sexual excitement to occur. Excess prolactin production may interfere with spermatogenesis, but this is a rare condition. Additional hormones are affected by prolactin, namely cortisol, estrogen derivatives, and testosterone, among other androgens. Prolactin levels have been explored more fully because they vary with disposition, parity, and reproductive condition (Storey et al., 2000; Schradin and Anzenberger, 2004). In humans, prolactin levels in males and nonpregnant females overlap considerably, while those in pregnant and lactating women can be twelve times as high. In contrast, oxytocin levels of mothers and fathers of newborns overlap and change in response to different types of child interaction (Gordon et al., 2010b). Responsive males exhibit higher prolactin and cortisol and lower testosterone levels than males who did not show much interest in newborns (Fleming et al., 2002; Archer, 2006; Delahunty et al., 2007). An increase in prolactin levels was also shown in a study of Filipino males before and after becoming fathers (Gettler et al., 2012a). Males who are sensitive to the physiological changes happening in their partners increase prolactin production, which can result in some weight gain. Testosterone levels begin to drop precipitously as parturition approaches in pair-bonded men (Storey et al., 2000). Indeed, testosterone levels vary by degree of involvement in parenting and marital status (Gray et al., 2002), level of extraversion (Alvergne et al., 2010), and sexual behavior (Gettler et al., 2013). In a longitudinal study of Filipino males from Cebu, the Philippines, nonpartnered males who eventually became fathers had higher testosterone levels than males who did not become fathers. However, upon becoming fathers, those males exhib-

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ited lower evening testosterone levels than nonfathers and exhibited steeper declines of testosterone diurnally than nonfathers (Gettler et al., 2011b). Lower testosterone levels were also observed in married fathers compared to unmarried males among US military veterans (Mazur and Michalek, 1998); Harvard Business School students (Burnham et al., 2003); Albuquerque, Atlanta, Beijing, Boston, and Kingston, Jamaica, residents (Gray et al., 2004, 2006, 2007b; Hooper et al., 2011; Mascaro et al., 2013); Ariaal pastoralists (Gray et al., 2007a); and rural Polish farmers (Alvarado et al., 2015). This was also true for partnered University of Michigan students (van Anders and Goldey, 2010)— at least those without a strong desire for uncommitted sex (Edelstein et al., 2011)—and, to a lesser extent, among Swahili speaking monogamously married fathers from Kenya (Gray, 2003). The relationship between testosterone levels and reproductive status is the most pronounced in societies where nuclear households are normative (Gray and Campbell, 2009), such as industrial economies and among foragers. Additionally, it seems that testosterone levels are more responsive to father care than to marriage, given that African pastoralists who are wholly separated from infants do not differ from single men, while both differ from Hadza forager males with lower testosterone levels and greater father-infant proximity (Marlowe, 2000; Muller et al., 2009). Furthermore, fathers who cosleep with their infants and the infants’ mothers—who also exhibit greater infant care—exhibit lower testosterone than fathers sleeping apart (Gettler et al., 2012b). Among Hadza foragers, a greater difference between fathers and nonfathers is evidenced in the evening compared to the morning, reflecting the suppression effect of social contact with infants (Muller et al., 2009). In addition to lower testosterone, smaller testes volume characterizes those who see themselves as caregivers and who report more father care of 1- to 2-year-olds in Atlanta (Mascaro et al., 2013). However, acute testosterone increases can be observed in males during subsistence tasks, suggesting alternating levels are highly specific to social stimuli (Trumble et al., 2013). Hearing simulated infant cries with subsequent nurturance decreases testosterone in males (van Anders et al., 2012), while listening to infant distress without recourse increases levels, perhaps as an evolved reaction to imminent danger (van Anders, 2013). Lower testosterone decreases aggression, whereas higher oxytocin and prolactin increase the empathy of fathers, suggesting an evolved physiological response (van Anders et al., 2011).

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Affectionate fathers of newborns exhibit higher oxytocin levels than those who are uninvolved (Gordon et al., 2010a). Oxytocin modulates mother-infant bonding in mammals, and it is possible that all social bonds are influenced by this hormone (Kosfeld et al., 2005; Gordon et al., 2010b; Feldman et al., 2012), including those between fathers and their infants (Naber et al., 2010; Feldman et al., 2011) and between males (Rilling et al., 2012). Hormones such as oxytocin and arginine vasopressin provide proximate reactions to social bonding and nurturance, and modulate feelings of affinity essential to maintain relationships between social partners (van Anders et al., 2011). During human evolution, fathers likely bonded with neonates using couvade, which was reinforced by the hormonal correlates of reproduction and nurturance. The greater frequency and duration of proximate contact between fathers and infants, the stronger the social bonds between them. These social bonds would act to ensure the provisioning of dependent children until the requisite survival skills, such as hunting, extractive foraging, and reciprocity, were mastered at adulthood (Kaplan and Robson, 2002).

4 Postnatal Infant Development During the first three months of life, neonates sleep up to twenty hours per day. Neonatal sleep-wake cycles are spaced evenly across day and night over a twenty-four-hour period. Over the course of the first few postnatal months, a segment of the hypothalamus known as the suprachiasmatic nucleus matures, and eventually neonates learn a circadian rhythm using daylight and social cues to help consolidate sleep (Guyer et al., 2015). During this period, the body grows rapidly, but the brain outstrips the pace of body growth and doubles in size over the course of a year. The interaction between neonate and caregivers (fathers and mothers) grows increasingly richer, and includes eye contact, recognition, smiles, and elimination communication (Sun and Rugolotto, 2004; Woermann et al., 2014). The separation of infants from caregivers reflects cultural ideals particular to Westernized societies that value independence and individuality (Edwards et al., 2015). Hunter-gatherer societies, in contrast, exhibit cooperative child-rearing by multiple adults and older children, near-continuous proximity, breastfeeding on infant demand, cosleeping with infants, and other traits that can describe the ancestral condition of humans (Konner, 2010). These patterns resemble infant care in nonhuman primates, particularly anthropoid monkeys and apes, labeled the “evolved developmental niche” (Narvaez et al., 2014: 7). The separation of infants from trusted caregivers leads to infant anxiety, signaled by crying, which is why it is avoided in many cultures. Many non-Western cultures tend to prioritize caretaker-infant proximity, particularly among breastfeeding mothers. For example, among Aboriginal foragers of central Australia, “when a child is born into a family it is normally left to the mother who gave it birth to nurse and suckle it, a process which usually lasts some four years” (Montagu, 1974: 345). Among the Batek, infant cries were responded to rapidly until the age

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of three or four years. At this age, mothers would “not heed every cry” to inculcate independence (Endicott and Endicott, 2014: 111).

Neonatal Period One of the primary means to communicate mutual interest among humans is to examine the pupils of nearby individuals. Neonatal eyes are flatter than those of adults and lack the ability to focus, stemming from the immaturity of the visual system (Snow and McGaha, 2003). However, neonatal pupils can often focus on those of another human or an object from the moment of birth (Super and Harkness, 2015), although, depending on the infant, the focus can momentarily be suspended after the loss of coordination of the eye pair. This loss of focus diminishes steadily over the course of a week, so that by the end of seven days, the baby can generally track the subtle shifts of eye movement that are the basis of human social interaction, face-to-face conversations, and other intimacies. Soon after the immediate neonatal period, infants may smile when their eyes focus on a familiar person, evidently recognizing an individual. The smile is an ancient behavioral characteristic that evolved from fear grimaces in ancestral primates. Infants may repeat short smiles, separated by about ten seconds. However, some infant smiles may not communicate emotional states during the neonatal period (Fitneva and Matsui, 2015).

First and Second Weeks The first and second weeks of postnatal life is transformative in terms of body coordination and orientation. Infants most often are able to interact socially via eye contact, and are attracted to human faces even as neonates (Fitneva and Matsui, 2015). Using eye-to-eye contact during these social events, both parties come to realize a mutual awareness exists. In this way, human neonates differ from other mammals from a very young age by the ocular awareness evident in a newborn’s eyes as they follow the social cues demonstrated by others. Toward the end of the first week, through subtle movements, neonates can direct their bodies toward a desired object, such as an arm, when their body is positioned vertically. Human infants naturally gravitate toward being erect, and this position becomes increasingly preferred during the first or second postnatal week. Vertical postures are typical of nonhuman primates during feeding, social grooming, and some forms of locomotion, like hopping, bipedal survey, dominance display, and short bursts of bipedal walking (Figure 4.1).

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Figure 4.1. Exemplified by this sifaka (Propithecus verreauxi ) is the tendency for all primates, including neonatal and infant humans, to prefer vertical postures. This enhances the ability of the forward-facing eyes, in concert with a mobile neck and relatively large brain, to process stereoscopic visual images. An emphasis on vertical postures must be an ancient trait for primates, given its presence in lemurs, lorises, tarsiers, monkeys, apes, and humans.

Vocalizations and sighs are regular events during the first week. These become more cohesive during the weeks thereafter, as neonates continue to mimic the language rhythm they heard prenatally (Fitneva and Matsui, 2015). These vocalizations differ from crying in its various forms, including what some call “fussiness,” which serves to signal discontent. Crying is one of six universal calls that humans make irrespective of culture. Others include laughing, sighing, groaning, sobbing, and crying in pain (Schultz and Lavenda, 2009). Neonates are noted to have five primordial emotional states, including distressed, disgusted, startled, experiencing pleasure, and exhibiting interest (Friedlmeier et al., 2015). Crying is communicated by the first three of these. Throughout the first two postnatal years, and particularly during early infancy, when the cries of infants for trusted caretakers are promptly addressed, it promotes an increase in self-confidence later during maturation and adulthood. Nonresponsive parents are relating to infants that their needs and wants are unimportant, which can result

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in deeply experienced feelings of anxiety (Sears and Sears, 2003). The philosophical perspective that values independence and individualism at the expense of comfort to infants is a form of neglect. Indeed, “the cross-cultural variation of parental roles should lead us to question how much of our own categorization of Western parental roles has to do with cultural beliefs” (Endicott, 1992: 294). In infants of Efe foragers, where babies are passed to different familiar caretakers throughout the day, crying results in a quick reunion with the mother for breastfeeding. The need for nurturance and comfort is often the reason for the infant’s distress. Infant needs are addressed without delay, within an average of 8.4 seconds for young infants and similarly for older infants (Morelli et al., 2014). To comfort infants, a soft, soothing tone is often employed by trusted caretakers. The practice of speaking to infants in a soothing voice may be universal (Fitneva and Matsui, 2015) and ancient (Falk, 2009).

Third Week During the third week, and sometimes earlier, infants can hold their heads up for a limited period of time (several seconds) if allowed to be vertically positioned during wakefulness (Lamb et al., 2002). Infants who are not held often will be slower to develop the ability to hold their heads independently. Neonates will respond to cues about elimination, such as a caretaker blowing on the top of the infant’s head, followed by vocalizations mimicking urination and defecation while the neonate is held over a receptacle (Rugolotto et al., 2008). Infants like their hands free and readily find their thumbs, although thumb-sucking, at least for babies breastfed on demand, is often only for short intervals. During this time, babies start to extend their legs as if trying to stand. These are their first efforts at bipedal walking. It is possible for very young neonates to exhibit limited communication. As primates, neonates are born with an interest in mimicking other social group members. For example, to increase breastfeeding efficiency, mothers often open their mouths wide so that the baby will mimic this behavior. Opening the mouth increases the surface area between the mother and infant during breastfeeding. This also eliminates a painful latch from a partially closed infant mouth. Other ways neonates, from birth to three weeks, can imitate include lip pursing, tongue sounds, smiles, staring with alternating focus on each eye, and opening the eyes wide. These kinds of social mimicking also provide a way for caretakers and infants to bond and socially attach.

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Fourth to Sixth Weeks During the fourth week or thereabout, an infant may be able to follow the movement of a familiar face from one direction to the other. Infants may now be able to move their focus to maintain eye contact with movements of the eyes and neck (also known as tracking). Infants often respond positively when their feet are moved and enjoy bracing their feet or hands against a caretaker’s hands. In the fifth week, infants show some increase in the strength of their legs and enjoy bracing them as though in bipedal stances. Infants begin to have much more control of their bodies and are able to bring their limbs inward at will. Infant smiles and eye contact are now increased substantially (Woermann et al., 2014). Defecation and urination slowly becomes more episodic, at least for babies breastfed on demand, compared to the earlier weeks of postnatal life. At this point, infants turn their heads and “lock” into a focus, which is categorically distinct from earlier weeks. Infants during the sixth week begin to stare at caregivers. These intervals demonstrate a desire for sociality that is inherent in primates. Infants signal contentment when they are awake and not showing signs of agitation, and these periods can be increased by allowing for a mutual interest to be signaled by close proximity and mutual gazing.

Monkey Feet and Sociality Infant feet are highly sensitive and are sources of communication with caregivers. Obviously, warm-weather babies are provided a greater amount of time to explore with their feet compared to infants born in cold climates or during the winter months. The number of touch receptors in the feet is nearly equivalent to those governing the hands, owing chiefly to the former use of the feet as grasping organs in a distant ancestor. The hallux or big toe is slightly divergent from the other toes at this stage of the infant’s young life, as this digit has yet to be subjected to the regular constraints of footwear. Infants will try to grasp with their toes against a caretaker’s finger. By increasing tactile communication with the feet and hands, a caregiver can amplify the sociality of infants by stimulating the sensory cortex of the brain. The proximity between nonhuman primate individuals in social groups communicates their mutual interest. Across primates, proximity reflects levels of intimacy and kinship. Being proximal to the baby communicates to them that the known caretakers are interested and engaged. Devices such as car seats, perambulators, baby carriages, playpens, and

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other tools that separate infants from caretakers interrupt these proximal relations. Being carried in caregivers’ arms, or within arm’s reach, for the first several months if not the first year for the majority of the time limits distress, which enhances the cerebral organization of information and somatic growth. Infant stress is energetically expensive and interferes with processes involved with maintaining attention (Morelli et al., 2014). The separation of the baby from caretakers does not necessarily allow for sounder sleep and greater independence (McKenna et al., 2007); these babies must self-sooth to sleep. Infants who spend more of the day alone than in contact with a caretaker become attached to material substitutes, including pacifiers and other objects (Karp, 2002). These become fetishes during the first several years of life, in some cases creating severe repercussions later on. By being carried or in contact, babies will fall asleep faster and without crying. Sometimes swaddling functions to reduce agitation, but the pocket sling remains the single most essential tool for parents. Fathers can be quite adept at carrying infants in slings, and the broad upper torsos characterizing males can bear loads for hours at a time without fatigue. Neonates and infants in nonhuman primates need constant contact to feel calm and safe, and are typically carried by the infant’s mother or, in some species, by other social group members until weaning. In many forager bands, it is typical for fathers to be engaged (Hrdy, 2009). Infants among foraging groups must be carried while adults search for dietary resources. Across foraging and small-scale societies, infants are carried or held nearly continuously for the first year of life (Morelli, 2015). Male involvement in carrying may have been essential in the evolution of protracted human infancy. For example, paternal carrying of infants could have reduced energetic stress on mothers, influencing lifetime reproductive fitness (Gettler, 2010; Bribiescas et al., 2012). Human anatomy is structured to carry infants with respect to the elevated center of mass, lordosis of the spine, and the shorter forearms relative to the upper arms (Williams et al., 2015). These anatomical traits maintain equilibrium and increases efficiency while carrying infants. To increase efficiency further, a carrying device such as a sling may have been one of the earliest tools (Falk, 2009). Slings may have been invented multiple times, and were probably created by females. The sling, like the womb, constrains much of the infant’s exterior, resulting in a calming sensation on the infant’s skin, along with feelings of safety and security signaled by an absence of discontent. Slings free one or both hands for additional manual tasks while allowing the caretaker

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Figure 4.2. Slings were likely among the earliest tools invented by ancient humans (Hrdy, 2009). These carrying devices are soothing to infants and reduce the caloric expenditure of the caretaker (Sears and Sears, 2003; Wall-Scheffler et al., 2007). This young infant fell asleep in a pocket sling as his father (the author) carried him.

to safely hold the infant (Figure 4.2). Slings would have been essential for ancient foragers in order to process resources while safely supporting an infant, and would have been particularly useful during longdistance walking.

Seventh and Eighth Weeks The second month marks a transition for infant-caretaker interaction, with the first true social smiles evident, even in blind infants (Woermann et al., 2014; Friedlmeier et al., 2015; Super and Harkness, 2015). During the seventh and eighth week, infants mimic some of their caretakers’ gestures, such as eating, smiling, and other facial movements. Infants at eight weeks are able to engage a trusted caretaker in a real dialogue, through movements rather than words; these exchanges resemble the basic tenets of everyday good-mannered conversation (Halton, 2014). The elimination communication process, if initiated earlier, begins to be more predictable if infants are regularly and consistently provided an opportunity to remove waste and never scolded for accidents (Sun and Rugolotto, 2004; Benjasuwantep and Ruangdaraganon, 2011). Infants

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urinate between twelve to twenty times a day (Brauer, 2001), and these tend to cluster in the morning hours and become reduced late in the afternoon. In Busama, a village in Papua New Guinea, mothers and others traditionally initiated infant hygiene by the third month, whereby the caretaker “grunts and strains to indicate what is wanted but is still extraordinarily gentle,” and eventually “she comes to recognize the signs and takes appropriate action” (Hogbin, 1963: 64). Infants often wake early in the morning and can effectively be soothed by carriers such as a pocket sling and by breastfeeding. According to Karp (2002), pacifiers should be limited or removed altogether during this time interval, as these tools can become fetishes that substitute for human social contact, specifically breastfeeding. Karp (2002) also believes that colic does not exist in all cultures, suggesting it is a result of a failure of the parents to respond appropriately to infant distress (Morris, 1992).

Ninth and Tenth Weeks During the ninth and tenth weeks, infants coo and smile when well rested. Sling carrying becomes increasingly important as a soothing device during this period. The rhythm of human walking and/or dancing can lull infants to calmness, rest, and sleep. Combining songs with the moment further assuages the distress of infants by increasing their sensory organ recognition of caretaker proximity. Infants continue to sleep a minimum of ten to fourteen hours per day, at least for babies breastfed on demand. Increased social signaling is present toward the end of the third postnatal month. Infants may begin to increase drooling in anticipation of the emergence of the deciduous dentition (or “milk” teeth), beginning with the incisors, which erupt at around six postnatal months.

Eleventh and Twelfth Weeks During the eleventh and twelfth weeks, infant bodies become stronger, and they can begin to hold up their heads with increasing efficiency. Infants at this age begin to enjoy grabbing games, wherein they can repeatedly grab and let go of a trusted caretaker’s hand or object corresponding to the increased coordination of the grasping reflex (Morris, 1992). Infants are often able to locate their own hands, demonstrating a maturation of the motor cortex. They may start to place their hands in their mouths as a way to self-soothe or explore.

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Thirteenth and Fourteenth Weeks During the thirteenth and fourteenth weeks, real changes occur corresponding to the end of the “fourth trimester.” Infants are increasingly social and “talk” while making eye contact. Vocal gestures often signal happiness. Recognition is apparent as infants gaze into the eyes of their caretakers. At this point their legs have grown stronger, and often infants find their feet, which they grab with their hands at will. They also begin to direct objects toward their mouth. Infant cognition of social relationships becomes much more enhanced, and infants can be described as having “woken up.” During this stage, they are able to turn over from a ventral to dorsal position and can elevate their heads while on their abdomens.

Fifteenth and Sixteenth Weeks During the fifteenth and sixteenth weeks, infants continue to vocalize and to be “social” with smiles and recognition (Woermann et al., 2014). The sleeping patterns from the first three months are now totally altered, with more wakefulness and shorter time intervals for sleeping, particularly at night. Infants can often reach their feet to their mouths at this age. They become more humanlike after the “fourth trimester” (Karp, 2002). Also during this time, infant tooth buds start to form a hardened area just below the gums.

Movement Potential beyond the “Fourth Trimester” During the fourth postnatal month, infants further their social cognition into new domains of knowledge, including the recognition of caregivers and increased dyadic social interactions. Negative emotional states are accompanied by appropriate facial expressions by five months cross-culturally (Fitneva and Matsui, 2015). This control of the facial musculature is coincidental with a new mastery of the limbs, which strengthen during the fourth to sixth months. Infants of this time interval can learn how to be pulled up using their hands from a prone to a sitting position. Infants more consistently direct their extremities to their mouths at this time, signaling increased neurological control of the limbs. The neck and back (epaxial) musculature along the spine becomes increasingly strong during this period to support vertical postures and the weight of the head. Independently holding up the head is mastered between two weeks and three months postnatal, depending on the amount of time the infant is carried. By the fourth month, infants

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have sufficient control over their necks to alter their head position independently. During the first six postnatal months, the neural arches enclosing the spinal cord begin to fuse to the vertebral bodies, further anchoring these muscle attachment sites. Muscles of the neck, including the sternocleidomastoid muscles (which attach from the lower temporal bone to where the clavicle or collar bone meets the sternum, or breast bone), begin to strengthen, as does the nuchal (neck) musculature that links the lower back of the head (occipital bone) to the scapula (shoulder bone) and neck vertebrae. The neck musculature of infants is recruited and strengthened when placed in a vertical posture while being carried.

Fourth to Sixth Months: Rolling Over Infants increase limb strength and back stability during the fourth to sixth postnatal months. Rolling over from the stomach to the back, then from back to stomach, precedes crawling. In rolling from the stomach to the back, infants position the thigh as a fulcrum to leverage the transverse and horizontal abdominal muscles while the arms lift the body upward. Once the infant’s body is transverse with respect to the underlying substrate, gravity does the rest. To roll from the back to the stomach, the infant can no longer rely on the legs and arms to prop the body into a transverse position, so the abdominal musculature must be adequately developed to master supine (up) to prone (down) rotation. The gravitational pull from the weight of the arms and legs positioned over the transverse plane of the body are used to help infants roll from back to front. This level of movement is often followed by the ability to fully recruit the longitudinal abdominal muscles to move the body from lying to sitting. The vertical postures of infants (e.g., when they are carried in slings or in caregivers’ arms) generate the recruitment of the back stabilizers and abdominal musculature. Moving from a lying to a sitting position is often mastered between four and six postnatal months and thereafter. The stabilizers of the lower back, from the upper pelvic rim to the lower segment of the rib cage, must strengthen considerably, and neurological control of the musculoskeletal system must also mature for infants to sit up with their back positioned vertically. The erectors and stabilizers of the waist are important to develop, because this portion of the trunk lacks substantial bony elements. The infant must simultaneously balance the forward and backward momentum of its weight under the influence

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of gravity. Infants normally bob slightly from front to back when first mastering sitting postures, reflecting the developing sense of balance that will be utilized later during bipedal locomotion at the end of the first postnatal year. Directed actions, such as finding the hands and feet with intent, occur during this interval. Oral stimulation is also pronounced. The lips and musculature of the tongue and face are relatively well developed compared to the appendicular skeleton. Although olfactory cues must also make obvious impressions on infants, and stem from the extreme antiquity of the organs of smell, the tactile and visual systems are the primary sense organs in young primates.

Seventh to Ninth Months: Crawling Crawling often begins during the seventh or eighth postnatal month (Campos et al., 2000), but can occur much later depending on the infant, the parents, and cultural norms. For example, in habitats such as tropical rain forests, where parasites and predators abound, forager parents discourage independent movement, such as crawling or walking, until the infant is well past the first postnatal year (Hill and Hurtado, 1996; Tracer, 2009). Among the !Kung who live in a dry savanna, walking is encouraged very early, and independent movement occurs at around six months. In Western-style societies where independence is highly valued, infants are given every opportunity to crawl and walk on their own. The consequence is often a rapid progression of crawling to walking while holding on, and then to independent bipedal locomotion between nine months and the end of the first postnatal year. The arm and leg muscles must be adequately strengthened for effective crawling to take place. Often infants attempt to strengthen and stretch the flexors and extensors of the thigh by rocking front to back on their hands and knees. The limb bones themselves are calcifying during the first postnatal year, and the added rigidity helps form a substrate upon which the limb muscles can pull. Crawling may never occur, or may be preceded by movement resembling those of adults scaling up a steep incline using all four limbs. Some infants begin their movements by rolling or by “walking” on hands and feet (as opposed to the hands and knees). There are a number of variations available, but clearly the desire to move occurs if infants are left on a floor for extended periods of time. Carrying infants can facilitate movement potential. In-arms or sling transport of infants positions their bodies vertically, thereby strengthening the shoulder

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and neck musculature. Meanwhile, infants are also able to assimilate, process, and organize information about their surroundings when they are content (i.e., not crying) in a carrying position (Karp, 2002). Both males and females have adaptations that enhance infant carrying. Females have a shorter forearm with respect to the upper arm and have increased lordosis of the spine. Males often exhibit greater upper body strength and larger shoulder articulations than females for increased weight-bearing potential. Broad shoulders in males help position an infant directly alongside the trunk. The somewhat narrowed pelvis restricts the ricocheting swing typical of females. When a caretaker holds an infant in his or her arms, the epaxial muscles of the caretaker’s back are recruited, while the back arches to increase the curvature, or lordosis, of the spine. While prolonged lordosis may generate some back discomfort, switching the infant from the right to left arm, and back again, alters the distribution of weight, temporally relieving the side from which the infant was previously placed.

Social Interaction The crawling, and later walking, that begins between six months and a year changes the dynamics of infant-caretaker relations (Campos et al., 2000). While carrying behavior continues, independent locomotion gradually becomes more dominant. Evidence from the ethnographic record argues that the proximity of fathers helps increase the interaction of infants with social relations outside the domestic sphere when infants are carried. Book reading or storytelling provide the basis for future language acquisition and for bonding between father-infant pairs through proximity and social recognition. Activities such as reading stories require joint attention and prove valuable tools for learning language (Fitneva and Matsui, 2015). The precocious use of gestures precedes spoken language. Hand signals for waving, and gestures used to symbolize “eat,” “drink,” “nurse,” “sleep,” “bath,” “more,” “all done,” among others, can be learned toward the end of the first postnatal year. Although infants are unable to utilize spoken communication until nearly two years, other ways of communicating social interest, wants, and needs can be learned. The social world of primates is based on proximity, social recognition, and dyadic interactions. Infants are able to participate in all of these, except controlling to whom they are proximate. Available caregivers can take an active role in initiating proximity.

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Tenth to Eleventh Months During the interval between ten and eleven months, infants change dramatically. Infants are able to negotiate horizontal substrates at different levels—for example, climbing down from an elevated surface feet first. Infants also begin to communicate to caregivers using hand gestures. One of the first to arise is the pick-me-up signal consisting of balancing on the hind legs and positioning the arms above the head, often occurring after the infant crawls directly to the legs of the caregiver. Another important gesture is waving, which occurs during this time interval (Tomasello and Camaioni, 1997). Words may occur too, including (in English) “mmm” indicating taste and “ma,” “da,” and “hi.” Consonants such as the sounds for “b,” “p,” “f,” and “g” can also be articulated. Infants can begin to stand unassisted and voluntarily from one to five seconds, and some may “dance” by swaying from side to side when music or singing is heard.

Infant Hygiene If fathers are proximate, they must invariably contend with infant elimination. Fathers provide an important contribution to the care of infants of this age in some but certainly not all foraging and small-scale societies (Kramer, 2010). Carrying infants for extended periods necessitates observing cues and making predictions about when the infants will urinate and defecate. Communicating with infants about their elimination needs can occur by providing infants with multiple opportunities to relieve themselves (Rugolotto et al., 2008; Benjasuwantep and Ruangdaraganon, 2011). Often these urination episodes will bring forth a complete emptying of the bowels. These opportunities for elimination involve simply holding the infant over a bucket, toilet, or other device, and making a noise that resembles urination (Sun and Rugolotto, 2004). Using a signal to cue them causes a parasympathetic reaction to occur that becomes increasingly associated with the release of the bowels—particularly urination. Infants who are accustomed to being given opportunities to urinate may signal when they wish to eliminate. Having infants in clothes that can be easily and quickly removed facilitates elimination communication (Bauer, 2003). Western-style parents often repress elimination communication in favor of indicators that show the child between two and three years is ready for toilet training. After years of neglecting their bodily functions, children have learned to ignore their own urination or defecation. During the past sixty years, there has been a steady increase in

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the acceptable age of urinary control due to the increasingly culturally sanctioned and widespread use of disposable diapers (Bakker and Wyndaele, 2000). Most infants in the world must learn how to control their elimination during early postnatal development, because teaching them to ignore their bodily functions is unaffordable or undesirable. For example, in Thailand, most infants are trained to use the toilet by one year (Benjasuwantep and Ruangdaraganon, 2011). Furthermore, elimination is an important avenue of communication that can occur between infants and caretakers, long before language is available. Elimination communication can begin from the first week, although the communication can be disrupted at around the time infants begin crawling. Infants who are between eighteen and twenty months can be readily trained to eliminate in designated locations when allowed to be diaper-free and when given positive, nonpunitive encouragement. For instance, among the Bangangté of Cameroon, children were traditionally taught to “perform their natural functions” at specified locations beginning at “about eighteen months” (Egerton, 1939: 238). Among the Busama of Papua New Guinea, an infant can move independently “with reasonable assurance and to some extent feed itself, at an age of from eighteen to twenty months” (Hogbin, 1963: 62), and “parents expect that a two-year-old child will have his bowels and bladder under control, at least during the daytime” (Hogbin, 1963: 64). However, “training begins much earlier, in about the third month, when the mother makes a practice of holding the infant out as soon as it wakes in the early morning” (Hogbin, 1963: 64). Positive reactions and receptivity to signals increase willingness to communicate about elimination, whereas negative reactions and neglect thwart the acquisition of urine and bowel control. Trusting infants’ ability to learn patterns of human behavior and accepting those moments when infants fail to adhere to the norms of society, without reaction, are the basis of early elimination communication (Bakker and Wyndaele, 2000). Once infants can remove their own clothes (at around seventeen to nineteen postnatal months), they are able to take care of their own needs, albeit with continued assistance, encouragement, mutual understanding, and reinforcement. Morris (1992) disagrees and suggests that infants cannot be trained earlier than language acquisition occurs. However, empirical evidence from around the world suggests otherwise (Rugolotto et al., 2008; Benjasuwantep and Ruangdaraganon, 2011). Even without early communication about elimination, bladder and bowel control can be inculcated between 1.5 to 2 years, albeit with

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occasional accidents. Incidentally, infants between 1.7 and 2 years of age are often able to run, signifying a different method of locomotion than walking and greater motor control of the lower limbs. Cloth diapers allow infants to use their sense of touch to notice that they have urinated, which aids in the recognition of elimination needs. Before disposable diapers became widely available in the early 1970s, babies who were cloth-diapered normally learned how to control their elimination by the first or second birthday (Mead, 1955; Bakker and Wyndaele, 2000), because it is at this time that infants master the coordination to partially undress. Underwear worn by infants naturally facilitates the process of independent elimination because they are easier to remove than diapers. Infants of this age need to urinate about as often as their caretakers do, and so can be prompted socially as they begin to identify their basic needs.

Language The word baby derives from an Old English form of babble, whereas infant originates from Latin—in meaning without and fant referring to speech (Lamb et al., 2002). Language acquisition begins gradually between the first and second year of infancy and replaces or augments hand gestures. The similarity in timing of language acquisition cross-culturally suggests a universal grammar is embedded within the genetic code of humans, comprising an intrinsic ability to impose or internalize syntax on human communication systems (Chomsky, 1965). Although language is learned by infants during the first two years, it is acquired according to cultural norms. For instance, English speakers emphasize personhood, whereas other cultures, such as Western Samoa and the Kaluli of New Guinea, do not address infants directly until after language is acquired, as they are not considered conversational partners (Ochs and Schieffelin, 1984). Among English speakers, spoken language occurs first with nouns and isolated verbs, and later by phrases. Imperative declarations precede questions. These examples illustrate that children learn the language of their culture by different routes, such as active teaching, passive instruction, or some combination of the two. Shortly after two years of age, when the brain is approximately 80 percent of adult values, real language begins with grammar, syntax, direct/indirect object use, substitution with pronouns, memory, mastering of abstract concepts (e.g., pretend worlds), and independent thought processes. Counting occurs much later than language use.

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Language Use during the First Year Incipient language development begins early during the first year, signified by utterances that vary in pitch and intensity as a reflection of social and emotional mental states. This early development of communication heralds more humanlike symbolic signaling established later (Halton, 2014). Between four and six months, infants discover their tongues, as demonstrated by the positioning of the tongue between the lips repeatedly with muscle flexion. Between six months to one year, social recognition of caregivers includes reciprocal patting and reaching out of arms at the approach of caregivers (Campos et al., 2000). Approximation of caregiver names also occurs during the second six months of life, and includes mama, dada, and older sibling names. At nine months, infants are able to discriminate phonetic contrasts in their own language (Kuhl et al., 1992). They are also able to identify phonetic contrasts when foreign language instruction is repeated multiple times over a month, if learned from a social actor rather than a virtual representation of a person (Kuhl et al., 1992). Apparently, infants can only learn language within a truly social context (Kuhl, 2007).

Twelve to Eighteen Months Around one year, sometimes a bit before, or after, infants begin pointing to objects (Tomasello and Camaioni, 1997), waving, clapping, and hiding. They also follow the gaze and pointing of social actors at this age (Fitneva and Matsui, 2015). Interestingly, the names of caregivers become more refined. For example, “dada” becomes “daddy” as infants learn the use of the diminutive-affectionate form of “father.” Infants can be taught by imitation to click their tongues against the roof of the mouth at around one year of age. This ancient human phoneme is preserved in several indigenous languages, such as Xhosa. Listening carefully to interpret and validate the developing speech patterns of infants can enhance their emerging ability to approximate sound symbols and convey meaning. The auditory environment to which infants are exposed directs their vocal recognition and usage. In this regard, repetition and reading books aloud to infants greatly enhances infant comprehension and vocabulary. Repeatedly reading a book or recounting a story builds a scaffold whereby different parts of the story are gradually understood. Book reading also allows for words to be explained and ideas to be introduced (Fitneva and Matsui, 2015). Metaphorically, reading aloud or storytelling is akin to a vessel being filled before it can be poured. Book reading, like active engagement in a

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game or a puzzle, communicates mutual interest (Fitneva and Matsui, 2015). Asking infants to point out animals or objects in a book rapidly engages them with the story. When infants learn to recognize words and ideas, their brain language centers are stimulated. These activities also enhance their social and emotional stability and intellectual potential. Infants begin pointing to themselves at about 15 to 16 months, followed by an indication for the direction that the infant wants to be taken. Directional pointing is something also present in ape infants raised with human caregivers (Savage-Rumbaugh and Lewin, 1996). However, in human infants, pointing becomes increasingly accompanied by vocalizations. Real words begin from nine months to three years, but most individuals begin articulating words, or at least the first phoneme of the word, between twelve and eighteen months. Between about sixteen and nineteen months, sometimes earlier and sometimes later, infants begin to formulate well-formed words and distinct sounds by themselves. The sounds of animals seem to be some of the earliest distinctions that infants can mimic. Question-and-answer routines strengthen skills of communication early on. For example, when asked what a cow says, the infant can respond “moo.”

Eighteen Months to Two Years Between 1.5 to 2 years, infants begin combining single words into twoor three-word phrases (Fitneva and Matsui, 2016). These protosentences may incorporate subjects and predicates, but far more nouns are used than verbs, at least in English, which can be described as a referential, rather than expressive, language (Fitneva and Matsui, 2015). Contractions, such as “and,” occur much later. The mental pictures for objects and people are now formed, such that infants may be able to recognize abstractly that the word for “squirrel” applies to all squirrels. By eighteen months, infants are able to decipher meaning from speech directed toward them and others, suggesting they can acquire vocabulary using multiple methods (Fitneva and Matsui, 2015). Closer to the end of the second postnatal year, infant language use continues to sharpen with the formation of two-word sentences, such as “Here daddy!” Combinations of word phrases become regular occurrences, forming the basis of conversation skills. Language and vocabulary acquisition, regardless of modes of learning (active or passive, formal and informal), occurs cross-culturally within a social environment (Fitneva and Matsui, 2015). Incipient critical thinking

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arises when infants at this age can apply their memorized responses to novel situations correctly. Infants increasingly develop recognizable phonemes, or significant sounds within a language, which improves understanding. Infants often experiment with unusual combinations of phonemes, almost as if testing the language speaker to see if just any assemblage of language sounds can be understood. They may learn sequences of phonemes that they know are nonsense phrases, and this continues throughout the third postnatal year. It is in this way that infants begin to understand the difference between real and pretend— things that exist in this world and things that do not. The comprehension of words far outstrips language production during this age. Infants prior to two years are able to play the “yes-no” game, whereby participants nod “yes” followed by “no” with the sequence alternating. Infants of this age are not yet able to form questions, but they become adept at indicating possession using language. Interestingly, as the rules of grammar are internalized, they are applied to novel situations, such as when an infant uses “my’s” rather than “mine,” as the possessive first-person pronoun in English, which is irregular. It is at this time that infants can begin to memorize lists, such as counting numbers from one to ten and the alphabet, with varying degrees of success. Before the age of two years, infants begin to recognize the difference between exact and approximate, as shown by phrases that help differentiate location, such as the use of “right there.” Puzzles show that infants of this age are able to understand directional cues from caretakers, further demonstrating their knowledge of approximate and exact values. Infants prior to their second year of life are often able to sing, following the rhythms of known songs. They also begin constructing complete sentences. These complete thoughts can express preferences, such as “I like beans,” or greetings, such as “nice to meet you.” Sentence development is enhanced by multiple daily reading intervals of at least twenty minutes. Reading embodies the act of telling stories and mimics primate sociality through affiliative proximity. Furthermore, reading increases infant understanding of social knowledge and cultural norms. The time interval, 1.7 to 2 postnatal years, witnesses the development of the inquisitive—in other words, asking questions. By two years old, infants understand indirect commands and requests across cultures (Fitneva and Matsui, 2015). Initial questions, at least in English, are

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introduced with a rise in pitch at the end of a sentence, whereby “Do you want more?” is simplified with “More?” As the inquisitive is further mastered, infants begin to add verbs, such that “More?” becomes “Want more?”

Two to 2.5 Years: Language Explosion Between age 2 and 2.5 years, the language capabilities of infants experience a tremendous advance alongside basic changes in abstract thought (Fitneva and Matsui, 2015). The conversational abilities of humans at this age progress substantially over a period of about three months, initiated approximately six weeks to three months after the second birthday. Infants begin to utilize language as an instrument of culture rather than simply grammar, syntax, and vocabulary (Fitneva and Matsui, 2015). Parallel with conversational abilities, infants may mimic the play behavior they experience with their caretakers with their own dolls, showing imitation—the basis of human language acquisition. Infants who previously used only partial words begin to place consonants at the ends of words, such that “ya” becomes “yes” and “plea” becomes “please.”

Two and a Half to Three Years Carrying infants during the first 2.5 to 3 years of life allows them to examine adult social behavior. In this way, infants learn valuable social skills, along with the daily tasks that adults do, such as preparing dinner, cleaning, interacting with others, gathering and distributing resources, and other seemingly mundane chores. Before the third birthday, infants are able to communicate complex ideas with grammar rules intact and to master intricate movements with the hands and feet. The need for infant carrying diminishes as infants reach 2.5 years, or when the inclination to be independent takes hold. At around 2.5 years of age, a transition occurs in the self-perception of infants who before may have referred to themselves as babies; after 2.5 years, or thereabout, these same individuals often refer to themselves as children. This time period also corresponds to weaning in many traditional societies (Bogin, 2006).

Discipline Disciplining infants is rare when they are closely proximal to their mothers and, in many cases, fathers, as well as grandparents and older siblings during most of the day. For example, Pacific Islanders in a

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New Zealand study suggested that fathers only rarely disciplined their one-year-old infants (Iusitini et al., 2011). Similarly, among the Arunta, Aboriginal foragers of central Australia, “all children are treated with exceptional kindness and affection and an extraordinary amount of consideration, and only very rarely, and upon the greatest provocation, are they chastised physically” (Montagu, 1974: 23). When infants are frequently left alone, they attempt to attract the attention of caretakers by behaving in socially unacceptable ways. Historically and cross-culturally, corporal punishment was employed to contain such outbursts. More recently, a “time-out” has gained prominence. These forced separations do little to alleviate the source of the problem. It may be that the infant perceives a lack of interest from the caretaker, which exacerbates feelings of frustration and social isolation. In contrast, a “time-in” following Sears and Sears (2003) repairs the negative feelings that produce the motivation for behaviors that are intended to disrupt normal social interaction. By being proximal, caretakers are able to demonstrate their interest and remove, at least momentarily, feelings of insecurity that may arise in infants who are left alone. Sears and Sears (2003) also advocate that it is better for an infant to cry in a caregiver’s arms than to cry alone. They propose that letting an infant “cry it out” destroys their self-confidence by denying them validation for their emotional distress. Although they may not remember, this emotional stress may play key roles in the development of antisociality, chemical dependence, self-destructive behaviors, and a range of social pathologies (Lamb, 1997). Isolation is the most extreme form of punishment for social animals, such as humans and nonhuman primates. The effects of isolation during development have been explored by comparative psychologists using infant deprivation experiments involving mother-infant separation among macaques and other nonhuman primates, resulting in psychosocial/emotional/ sexual pathologies in adulthood, combined with an excessive attachment to peers, and a lack of play and exploratory behavior (Jolly, 1985; McKenna, 2014). Human infants and young children who are chronically neglected, or abused, by caregivers tend to exhibit less pretend play, more antisocial behavior, and poor interaction abilities (Valentino et al., 2014). In contrast, devoting too much attention to infants has never been shown to be detrimental. For example, in Bali, Indonesia, infants are not permitted to touch the ground until six months of age, and are carried continuously until one to two years of age. In this culture, parents

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and others demonstrate interest in infants through proximity and direct care (Mead, 1955). The same can be said for a variety of small-scale cultures around the world, and particularly foragers (Hewlett, 1991).

Growth in Height Growth in height continues in a similar fashion in male and female infants, although males may be larger at birth and are often slightly larger at every age thereafter. At one year, infants have reached about 42 percent of their adult height (Figure 4.3). Males and females achieve 50 percent of adult height at about 2.5 and 2.3 years, respectively. The rate of increase slows during early childhood (Bogin, 1999) but increases substantially by ten years of age in girls and twelve years of age in boys. Adult height is attained earlier in females, usually by sixteen or seventeen years. Whereas most of male growth in stature is completed by eighteen years, some males grow for two to three years thereafter (Figure 4.3).

Figure 4.3. Percentage of adult height attained as a function of age. Data from Sinclair and Dangerfield (1998), from a longitudinal study of three hundred healthy children by N. Bayley (1956), Growth curves of height and weight by age for boys and girls, scaled according to physical maturity, Journal of Pediatrics 48:187–94.

5 Reproductive Careers among Forager Males

Human life histories are slow compared to those of the great apes. This elongated maturation may be simply a consequence of selection for longevity, a prediction of the grandmother hypothesis. Alternatively, longevity can be explained by selection for time to learn skills related to hunting prowess and extractive foraging, which effectively reach their peak between thirty-five and forty-two years in foraging societies. Even among herder-agriculturalists in East Africa, such as the Gogo in Tanzania, males did not traditionally achieve “elderhood” until thirty-five years and older (Rigby, 1969), and historical anecdotes from early nineteenth century France suggest men approached forty years before they married (e.g., Steegmuller, 1959). The reproductive life history of males may be reflected in peak skeletal health beyond maturation but before decline. The Ache, along with two other hunter-gatherer societies (!Kung and Hadza), are among the few for which reliable demographic data exist, and those from the Ache are the most comprehensive. Estimated ages of first and last “birth” in Ache forager males are twenty-four and forty-eight years, respectively. The age of greatest political power in Ache males is thirty-five to fifty-five years. Ages of peak hunting among these three forager societies is thirty-five to forty-two years. Similarly, Gidra hunters of Papua New Guinea exhibit peak rates of prey capture between thirty-five and forty-five years (Ohtsuka, 1989). Forager adult males are able to produce more than they consume between nineteen and fifty-nine years. Forager males have their highest reproductive output between the ages of thirty-five and forty-five years. This allows adult males to provision several socially recognized weaned dependents until they too can produce more than they consume. This surplus

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affects the interbirth interval of males and the effectiveness of males as caretakers of infants.

Life History Theory Adolph Schultz (1924) was the first to describe the progressive tendency in the order Primates toward a lengthening of gestation, infancy, the juvenile period, subadulthood, and adulthood. Schultz (1969) showed that the life-cycle stages found in humans are the same ones seen in nonhuman primates, only elongated. However, gestation is similar across the great apes and humans, and relatively long in primates compared to similarly sized mammals. In humans, an extended life cycle with respect to those in apes occurred because cohesive social groups were available to care for nonadults over an extended period of time. Human longevity may simply be a consequence of stretching of life history profiles, or perhaps the ability to live to an old age was a target of selection. Longevity in humans is clearly related to slower rates of aging compared to those characterizing our closest relatives (Robson et al., 2006). What does this elongated human life cycle mean? In humans, skeletal and dental maturation occur over nearly two decades. In most mammals, eruption of the first permanent molar signifies weaning. In humans, the first molar erupts at about six years of age. Once most mammals, but not primates, are weaned, they enter puberty and then adulthood. This is not the case in humans, who exhibit a long juvenile and subadult period of about six years each. In apes, skeletal and dental maturation is largely complete by eleven to twelve years, and in Old World monkeys, such as baboons, maturation occurs at about six years (Table 5.1). In all of these primates, males take about two years longer than females to mature. The dental stages that demarcate major life history events, such as weaning, puberty, and adulthood, correspond to the eruption of the first, second, and third molars of Old World monkeys, apes, and humans. What differs is that humans exhibit a longer time period in each of the stages, as well as the possible addition of a childhood stage from three to seven years of age, between weaning and the juvenile period, characterized by slow somatic growth but enhanced cerebral development (Bogin, 1999, 2006). Human children are not able to survive without immediate caregivers until they are older than seven years of age. Myths of feral or street children younger than seven years remain unsubstantiated (Bogin, 2006). Weaned but completely dependent three- to seven-year-olds

5.8–6.4 b

3.2–3.4 b

1.5 k

0.74 b

0.62 b

0.54 j

Humans

Chimpanzees

Baboons

2.5–3 k

4–6 h

9–15 c

Juvenile M2

4–6.5 k

10.3–11.4 b

19.8–20.5 b

Subadult M3

25–30 l

53.4 b

1.2–3.3 j

5–6 i

13.7 i 4–7 j

5.46 b

13.3 b

11g

72 f

3.69 b

Inter-birth interval

3–4 e

19.5 b

Female first birth

43–53 d

85 b

Life span

eruption times for the first (M1), second (M2), and third (M3) molars correspond to the end of the infant, juvenile, and subadult categories, respectively. The ages in the life span column are highly variable. b Robson et al. (2006), c Steele and Bramblett (1988), d Gurven et al. (2017); e Konner (2016); f Hrdy (2009); g Wells and Stock (2007); h Dean and Wood (1981); i Stumpf (2011); j Swedell (2011); k Bramblett (1969); l Fedigan and Pavelka (2011).

a Dental

Infant M1

Gestation

Table 5.1. Human, chimpanzee, and baboon life history and molar (M) eruption comparison in yearsa

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must be provisioned daily and given shelter or protected, as children, unlike adults, can only live for a week without food (Hill and Hurtado, 2009). Similarly, ape infants cannot survive without their mothers until weaning, which occurs at about 2.8 years in gorillas, around 4.5 years in chimpanzees, and up to 8 years in orangutans (Robson et al., 2006). Humans tend to wean earlier than chimpanzees and orangutans do, with a cross-cultural average of 36 months (Bogin, 2006). But thereafter, these weaned infants require a heavy caloric load to support the growth and maintenance of a large brain (Hill and Hurtado, 2009). After weaning, nonhuman primates survive much more frequently if other social members are present, such as older siblings or familiar nonkin. The same is certainly true of humans.

Life History in Comparative Perspective The life history of humans differs from those of apes in three important ways. Humans have a relatively long post-reproductive life, a later age at first birth (females), and a shorter interbirth interval. This means that human mothers can have several weaned dependents to provision, even when she is no longer reproducing herself. Slower rates of aging in humans compared to those of the great apes may at least partially account for the extended life histories of humans. In the wild, chimpanzees can live to about forty-five years, while orangutans die before fifty years. The maximum life-span of any great ape recorded is sixty years. Among humans, the oldest known savanna forager is eighty-eight years, while the oldest documented forest forager is seventy-seven years (Hawkes et al., 1998). The oldest human recorded is 122 years (Robson et al., 2006). Modern human lifetimes are at least several decades longer than those characterizing the common ancestor of apes and humans. Life expectancies also differ between the great apes and humans. For example, the life expectancy in chimpanzees at fifteen years is thirty to thirty-five years, whereas in human foragers at fifteen years, it is at least forty-five years, or nearly double. A longer life-span is influenced by lower mortality rates. Mortality rates increase greatly in apes during the fourth decade. Chimpanzees older than thirty to thirty-five years in the wild are visibly weaker and thinner than their younger counterparts (Goodall, 1986; Finch and Stanford, 2004; Robson et al., 2006), whereas in human foragers, the muscular system declines much more slowly (Walker and Hill, 2003). Age at first birth also differs between apes and humans. In wild chimpanzees, age at first birth for females is thirteen years, while in

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bonobos it is fourteen years. Orangutans at fifteen years have the latest age at first birth for the great apes, whereas gorillas at ten years, both in the wild and nearly so in captivity, exhibit the earliest age at first birth (Robson et al., 2006). The mean age at first birth for human foragers is about 19.5 years, which is not very different from the mean age at first birth, about 19 years, calculated from cross-cultural studies (Bogin, 2006). Historical records for humans in industrialized societies indicate age at first birth was most often early or midtwenties. The age at first birth in males, who mature later and achieve larger adult sizes, may be later than those of females. Ache males rarely become socially recognized fathers before 20.5 years, with a median age of about 5 years later than first birth in Ache females at 19 years (Hill and Hurtado, 1996). These reproductive histories are comparable to those characterizing urban populations in New Mexico, where median ages of first reproduction in males ranged from 24 to 31.7 years over the twentieth century (Lancaster and Kaplan, 2000). Human mothers wean their infants earlier than the great apes, such that several weaned dependents must be provisioned with high-quality protein to support a large encephalized brain until these dependents are about eighteen years. No one argues that an auxiliary food source must have been available for an extended maturation to evolve in humans. However, who did the provisioning is currently under scrutiny.

Provisioning by Grandmothers, Fathers, or Others? Grandmothers, particularly maternal ones, have been observed among the Hadza, participating extensively in provisioning activities (Hawkes, 2006), but in most foragers, including the Hadza, it is the males that provide the extra protein-rich calories that are needed to grow and maintain others, such as children and their mothers (Kaplan et al., 2000). The grandmother hypothesis is based on Charnov’s equation, which divides an organism’s allocation of energy into present and future reproduction parameters (Hawkes et al., 1998; Blurton Jones and Marlowe, 2002) and was tested on observations of Hadza social groups and others. Kristen Hawkes (2006) concludes that longevity (or survival) was advantageous because postmenopausal women, while not reproducing themselves, could nonetheless devote their energy to provisioning dependents. Among the Hadza, children in households with grandmothers are healthier and have better chances of survival than those without. Observations among the Tsimane, a small-scale forager/farmer society, do suggest intergenerational transfers of resources that are particularly

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important during infancy (Gurven et al., 2017). However, among the Ache and Hiwi foragers of South America, post-reproductive females are not numerous and contribute less to provisioning kin compared to younger males (Hill and Hurtado, 2009). Furthermore, if two-parent families are the social glue of mobile foragers, then it might be expected that fathers engage in provisioning more consistently than grandmothers. Father care could have provided a strong proximate motivation for hunters. However, father care may not be the only motivation for hunting by males. Showing off hunted returns would be a costly but honest signal of male vigor, and could have been an important motivator to secure game (Hawkes and Bliege Bird, 2002). A dietary shift that involved a heavy reliance on meat protein allowed for an increase in the size of the brain, an expensive tissue to grow and maintain (Aiello and Wheeler, 1994; Leonard et al., 2007). Kaplan et al. (2000) suggest that regular hunting increased the availability of large animal protein well above consumption levels. However, mastering the skills to regularly obtain high-density food packages, from hunting and extracting resources, reaches a peak at thirty-five years. This delay in mastering foraging techniques could have also selected for longevity following Charnov’s model, because males invest in future reproductive efforts by acquiring skills, ten to fifteen years after skeletal maturation, that are necessary to adequately provision dependents. By delaying age at first “birth,” both males and females learned survival skills as embodied capital for later reproduction (Lancaster and Kaplan, 2000). These skills could be passed on to descendants once they reached late subadulthood, as among Ache fathers and sons (Kaplan and Robson, 2002). Hawkes and colleagues suggest that grandmothers provided the calories needed to provision dependents because male hunting was unreliable and, if obtained, distributed equitably. Production generated by grandmothers, however, primarily from root extraction, benefits only close lineal relatives, and therefore initiated selection for postmenopausal longevity. However, with respect to hunting, mortality rates fall when high-quality protein is consistently available, even when individuals are sick or injured. Large packages of protein-rich dietary staples would increase the potential of individuals to ward off infection and heal (Kaplan et al., 2000). In several societies, women also hunt (Endicott, 1992) or participate in net hunts with the men (Hewlett, 1991), suggesting embodied capital is not necessarily tied to one sex.

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Paleodemographic evidence suggests that consistent longevity beyond fifty years is a recent evolutionary phenomenon, although epidemic disease outbreaks during the past ten thousand years of food production may have reduced human life expectancy as well (Paine, 2006). After forty-nine years, the skeleton declines more markedly, which agrees with reports of Ache male hunting abilities decreasing after fifty years (Hill and Hurtado, 1996); grandparents would have to consistently live more than a decade longer than fathers to positively influence the survivorship of descendants. The biological contribution of males to infants is absolutely essential, and the pair-bonded twoparent family is more common among foragers than multigenerational units of subsistence. Human female foragers end reproduction between thirty-seven and forty-two years (Kaplan et al., 2000), although among the Ache, females often exhibit a later peak of fertility, between thirty to thirty-five years, and remain fertile longer than !Kung and Yanomamö women (Hill and Hurtado, 1996). Male life histories may approximate those of females, with two important exceptions. First, males have greater variability of reproductive success than females. Second, males reproduce later than females and remain fertile for longer (Bribiescas et al., 2002), perhaps reflected in the maturation and decline of the skeleton.

Estimating the Length of Male Reproductive Careers Peak rates of food production also coincide with optimal skeletal health. The contribution of males in foraging societies ranges between 25 percent and 100 percent (Marlowe, 2001). In seven out of ten foraging societies, males supplied between 60 and 84 percent of the daily caloric needs, while in the other three, males and females contributed more or less equally (Kaplan et al., 2000). The skills needed to be successful hunters include an intimate understanding of animal behavior, shifting climate conditions, and tracking more than aim. Males continue providing more calories than they consume until the end of their sixth decade, and provide four thousand to more than eight thousand calories per day (Figure 5.1), depending on the foraging society, during peak production years (Kaplan et al., 2000). Among Efe foragers, children are calorie-dependent on their parent until they reach early adulthood (Morelli et al., 2014). The same is true of Ache foragers, where subadults need to be provisioned until they are fifteen to nineteen years, when production starts to equal consumption. The last “birth” for males would be predicted to be about forty

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Figure 5.1. Male foragers produce more than they consume between the ages of nineteen and fifty-nine years. Most of these excess calories are from hunting. Forager male calories obtained per day are averages of the daily caloric production of Hiwi, Ache, and Hadza males. Age point estimates were averaged. Since data for Hadza males younger than twenty and older than sixty years were unavailable, younger and older average ages from Hiwi and Ache were used. Calories consumed per day by foragers are averages and interpolated using spline regression. The data are from Kaplan et al. (2000).

to forty-five years if male returns from hunting begin to diminish at fifty-nine years to provide enough time for a father, barring extrinsic mortality, to provision a developing descendant until self-sufficiency is achieved. During the fifth decade, a slow but steady degradation in the structural integrity of the skeleton is already underway, including osteoarthritis of the vertebral column and increased compression of the joint surface areas of the weight-bearing lower limbs, particularly the knees. In many forager societies, fathers engage in extensive carrying of infants. Examples include the Aka, who carry their infants between one to four hours a day (Hewlett, 1991), and the Batek, where fathers are second only to the mothers in caregiving (Endicott, 1992). Carrying behavior occurs among Agta young adult fathers (Griffin and Griffin, 1992). Forager males would be affected by the decline of the skeleton after forty-nine years, such that last “birth” would be expected to be approximately forty-six years for fathers to effectively withstand the mechanical loading of infant carrying during the first three postnatal years. It should be mentioned, however, that forager and small-scale

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agriculturalist males exhibit fertility distributions, defined by the age-specific probability of becoming a father with respect to total fertility outcomes, that are longer than those of females, such that some males continue fathering infants into the sixth (Dobe !Kung), seventh (Ache, Yanomamö, Tsimane), and eighth (Gambia) decades (Bribiescas et al., 2012; Vinicius et al., 2014). Although paternity may occur at later ages (older than fifty years) in small-scale societies to a greater extent than in industrialized countries such as Canada (Bribiescas et al., 2012), father care after fifty years may be constrained by the accelerated decline of skeletal tissues. For example, among the Batek, older fathers participated less in father care than their younger counterparts (Endicott, 1992). Comparisons of forager male life histories suggest that the age at first and last “birth” are relatively consistent, although in some societies, such as the !Kung, males start later and end earlier. Hill and Hurtado (1996) reported the median and mean age for first “birth” among Ache male foragers during the forest period (before contact was established in 1974) to be 24 years, and the mean age at last birth to be 48.1 years, with greater variability (zero to 15) in the number of children compared to those for females (7 to 8 infants). Some males never became fathers, particularly if they had not fathered an infant before 40 years. Meanwhile, political influence for males peaks from thirty-five to fifty-five years in Ache males, a time interval when some males are able to maximize their reproductive potential. Ache forager males were most likely to become fathers between twenty-five to forty-four years, with an elevated fertility between thirty-five and forty-two years, and a peak at forty years (Hill and Hurtado, 1996). Among the Ache, males and females tend to converge in total length of reproductive careers at twenty-four and twenty-three years, respectively. These life histories are reflected in age classifications of foragers. For example, among the Batek, life-cycle categories included “infant, child, female youth, male youth, parent of young children, and old person” (Endicott and Endicott, 2014: 114). The classification lacks a term for individuals not yet old without young children. By the time all the children matured into youths, the parents would indeed be old. The aging of the skeletal system is a good proxy to estimate the range of reproduction in males (Figure 5.2). Substantial age-related changes begin to occur in the skeletal system after forty-nine years, while optimal subsistence skills begin to wane after about forty-five years, thus reducing the prime years for direct father care to thirty-five to forty-five

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Figure 5.2. A comparison of minimum and maximum age estimates for father care calculated from (1) Ache forager male mean ages for first and last “birth” at twenty-four and forty-eight years, respectively, with a peak of fertility at forty years (Hill and Hurtado, 1996); (2) peak hunting years where calories generated by Ache and Hiwi males exceed six thousand and four thousand calories per day, respectively, at thirty-five to forty-two years, with an average of thirty-eight and a half years (Kaplan et al., 2000); (3) political influence peaks from thirty-five to fifty-five years in Ache males (Hill and Hurtado, 1996), with an average of forty-five years; (4) production exceeds consumption for forager males, from nineteen to fifty-nine years, with peak production at thirty-five years (Kaplan et al., 2000); and (5) skeletal adulthood in males before the onset of degeneration, twenty-five to forty-nine years, with some secondary remodeling activity at thirty-five years (Steele and Bramblett, 1988). The data are shown with a spline regression for each of the indicators.

years. This differs from the reproductive profiles for females because males reproduce for longer periods of time, but with a shorter peak that is about ten years later. Female reproduction peaks after twentyfive years, and decreases slightly between thirty to thirty-five years, then declines more rapidly between thirty-eight to forty-two years, and ends markedly, usually between forty-five to fifty years (Ellison, 2002).

Interbirth Interval One way to estimate male “birth” intervals for pair-bonded fathers is to model those of females. Among the nonhuman primates, the birth interval of apes and humans tends to be longer than those in monkeys, lemurs, and lorises. Female chimpanzees exhibit an interbirth interval of about 5.5 years, while that for bonobos is about 6 years (Stumpf,

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2011; Table 5.1). Gorillas exhibit the shortest, and orangutans the longest interbirth interval among the great apes, at 4.4 and 8 years, respectively (Robson et al., 2006). The ethnographic record suggests a great amount of variability in reproduction among males. Pair-bonded males in hunter-gatherer societies are expected to exhibit less variability in fertility than males in polygynous societies. Among societies where monogamy is often practiced, males are expected to have similar interbirth intervals as females, which is every three to four years in populations that do not control fertility (Bogin, 2006; Robson et al., 2006). Interbirth interval decreases with greater male contribution to the diet (Marlowe, 2001). Ache male foragers fathered an average of 6 to 8 live births, out of which about 2.9 survived to adulthood (Hill and Hurtado, 1996). However, a later age of marriage for males in many societies—for example, over thirty years among the Maasai and some recent Aboriginal foragers in Australia—may decrease the total number of infants fathered. With an expected age of death between fifty and fifty-five years, if a male begins mating beyond thirty years, only 5.6 infants per life cycle would be expected. Ache males who lived to sixty-five years fathered more infants, suggesting a link between reproduction and longevity. The interbirth interval for males varies more than those of females because of the multiple families of some males and the absence of any children, at least among the Ache, in about 12.5 percent of males (Hill and Hurtado, 1996).

Proximate Mechanisms of Father Care Father care likely played a key role in provisioning weaned dependents, because they had bonded with them as neonates (Gettler et al., 2011b, 2012a,b). Imprinting, or initial bonding between fathers and infants and the memory of the stimulus, could have helped initiate further paternal behaviors, including carrying of infants and maintaining the partnership of the pair-bond. The greater frequency and duration of proximate contact between fathers and infants, the stronger the social bonds between them. These bonds may have led to provisioning behaviors by males for their weaned three- to seven-year-olds and later for older children, until the requisite survival skills such as hunting, extractive foraging, and reciprocity were learned. Between three to seven years, the body grows at a slower rate (Bogin, 1999), while at the same time, the brain reaches peak levels of metabolic cost such that provisioning becomes dire (Kuzawa et al., 2014). By age seven, human children have erupted their first molars, increasing the effective chew-

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ing surface, and their permanent incisors, which allows for better processing of food. However, provisioning by males and females would have to occur until production began to outstrip consumption during late adolescence (Kaplan et al., 2000). Although older children are wellequipped to collect a variety of food items among hunter-gatherers, it is not until the late teen years that subadults are given increasingly intensive instruction from adults on complex foraging tasks such as hunting and extracting foods that are difficult to acquire (Lew-Levy et al., 2017). Correspondingly, the length of time needed to learn social and subsistence skills is around the age of eighteen years among foragers and small-scale food producers (Kaplan and Robson, 2002). Such an enormous range of variability in father-child relations cross-culturally suggests that the bonds between fathers and infants are established by familiarity rather than as a genetic trait. Preferential treatment and kin recognition are believed to be related in a linear fashion, such that the degree to which relatives can be recognized should predict the amount of preferential treatment close kin receive (Bernstein, 1999). However, humans spend nearly two decades living in social groups before they begin their reproductive careers. Familiarity may predict preferential treatment much better than recognizing genetic relatedness in a social species in which individuals take a long time to mature (Bernstein, 1999). This familiarity between fathers and infants crystallizes during early postnatal development, and is an extension of the mother-infant breastfeeding relationship, and the mother-father pair-bond (Quinlan and Quinlan, 2007). Among nonhuman primates, the social relationships between males and females is a better predictor of specific maleinfant interaction than paternity as most one-male groups exhibit little male-infant involvement (Smuts and Gubernick, 1992). Fathers who are also caretakers may not be related to their infants, although they most often are (Lancaster and Kaplan, 2000). In sum, father care is most often expressed in forager groups (Katz and Konner, 1981). The father-infant bond is adaptive because it directly increases the survival of descendants. Direct father care is a function of age, and peak male reproductive effort is estimated to be thirty-five to forty-five years. The general correspondence of age at first and last “birth” in male hunter-gatherers, as well as those living in urban neolocal two-parent families, suggests that evolutionary forces have acted on males to ensure that an extended human maturation sequence can successfully occur.

6 The Duration of Father Care Estimated from Skeletal Maturation and Decline In the absence of pregnancy and birth, the reproductive histories of males must be inferred from other indicators, such as maturation. For example, the teeth erupt slowly over the course of nearly two decades. The human skeleton takes well over twenty years to complete ossification of the growth plates (epiphyseal plates) on the long bones in males. Skeletal elements begin to degrade (barring extremes in physical labor) more rapidly after forty-nine years. From twenty-five to forty-nine years, males are in their peak skeletal health, although the variation is substantial. Skeletal indicators can be compared to other possible correlates of male fertility to approximate the length in years of father care during the life cycle.

Dental Eruption Neurological and physiological development closely correspond to the eruption of the teeth such that new mental abilities and body control occur at the onset of dental development events. Eruption of the dentition in humans follows a predictable sequence with respect to age. The deciduous dentition begins to erupt at around six months of age— initially the lower central incisors erupt followed by the upper central incisors. The lateral incisors erupt at about seven to eight months in the reverse sequence as the central ones. The sequence is often lower central, upper central, upper lateral, then lower lateral incisors (Schwartz, 2007). These eruption events occur at about the time independent movement emerges (e.g., crawling). At around a year, or between eleven and eighteen months, the deciduous first molars erupt, followed by

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the canines, which slowly emerge during the second postnatal year. These dental eruption events occur at about the time that bipedal movement is achieved. The deciduous second molar erupts toward the beginning of the third postnatal year. By 2.5 years, the deciduous dentition is usually complete, and this maturation event corresponds to the average age for weaning in traditional societies. The full deciduous dentition is able to process food more effectively. Infancy comes to an abrupt end when the permanent first molar erupts at 6.5 years or beforehand (Robson et al., 2006). The permanent teeth emerge earlier in girls than boys, and often erupt beginning at 5.5 to 6 years, with the eruption of the first permanent molar. This is followed by the shedding of the deciduous incisors between 6 to 7 years, which are replaced by their permanent counterparts at 6.5 to 7.5 years. Deciduous molars are replaced by permanent premolars, and permanent canines replace the deciduous ones variably between 9 and 13 years (Steele and Bramblett, 1988). At about 12 years (plus or minus one year), the permanent second molar erupts behind the already partially worn first molar. The permanent third molar, or wisdom tooth, erupts at 18 years (plus or minus three years), or possibly later, between 19.8 to 20.5 years (Robson et al., 2006), but with much variation (Steele and Bramblett, 1988).

Skeletal Maturation Epiphyseal, or growth, plates begin to form from cartilaginous centers during early childhood, and form at the ends of bone shafts to permit growth in length; bone shafts often ossify by birth, or during early childhood, for mechanical and structural loading. These epiphyseal plates begin fusing to the bone shafts in a predictable sequence after puberty and the growth spurt. For example, the epiphyses of the lower humerus, which anchor some of the forearm musculature, begin closing between twelve and fourteen years; active fusion occurs between fifteen and sixteen years, but complete closure does not occur in the lower humerus until nineteen to twenty years. Similarly, the lower epiphysis of the radius from which many of the short muscles of the hand emanate, begins fusion to the shaft at seventeen years, but does not complete the ossification process until twenty-two to twenty-three years (Steele and Bramblett, 1988). The epiphyseal plate of the humeral head begins fusion at sixteen years; active fusion occurs between nineteen and twenty years, and it is complete between the ages of twenty-

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Figure 6.1. Growth (epiphyseal) plates close at predictable times. For example, the growth plate separating the humeral head from the shaft (left side) begins ossification at sixteen years, and active fusion occurs between nineteen and twenty years. Complete union is evident between the ages of twenty-three and twenty-four years. Similarly, the medial epicondyle (upper right) begins fusion at twelve years. Active fusion occurs between fifteen and sixteen years, and the growth plate is completely ossified by nineteen to twenty years (Steele and Bramblett, 1988). This individual was probably not yet sixteen years, given the lack of activity at the humeral head epiphysis and the medial epicondyle, despite its adult length. Scale bar is in centimeters.

three to twenty-four years (Figure 6.1). The epiphyseal plate of the clavicle, or collar bone, which meets with the sternum, or breast bone, may not completely ossify until twenty-five years. The vertebral bodies also do not completely mature until twenty-five years (Steele and Bramblett, 1988). The leg bone epiphyses close between sixteen and twenty years, whereas many arm bone epiphyses close later. Since the arms are heavily involved in subsistence tasks, epiphyseal union in the upper limbs is often later to permit extended growth long after sexual and dental maturation are complete. The lower sacral vertebrae do not completely ossify until twenty to twenty-five years, and an epiphyseal plate can still be observed in individuals until thirty to thirty-two years. Marked increase occurs in male facial dimensions between eighteen and twenty-five years from muscular and skeletal growth. For example, cheekbone dimensions may not reach their peak until twenty-three to twenty-five years in some males (Figure 6.2), and the supraorbital torus continues to grow substantially after eighteen years. Facial robusticity is not a characteristic of most young adult males. Male facial skeletons continue to respond to chewing stress, and corporal muscular activity, through their mid-twenties. Females, in contrast, tend to retain their subadult facial morphology into adulthood, albeit with substantial variation.

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Figure 6.2. Cheekbone dimensions, measured as the maximum extent of the zygomatic bones, as a function of age and show that males continue growing larger than females, even after dental maturation is largely complete. Age was estimated using dental eruption, dental wear, and cranial suture closure (Williams, 2013). The sample (n = 254) includes adults and subadults of unknown sex.

Skeletal Decline The major indicators of adult skeletal age in both males and females occur in the cranium, pelvis, articular surface areas, and along the vertebral column (Milner and Boldsen, 2012; Brennaman, 2014). Occupational stress, however, should not be underestimated, particularly for individuals engaging in heavy lifting and demanding repetitive tasks (Ortner, 2003). Those experiencing regular traumatic lesions from conflict with animals or other humans would also appear to age faster. Excluding extremes in physical wear, the skeletal system ages at a predictable rate across populations and time periods, such that a species-specific pattern can be discerned (Jurmain, 1977). For example, before forty years the coronal suture that separates the frontal from the two parietal bones is frequently open (Figure 6.3); after forty years it is often obliterated. Toward fifty years, with considerable variation, the sagittal suture, which separates the right and left parietal bones, ossifies. The sutures ossify from the inner table of the cranial vault, through the diploe, to the outer table, or endocranially to ectocranially (Meindl and Lovejoy, 1985; Buikstra and Ubelaker, 1994).

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Figure 6.3. The frontal and parietal bones form the majority of the superior neurocranium. The coronal (1) and sagittal (2) sutures begin to ossify on the outer, or ectocranial, surface by forty and fifty years, respectively, although much variation is observed (Meindl and Lovejoy, 1985; Steele and Bramblett, 1988). Scale bar is in centimeters.

Age-related changes on the pelvis occur on the pubic symphysis, where the right and left sides of the pubic bones meet. The two sacroiliac joints between the sacrum, or base of the vertebral column, and the ilium, or hip, also bear age-related changes. The pubic symphysis and sacroiliac joints begin to show activity by thirty-five years, but more substantial decline begins to occur after forty-nine to fifty years (Meindl et al., 1985; Lovejoy et al., 1985; Meindl and Lovejoy, 1989; Buikstra and Ubelaker, 1994; Figure 6.4).

Figure 6.4. The pubic symphysis shown in (a) represents an individual younger than thirty-five years because the ventral buttressing is missing and transverse ridges are still present. The individual (b) is estimated to be within the age range of thirty-five to forty-four years. The ventral buttressing is present, as are most of the transverse ridges. Individual (c) exhibits an age that is likely to be older than forty-five years, as evidenced by the diminished oval outline and bony islands, representing reactions of the skeletal system to mechanical loads (Meindl et al., 1985).

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The pubic symphysis bears the weight of the anterior trunk, and withstands bending energy from weight transmitted from the pelvis, laterally to the thigh, or femur. Degradation in this region can proceed as a function of age, largely independent of occupational stress (Meindl et al., 1989). For example, by thirty-five years, a ventral buttressing of bone appears, perhaps to support extra weight gained since adolescence when the bones formed. Regular changes to the pubic symphyseal surface begin to increase after forty years and include the development of an oval outline, and a gradual decrease in the height and distinction of the transverse ridges. After fifty years, the pubic symphysis begins to lose its structural integrity as the oval outline begins to deteriorate and the transverse ridges vanish entirely. Eventually the ventral rampart diminishes further, creating less structural cohesion to the front of the pelvis by the seventh decade (Steele and Bramblett, 1988). The articulation between the pelvis and sacrum, the auricular surface, also changes as a function of age (Lovejoy et al., 1985). A young auricular surface has a raised outline along its margin, and the articulation presents a billowing and dense surface. By the age of about thirty-five years, the most forward-facing margin, or apex, becomes blunted, and the articular surface shows striations reflecting biomechanical stress and strain. During the fourth and fifth decades of life, the outer margin degrades further, such that the articular surface becomes more diffuse; calcified “islands” may form within the surface, which becomes increasingly macroporous as a function of increasing age (Lovejoy et al., 1985; Steele and Bramblett, 1988). The spinal column also exhibits degenerative changes (Figure 6.5). Aging on the spine can accelerate greatly, depending on subsistence economy and occupational stress (Maat et al., 1995). Changes can include lipping around the body of the vertebra (Buikstra and Ubelaker, 1994; Snodgrass, 2004; Brennaman, 2014; Quispe and Williams, 2019). Bony irregularities and spurs (osteophytes) on the transverse processes, which face to the side, and the spinous processes, which project directly back, or posteriorly, are responses to mechanical stress (Listi and Manheim, 2012). The small facets that interlock mating vertebral pairs suffer disintegration as a function of age and biomechanical loading. Osteoarthritic lipping often forms on the margins of these articular surfaces, increasing markedly in the cervical (neck) skeleton between fifty and seventy years, particularly in males (Quispe and Williams, 2019). Macroporosity, or lack of bone density, and eburnation, or polish from bone-to-bone contact, increase after fifty years in both sexes (Snodgrass,

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2004; Quispe and Williams, 2019). The progressive loss of the vertebral bony integrity diminishes performance and can become arthritic by, for example, accumulating osteophytes (Steele and Bramblett, 1988; Brennaman, 2014). Dental wear, or attrition, and rates of gum recession begin to increase more markedly after forty-nine years (Figure 6.6). Older individuals suffer from more dental carries, dental abscesses, tooth decay, calculus buildup, and tooth loss compared to younger individuals (Maat, 1987; Maat and Van der Velde, 1987). The condition of the teeth is a good Figure 6.5. The vertebral body of this specimen shows lipping, which is a response to mechanical loading over several decades, although lipping can begin as early as twenty-three years (Steele and Bramblett, 1988). Occupational stress and caretaking of infants can accelerate the process of spinal degeneration, but age-related changes proceed regardless (Weiss and Jurmain, 2007). Scale bar is in centimeters.

Figure 6.6. Dental wear and tooth loss occur as a function of diet and age, as shown in this older individual. The third molar is heavily worn, suggesting that at least one to two decades have passed since its eruption. Tooth loss is more often associated with advanced age as the alveolar tooth-bearing bone diminishes, but can also occur early in life depending on diet, health, and oral behavior. Scale bar is in centimeters.

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proxy for the overall health of an individual, which also decreases with age. The loss of alveolar, or tooth-bearing, bone may accelerate the aging of the face as a function of time. Joint surface areas, where bones articulate with one another, present another site where age-related changes can be readily observed. These include a “lipping” of the joint surface toward the margins of the bony facet. The lipping associated with age, as well as with intense use, which would include occupational stress, forms a raised surface which buffers the joint extremes from damage derived from excessive use (Ortner, 2003; Weiss and Jurmain, 2007). This secondary remodeling of bone occurs throughout the skeleton in response to injury or trauma, but is particularly evident in areas where bones meet each other while transmitting significant loads, such as during locomotion or during other weight-bearing or repetitive activities (Ortner, 2003). Lipping of joint surface areas occurs on the shoulder joint, which includes the humeral head and glenoid fossa of the scapula; on the hip joint, including the femoral head and acetabular margin of the pelvis; on the knee joint, which includes the tibial and femoral condyles; and on the elbow joint, particularly on the trochlear notch of the ulna and trochlea of the distal humerus (Webb, 2010). Age-related changes, including osteoarthritic lipping of joint surface areas, also occurs in the finger and hand bones, as well as on the foot and toe bones (Steele and Bramblett, 1988; Ortner, 2003). These changes mimic the tumescence of effective father care as mechanical loads of carrying become more taxing to the pelvis, vertebrae, knees, hips, shoulders, and elbows. Moreover, these patterns are consistent across modern humans and can be seen in historic populations as well. Therefore, it is reasonable to suggest that this aging pattern is a species-specific trait that has evolved over time as an adaptation. Peak skeletal health in males is approximately twenty-five to forty-nine years, corresponding broadly to patterns of father care, particularly with respect to recent foragers. Fathers must be able to carry infants and provision weaned dependents for nearly two decades, and these activities are functionally enhanced by peak skeletal health after maturation and before decline. The progression of human aging is a response to selection pressures acting over thousands, hundreds of thousands, to millions of years. These skeletal changes may estimate age at last “birth” in males, with some variation, to be between forty and fifty years. Social circumstances and the relations of power may act to prolong male reproduction

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beyond fifty years (Bribiescas et al., 2012). Human patterns of life history are derived from the common ancestor of hominoids in a number of ways. One striking difference is the increased longevity of humans and a vigorous post-reproductive life (Hawkes and Paine, 2006). The skeleton, while degenerating at a more rapid pace after fifty years, still maintains considerable strength and vigor for one to two decades thereafter, with considerable variability. The maintenance of skeletal health provides males with a continued ability to assist provisioning dependents until their maturation.

Tsimane Aging indicators among the Tsimane of Bolivia, a remote foraginghorticultural group, agree with the breakdown of skeletal tissues as a consequence of advanced age observed by osteologists. The strength of men begins to decline between thirty and forty years (Gurven et al., 2017). As a consequence of decades of active foraging and food production, both men and women experience increasing frailty beginning at sixty years and intensifying greatly after seventy years in those who survive to this advanced age (Gurven et al., 2017). The decline in the skeletal system runs parallel to diminishing hearing and sight at close distances found in the majority of individuals older than sixty years. By seventy years, men must forgo hunting because of increased frailty, poor vision, hearing, and coordination; men also experience difficulty in walking long distances due to aches and pains from bone spurs, or osteophytes, coupled with joint and back pain, and lethargy (Gurven et al., 2017).

Reproduction in Older Males Understanding the way in which men age and the reproductive potential of older men is obscured by reports of specific individuals fathering infants into their ninth decade. Ethnographic descriptions of foragers suggest older males may be more effective hunters, providers, and caretakers than their younger counterparts (Bribiescas et al., 2012). Some males father children into their fifties and sixties, although it is unusual when historical records of male reproduction in industrial economies are examined (Tanner, 1981). However, for most men, sexual behavior leading to reproduction tapers off, in natural fertility populations, corresponding to the age at which women cease reproduction altogether between forty-five and fifty years (Ellison, 2002). Whereas females have a definitive demarcation between the onset and terminus

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of reproductive status, males differ by having no obvious indication of changes in potential fertility (Mead, 1955). Males gradually become fecund during the second decade of life, but are quite variable in the age at which a decrease in the ability to deliver viable sperm occurs. Between the ages of forty-eight and seventy years, males undergo a reduction in testosterone levels called andropause (Jones and Lopez, 2006). This is a gradual process that occurs over the course of decades, although a reduction in the ability to produce testosterone usually coincides with a more rapid skeletal decline beginning at fifty years, with some variation. However, in cultures lacking ad lib food consumption and high degrees of sedentary behavior, reduced testosterone after forty years is not as marked (Bribiescas and Ellison, 2008). Reduction of testosterone levels occurs from the diminished number of Leydig cells capable of hormone production. The seminal vesicles increasingly shrink as a function of age, as do the penis and scrotum. As males increasingly age in older adulthood, erection and ejaculation become more challenging without direct stimulation, and sperm motility and semen volume decrease (Jones and Lopez, 2006). Although some men remain fertile through the eighth decade, males at advanced ages are unable to effectively harness the skeletal and muscular strength and endurance of an effective caretaker, which involves carrying and caring for infants during the first three postnatal years, and provisioning for decades. Thus male reproduction and, correspondingly, father care is limited by age rather than unconstrained.

2 Evidence of Father Care in Humans and Animals

7 Forager Fathers and Infants Cross-culturally There is much variation in the relationship between fathers and infants cross-culturally (Gray, 2011). In general, however, it appears that subsistence strategy plays a large role in how fathers and infants interact. Subsistence strategies are ways in which social groups obtain food and other resources, and include foragers who live by hunting wild animals and gathering wild plant foods as well as food producers, which include herders, horticulturalists, intensive agriculturalists, and industrial agriculturalists. Horticulturalists create fields by slashing and burning tracts of forest. They then plant seeds in the ashes while leaving prior fields fallow for many years. Most horticulturalists also collect wild plants and hunt animals. Intensive agriculturalists utilize plowing and fertilizers to farm the same plots every year, whereas industrial agriculturalists use mechanized equipment, artificial fertilizers, and pesticides, and are normally controlled by capital investment, multinational corporations, and large factory farms. Industrial agriculture feeds urbanites who have been separated from food production altogether, given the sale of their labor for cash which can, in turn, be utilized for the purchase of food. Using father-infant proximity as a measure of paternal involvement, foragers have the highest level of paternal behavior (Marlowe, 2000). Similar to foragers, wealthy urbanites tend to have strong father-infant relationships, followed by horticulturalists. Less developed father-infant bonds often occur among agriculturalists and poor urbanites, with much variation. The least developed father-infant relationships are often found among herders, where the separation of the sexes is the most extreme (Katz and Konner, 1981). Rakash, an Indo-Caribbean male from a small town, provides an example of a poor urbanite father who is present but not affiliative.

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Rakash brings his youngest infant to his wife’s parents and an older child to a daycare facility during the work week. With the older child, the disciplinary “treatment can be harsh[,] involving physical punishment and a series of stern verbal reprimands” (Roopnarine, 2013: 203). Although he spends more time with his children than previous generations of fathers in his community, his interaction with the children is “confined to taking the children to places and events,” and he “remains quiet for long stretches of time when he is with the children” (Roopnarine, 2013: 204). Rich urbanites present another view of fatherhood, demonstrating the role of economics on father-infant proximity. For instance, in Amherst, Massachusetts, a group of researchers conducted more than 1,200 spot-checks for 38 infants aged from 2 to 30 months for 8 months to assess the proximity of mothers (working both full-time and parttime), fathers, and other primary caregivers to infants. Mothers were “in the immediate vicinity” of their infants “in 73% of the observations compared to 44% for fathers” and “mothers were the closest adult for 64%, compared to 33% for the father” (Edwards et al., 2015: 169). Detailed accounts of father-infant interaction “revealed fathers to be very involved in both play and caregiving activities” (Edwards et al., 2015: 169). In the United States and perhaps internationally, positive fatherhood includes emotional closeness; protection from danger and negative elements; a substantial contribution of time, resources, and effort in direct childcare; encouragement of nurturing efforts of the spouse; and enabling educational and extracurricular activities that contribute to building character, procreation, marriage with the mother, secure employment, and providing a home (Townsend, 2002; Shwalb and Shwalb, 2015). Many families in India and elsewhere have made the economic decision of substituting father salience for greater income, producing the “skipped generation,” in which parents, and most frequently fathers, work in a different, often urban, location, while the children and grandparents remain at home. These “floating fathers” provide economically for their children, yet actually may see them only once per year or less (Shwalb and Shwalb, 2015: 612). Across cultures and even in smallscale societies, increases in status, wealth, and marriage stability seem to contribute to positive fatherhood (Shwalb and Shwalb, 2015). However, poorer fathers who work out of the family home may have greater social involvement with young children than those who engage in higher-paid extradomestic work, at least in India (Jain and Belsky, 1997). Therefore,

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differences in socioeconomic status among food producers do not fully explain the variation observed in father care.

Foragers and Father Care In forager groups, differences in status are much less pronounced, and opportunities to acquire status are reduced or nonexistent (Marlowe, 2000). Positive father care in these societies is enhanced by egalitarian relations between spouses, a reduced emphasis on the division of labor with respect to subsistence and childcare, and a lack of status markers (Fouts, 2008). Since humans evolved as hunter-gatherers, it may be that the traits correlated with positive father care in living foragers, at least in part, characterized ancient human cultures. Such an evolutionary innovation would most likely decrease infant mortality. It is noteworthy that the word for father, along with the word for mother, are among the earliest spoken by infants across cultures and subsistence patterns (Lubbock, 1873). In many languages, variants of the word papa derive from the root pa, which translates as “not to beget, but to protect, support, to nourish” (Lubbock, 1873: 283). Concerning foragers, there are a number of societies that are distinct in their father-infant involvement, including the Aka, the Bofi, the Agta, the Batek, the Lesu, and to a lesser degree, the Efe (Fouts, 2008). Forager societies that exhibit less extreme father-infant interaction include the Ache and the !Kung, although even in these societies, there is still substantial father-infant involvement, such as among the Ache, where males carry infants between campsites until children are about five years old (Hill and Hurtado, 1996). In contrast, agricultural Lesse males will only care for infants as long as other males are not present, if at all. There is a strict division of labor among the Lesse, which contributes to different male and female spheres. This serves to limit father-infant interaction. In cases where the division of labor is less pronounced or absent altogether, fathers have greater involvement in infant care (Marlowe, 2000). For example, among the Aka, both males and females participate in the net hunt to capture small animals, although males also leave the forager camp to hunt independently. Among the Agta, both males and females hunt cooperatively and individually. Both sexes will hunt and kill animals for food while holding infants (Hewlett, 1991). Among the Batek and Aka, father-infant involvement can include infant suckling when mothers are foraging (Hewlett, 1991; Endicott and Endicott, 2014). Males can lactate but only through active solici-

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tation and never in much volume. Males that care for infants among foragers must also attend to the elimination needs of their offspring. Infants learn to urinate and, later, defecate after signaling within the first year to year and a half, or earlier. To be caretakers among foragers, fathers must learn to anticipate the elimination needs of infants, and to clean the infant when a miscommunication occurs. Although subsistence strategy plays a large role in predicting father-infant interaction, the relationship between the sexes may be an even stronger factor. In egalitarian societies, where females and males do not have striking differences in access to resources, power, and prestige are shown to have greater father-infant proximity. Foragers, such as the Batek, have cooperative social relationships, which encourage the sharing of tasks and result in a less extreme division of labor based on sex, combined with much individual autonomy (Endicott and Endicott, 2014). The “cooperative autonomy” of the Batek also recognizes the strong empathy for others (Endicott and Endicott, 2014: 121). To avoid living alone, which is dangerous, mobile hunter-gatherers must consider the opinions of other camp members before arriving at their own decision. For individuals to decide, “discussions took place every day in camp about what people wanted to do and where they wanted to go, and the composition of work groups varied from day to day” (Endicott and Endicott, 2014: 121). Because “others are respected for what they are” and “men and women, young and old, do pretty much what they want,” there is a substantial degree of autonomy and equality within forager societies (Hewlett and Roulette, 2014: 132). Egalitarianism is also a set of moral obligations that fosters cooperative work and social activities (Endicott and Endicott, 2014), and is emphasized within the context of games, dances, and rituals (Gray, 2014). In contrast, where gender relations are highly asymmetrical, the sexes are separated, and infants are paired only with females. These societies often exhibit a strict division of labor, which contributes to different female and male spheres. In these societies, males do not participate in infant care at all. Status seeking also plays a role in determining father-infant relations. When males are driven to acquire access to more resources, including additional wives, father-infant involvement is limited. For example, among the egalitarian Aka foragers and polygamous Lesse farmers living in close proximity to one another, Aka fathers exhibit strong father-infant involvement, whereas Lesse fathers are less involved, particularly those who have multiple wives (Hewlett, 1991).

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Cross-cultural Context of Father Care Foragers and matrifocal horticulturalists exhibit the strongest fatherinfant relationships. Generally, a close relationship between the parents, monogamy, collective subsistence endeavors, and shared social activities are associated with positive paternal behavior (Katz and Konner, 1981; Fouts, 2008; Edwards et al., 2015). With regard to foragers, there are a number of societies that are distinct in their fatherinfant involvement. However, there is no uniformity (Kramer, 2010). Matrifocal societies also tend to exhibit pronounced father-infant interaction, regardless of subsistence practices. For instance, the Hopi, who are noted to exhibit strong father-infant bonds, can be described as strongly matrifocal (Curtis, 1921). If father care was an important component of infant development during human evolution, then these practices should remain in societies in which status and wealth accumulation have not distorted the relations between the sexes. Evidence for these practices can be found within the ethnographic literature from the past 150 years.

Evidence of Father Care in the Ethnographic Record A number of forager and small-scale farming and herding cultures exhibit positive paternal-infant relationships, and these can be grouped by region. Greater Australasia, the South Pacific, and Central/East Africa provide particularly illustrative examples of father-infant proximity. Much variation in father-infant relations exists in the Americas, Papua New Guinea, and South Asia. There are fewer examples of close father-infant proximity in North Africa, West Africa, Southwest Asia, and East Asia, where extreme forms of patriarchy exist, and particularly where polygyny is prevalent. The following ethnographic anecdotes are not exhaustive but do provide evidence for father care across smallscale subsistence strategies, including foragers, fisher/horticulturalists, horticulturalist/foragers, agriculturalists, and herder/agriculturalists.

Father-Infant Proximity among Foragers Agta The Cagayan Agta, a foraging society inhabiting the Pacific coast of the main island of the northern Philippines, hunt pig, deer, and monkeys, and collect nutritious wild tubers and other plants. The Agta can be characterized as egalitarian, in that they exhibit a strong equality between the sexes in making decisions. It should be no surprise that

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“bonding between siblings and with parents is profound” (Griffin and Griffin, 1999: 292). Both females and males hunt, and “the lack of a pronounced gender division of labor in many areas of life places fathers in a context in which their attention to children may be critical to mothers’ success in food provisioning and in bearing and rearing children” (Griffin and Griffin, 1992: 297). Agta fathers are within arm’s reach of their infants from the moment of birth, including at night, and are “present during illness and hunger” (Griffin and Griffin, 1992: 301). Fathers are less often recruited for carrying infants within camp but actively carry children during foraging and when the camp is relocated. The Agta embody a “widespread custom of giving much attention to infants and toddlers” (Griffin and Griffin, 1992: 301). The egalitarian nature of female-male relations is further emphasized by the statement, “Fathers’ caregiving to children among the Agta foragers of the Philippines is especially interesting because of the participation of women in hunting wild pig and deer” (Griffin and Griffin, 1992: 297). Aka The Aka represent the quintessential fathers among foragers. These Central African Republic and People’s Republic of the Congo societies exhibit intense male-infant proximity and are described as fiercely egalitarian (Hewlett, 1991). Males participate in infant care more than any other group known. “Holding provides psychological comfort as well as protection from the external environment” (Hewlett, 1991: 76). However, the Aka cannot be described as a child-focused society, meaning that they do not alter their behavior when a child is in proximity. Given their frequent proximity and contact, fathers “may influence the infant’s survival as well as emotional development” (Hewlett, 1991: 76). Infants were unlikely to cry when held by their fathers. Fathers cared for their infants about 20 percent of evening hours and about 9 percent of daylight hours, carrying and caring for infants. “Aka fathers provided quality time to their infants since in over one-fourth of the holds [holding the infant] the father did not engage in other activities and devoted his attention almost exclusively to the infant” (Hewlett, 1991: 95). Additionally, while mothers provided breast milk and more often transported infants, fathers “were more likely to kiss, hug, and clean the infant” (Hewlett, 1991: 94), as well as sing and hum to them. “During most holds, the father participated in other activities . . . Fathers in over one-third of the episodes [holding] engaged in conver-

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sation with others, especially adult males, while holding the infant . . . The father often held the infant while the mother was busy collecting firewood, preparing a meal, or net hunting” (Hewlett, 1991: 95) and “Aka fathers hold their infants and are around their children more than twice as often as fathers in other societies where comparable data exists” (Hewlett, 1991: 133). Additionally, “Aka fathers are within an arms-reach (i.e., holding, or within 1 m) of their infant more than 50% of a 24-hour period” (Hewlett, 1992b: 153). Moreover, “Aka fathers are not vigorous with their infants as suggested as the norm by Western psychology and are better characterized by their affectionate and nurturing interaction with the infant” (Hewlett, 1991: 105). Furthermore, “Aka fathers intrinsically enjoy their infant caregiving role and seek interaction with their infants” (Hewlett, 1992b: 171). Three factors seem to “predict intercultural variability in the level of father involvement: warfare, level of polygeny and ideology” (Hewlett, 1991: 125). A number of additional factors also influence Aka father involvement with infants. These include status, or the quest for status, and the presence of brothers, which implies social obligations. These factors take Aka fathers away from direct infant care. Aka father-infant involvement reflects the proximity and level of interaction between husbands and wives (Hewlett, 1992b). Father-infant proximity is frequent with males married well after adulthood, suggesting a maturation aspect to fatherhood. Other factors include living among nonkin, less support from relatives, and consequently less political ambition. Andaman Islanders Among the Andaman Islanders, which subsist on the foraging of wild plants, fishing, and hunting of pigs and turtles, fathers play an important role in the care of infants. This society is characterized by egalitarian relations between the sexes, such that “women may occupy a position of influence similar to that of men” (Brown, 1947: 47). Children are “hardly ever scolded” (Brown, 1947: 51). Further, although the primary caretakers of infants are their mothers, a child is “played with, petted, and nursed not only by his father and mother, but everyone in the village” (Brown, 1947: 76). Both mother and father carry children in slings made of bark (Brown, 1947). Except for hunting, which appears to be primarily a task of males, “both men and women perform all other daily activities, including child care, cooking, and gathering most food stuffs and materials” (Pandya, 1999: 245).

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Batek Endicott (1992) describes the social organization of the Batek of Kelantan, Malaysia, a nomadic and egalitarian foraging society inhabiting the Lebir River watershed. Among the Batek, “babies are usually held by mothers, fathers or other caregivers” (Endicott, 1992: 285). Although mothers are primary caregivers, “fathers play an important role in the social life of infants” (Endicott, 1992: 285). Fathers were observed to cook, clean, and hold their infants closely, and to “attend to their excretory needs” (Endicott, 1992: 285). They “held, cuddled, and chattered to the sons and daughters with as much obvious enjoyment as mothers showed” (Endicott and Endicott, 2014: 111). Both parents “bathed their children” and “took them outside camp to relieve themselves” (Endicott and Endicott, 2014: 111). Fathers “often made toys—such as blowpipes, swings, and clinging ladders—for their children’s amusement” (Endicott and Endicott, 2014: 111). When they returned to the camp, “fathers often carried their babies in a sling on their back and let the babies sit on their laps while sitting in their shelters” (Endicott and Endicott, 2014: 111). Both genders reported that “they desire male and female babies equally, and their affectionate behavior toward infants of each sex supports this claim” (Endicott and Endicott, 2014: 111). Fathers also provided attention to older infants when they were displaced upon the birth of a new infant. Fathers were so close to their infants that “they may go sit on their father’s lap when the men return from work—even when the mothers are nearby” (Endicott, 1992: 286), and “it was not uncommon for a man’s young son or daughter to wail despairingly for him when he left camp to hunt” (Endicott and Endicott, 2014: 117). Furthermore, “attachments to fathers appeared to be equal in intensity to those with mothers” (Endicott and Endicott, 2014: 117). Bofi The Bofi hunter-gatherers of Central African forests like the Aka are known for their positive father-infant proximity (Shwalb and Shwalb, 2015). Bofi and Aka fathers with less support from kin showed the greatest degree of positive interaction with infants (Fouts, 2008). A Bofi forager, Ba’win, was close with his three year old son as well as with his eighteen month old grandson, Lee, as evidenced by the observation that “Lee sat near or on Ba’win’s lap most of the afternoon” and with the onset of a tropical rainstorm, “Lee ran straight to Ba’win

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rather than to his grandmother or aunt (his parents were in the forest)” (Fouts, 2008: 152). Bofi fathers were observed to demonstrate the greatest degree of paternal care during the first twenty-four months of infancy and at three to four years during weaning, as these two periods represent the most dangerous junctions in the lives of young children (Fouts, 2008). Central Australia Among Aboriginal foragers of central Australia, extraordinary affection and tenderness existed between both parents and infants. It has been observed that “childcare among Australian Aborigines, like most hunter-gatherers, is characterized by a high degree of nurturance and indulgence” (Burbank and Chisholm, 1992: 179). Though a strictly defined sexual division of labor and asymmetric gender relations characterized these Aboriginal gatherer-hunters—with infants primarily attached to their breastfeeding mothers—the extent of involvement between an infant and father pair was noteworthy. For example, “in caring for children the ‘father’ generally assists as much as he is able” (Montagu, 1974: 345). Efe Efe foragers in Central Africa traditionally hunted game and gathered roots and other edible resources from a tropical forest habitat. In comparison to the Lese, a nearby farming society, “forager fathers spent over twice as much time with their one-year olds than did farmer fathers” (Morelli and Tronick, 1992: 252). Husbands spend substantially more time with their wives than do Lese fathers, who often seclude themselves. Therefore, “forager fathers often eat, work, and relax around their families providing one-year olds with ample opportunities to be with them” (Morelli and Tronick, 1992: 255). Given the lack of extremes in the sexual division of labor, “fathers, men and boys also share any activities with women including the care of young children” (Morelli and Tronick, 1992: 255). In other words, “it is therefore appropriate for males to be involved in the care of young children and there are plenty of opportunities for them to do so” (Morelli and Tronick, 1992: 255). In contrast, among Lese farmers, “women and children are often isolated from the company of fathers and men when [working] in the fields and when engaging in domestic duties” (Morelli and Tronick, 1992: 255).

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Father-Infant Proximity among Fisher/ Horticulturalists and Island Societies Anuta The Anuta, a Polynesian society on the outer reaches of the Solomon Islands, obtain their sustenance from farming, fishing, and hunting, and are described as egalitarian. According to ethnographic accounts, the children “may cling to either parent’s back while the latter goes about their daily chores” and “both parents play a role in their offspring’s discipline and education” (Feinberg, 1981: 84). Also, among the Anuta, it was noted that “as soon as the child is old enough to withstand a man’s less-skillful handling, the father begins to play a role” (Feinberg, 1981: 85). Additionally, “fathers are seen carrying children in their arms or holding them in their lap” and “men desire children and speak of them with obvious pride” (Feinberg, 1981: 86). Ifaluk The South Pacific Carolina Island of Ifaluk, about a thousand miles away from Australia and New Guinea, is located in the Federated States of Micronesia. Traditionally, females grew taro and other subsistence foods while men engaged in communal fishing. Many observers have commented upon the indulgence given to young children, with remarks such as “the baby is king in Ifaluk” (Burrows and Spiro, 1957: 274). With regard to paternal behavior, it has been observed that “Ifaluk fathers are doting fathers” and that “the men there love their children” (Betzig and Turke, 1992: 111). Although variability is present, “fathers on Ifaluk seem to spend as much or more time with their children as fathers in other traditional cultures spend with theirs” (Betzig and Turke, 1992: 111). Magi Among the Magi, an agricultural fishing society from Papua New Guinea, the relationship between the sexes can be described as egalitarian in that a rigid division of labor between females and males was lacking (Malinowski and Young, 1988). Polygamy was also absent, although warfare was continuous. Nevertheless, Magi fathers were often observed caring for and carrying infants (Malinowski and Young, 1988).

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Tikopia The Tikopia of Polynesia were traditionally subsistence farmers. Although the mothers were the primary caregivers, other members of the household such as unmarried sisters of the father or mother also contributed care. Still, “the father is expected to take his turn at looking after the child, and usually does this with apparent interest and pride” (Firth, 1936: 140). This was particularly true subsequent to the immediate postnatal period. After the earliest days of life, fathers would provide direct care to infants such that “he is frequently to be found holding it in his arms” (Firth, 1936: 140). As an infant matured and was able to crawl or move about, “the father may be called upon to mind it in the absence of its mother, and respond to the duty as a matter of course, if not with alacrity” (Firth, 1936: 140). In this way, parenthood was a shared responsibility built on cooperation and “an obligation to be shared between them” (Firth, 1936: 140). For example, “if the woman goes on to the reef she leaves the little child to its father to look after” (Firth, 1936: 140). Trobriand Islanders Among Trobriand Islanders from an archipelago off the coast of Papua New Guinea, father-infant interaction was pronounced, although both females and males were observed participating in the care of infants in this egalitarian society (Malinowski, 1927; Weiner, 1933). Fathers “work hard for their small children” (Weiner, 1933: 58) and would decorate the infant to convey social status and wealth. Additionally, “men care for young children while working” (Weiner, 1933: 59) and “men walk around the village holding a baby or toddler straddled on their hips, often with another child in tow” (Weiner, 1933: 58). Fishing, domestic pigs, and the cultivation of root crops formed the basis of the subsistence strategy in the Trobriand Islands. The division of labor was not strictly enforced such that males could participate in family activities without suffering a loss of status among other males. Although patrilocal, the Trobriand Islanders were described as matrilineal, where kinship was reckoned through the mother and her brothers. Since property traditionally passed through the matriline, as children approached adolescence, the mother’s brothers increasingly became involved in paternal care, eventually supplanting the mother’s husband. However, the mother’s husband also gave their children names from their sister’s matrilineal descent group because

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“so important is the circulation of a man’s matrilineal property that a man’s gift to his children establishes intimate bonds with them” (Weiner, 1933: 56). Indeed “[fatherless] children” were disadvantaged, not in material well-being provided by the matrikin, but “not to have a father is to lose the social potential to be gained from the kinship ties he makes available” (Weiner, 1933: 58). Therefore, to be a socially recognized father came with responsibilities and obligations such that “men not only must provide food for their children but also are responsible for enhancing their children’s beauty” (Weiner, 1933: 59). When infants were a few months old, they were “decorated with shells by [their] father to make [them] socially beautiful” (Weiner, 1933: 59). In other words, to be socially beautiful means “powerful and wealthy relatives” such that “social and political advantage is already established through the messages that decorations convey about the infant’s father” (Weiner, 1933: 59). Noteworthy father care among Trobriand Islanders has been emphasized by others such as Bronislaw Malinowski (1927). The father was considered an outsider to the wife’s family, although the married couple resided in the same house and “the father is a close companion of his children” (Malinowski, 1927: 16). Additionally, “he takes an active part in the tender cares lavished on the infants, invariably feels and shows a deep affection for them, and later shares in giving them instruction” (Malinowski, 1927: 16). Even the meaning of the term for father, tamala, or “mother’s husband,” emphasized the pair-bond, and reinforced the expectations of males “whose role and duty it is to take the child into his arms and to help her in nursing and bringing it up” (Malinowski, 1927: 72). The father’s role during pregnancy was equally important. Regarding the pregnant mother, “there is the need for a man to keep guard over her during childbirth” and, in the words of an informant, “to receive the child into his arms” (Malinowski, 1927: 83). Thereafter, “this man has also the duty of sharing in all the tender cares bestowed on the child” (Malinowski, 1927: 83). Indigenous belief systems provided meaning to these cultural practices. During pregnancy, women were believed to provide the flesh and blood of their babies, whereas an ancestral spirit that enters the mother through supernatural means is the essence of an individual. Since siblings are each from different ancestral spirits, resemblances between them were not recognized. As for the father, the children of his wife resembled him and him alone—not the mother or her family.

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The resemblance of the man’s wife’s offspring to him was reinforced through accentuating and reinforcing the father’s physical and behavioral similarities to his infants and children. These beliefs were substantiated by Trobriand Islanders’ disavowal of any relationship between sexual intercourse and progeny, attributing all resemblance between the father and his children to molding. This can be likened to what occurs when a palm is opened and upward-facing: “put some soft mash (sesa) on it, and it will mould like the hand” (Malinowski, 1927: 93). As the partner of the mother, the wife’s husband contributed his economic efforts, care, and proximity during pregnancy and early childhood, molding the physical features of his offspring. Active involvement in infant care by males—while at the same time ignoring paternity—may have been how father care evolved as a component of marriage, culturally mediated sexual relations between the genders, and the reckoning of kinship (Malinowski, 1927). Furthermore, through female choice for males who exhibited affiliative paternal behavior, father care may have preceded the evolution of pair-bonding. Such a scenario contrasts with the idea that male-infant involvement arose as a consequence of paternity certainty derived from the exclusive pair-bond (Smuts and Gubernick, 1992).

Father-infant Proximity in Small-scale Horticulturalist/Foragers Akuma In Brian M. Du Toit’s (1975) ethnography of the Akuna, a horticultural society in lowland New Guinea, fathers are described as highly involved with their infants. Fathers were observed to rival the mother in terms of active parenting, spending several hours per day proximate to, or holding, infants while affectionately stroking or patting them. For example, Du Toit (1975) relates that fathers would carry infants for hours while the infant’s mother worked in the garden. Father proximity to the infant began as soon as infants were able to crawl. Thereafter, fathers were seen carrying infants on their shoulders or on their hips. Dyaks The Dyaks of Borneo historically engaged in a variety of head-hunting rituals, which included cannibalism. Nevertheless, this rich horticultural society can be described as monogamous, although asymmetri-

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cal power relationships existed between the sexes. Given the lack of extreme patriarchy, it is not surprising that “Dyaks [males] show great respect for their wives, and are very fond of their children, whom they take in turn to nurse [take care of]” (Bock, 1881: 210). Lesu Among the forager/horticultural Lesu of New Ireland in the greater Australasian archipelago of the South Pacific, fathers held and playfully engaged with infants. The Lesu can be described as a society where a “dominating female cultural modality” pervaded the relationship between the sexes, and where fatherhood was a fundamental quality of manhood and male identity (Aijmer, 2007: 237). Correspondingly, fathers valued infants of both sexes, and additionally, among the Lesu, “uncertain biological fatherhood was irrelevant to the social positioning of children” (Aijmer, 2007: 236). Furthermore, “a young infant was an object of deep affection to his social father . . . as soon as the child was old enough to walk it would most frequently be the father who cared for it, while the mother was working in the gardens” (Aijmer, 2007: 236). Yanomamö The Yanomamö in the Amazon basin are described as seminomadic foragers who supplement the diet by cultivating root crops. It is clear that families care for their children and show much affection toward them (Good and Chanoff, 1991), albeit with much variation (Hames, 1992). Infants are in close contact with their mothers, and fathers are clearly very nurturing of both their daughters and sons. Additionally, “fathers cuddled their babies or played with them in their hammocks” (Good and Chanoff, 1991: 42).

Father-infant Proximity in Small-scale Agriculturalists Anyanja, Angoni, and Yao The Anyanja, Angoni, and Yao of early-twentieth-century Malawi (British Central Africa) grew corn, pumpkins, beans, cassava, and other crops, which were supplemented by domesticated animals and hunted game. Although polygyny was practiced, it was not common. Children slept with both parents such that “the wife lies facing the back of her husband, a baby lies at the mother’s breast” (Stannus, 1910: 287). The mother’s kin claimed the children rather than the father’s, and a father

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would have to tend to the garden of his wife’s mother until “he has brought her the first grandchild” (Werner, 1906: 132). Although not overly affectionate, a father was “certainly not indifferent to their children” (Werner, 1906: 148). Traditionally, women would carry children on the back using a cloth or a skin or on the hip, while “a man carries a child sitting on his shoulders” (Stannus, 1910: 288). Bangangté The Bangangté of Cameroon were traditionally subsistence farmers and relatively egalitarian, although polygyny was practiced to a limited extent. Women were not forced into marriages to which they objected. Both males and females were obliged certain responsibilities, including childcare. For example, if a mother cannot be at home to care for the children, other wives or neighbors will do so; “otherwise, the husband must keep an eye on his children” (Egerton, 1939: 234). Busama Among the Busama on the eastern shore of Papua New Guinea, villagers practiced subsistence agriculture of root crops, such as taro, and kept pigs and chickens, fished, and maintained tropical fruit orchards. Males were not heavily involved during the first six months postnatal, unless the new father “is by nature fond of children, or if this is his firstborn, he may hold it earlier” (Hogbin, 1963: 62). Thereafter, throughout infancy, “he takes the child during the late afternoon when his day’s work is done and carries it about on his hip” (Hogbin, 1963: 61). Additionally, “fathers are no less tender than mothers, and they also croon, nuzzle, and stroke” (Hogbin, 1963: 61). Hopi The Hopi of the Southwest of the United States traditionally farmed maize, beans, and squashes, and hunted animals. Hopi fathers are known to be equally adoring and adored by their infants as their mothers and to express much affection for their children. For example, one would often observe “the baby toddle eagerly into the outstretched arms of the home-coming father who would then lift the child over his head with a laugh and dance it in the air to the strange, geometrical ever-changing rhythms of a Hopi Katzina dance-song” (Curtis, 1921: 555). Fathers among the Hopi conveyed cultural knowledge between generations through their interactions with infants at a young age. For instance, “the baby on its father’s knee was taught its first dance-

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gestures as the man sang and moved the tiny arms rhythmically, shaking an imaginary dance rattle, invoking rain, or spreading the water over the fields in the symbolic pantomime of the ancient dance-dramas whose traditions the child thus absorbed with its first consciousness” (Curtis, 1921: 555).

Father-Infant Proximity in Herder-Farming Societies Dakota and Other Plains Tribes The invocation of fatherhood and motherhood as sources of life-giving forces of nature is widespread among Native American cultures. For example, “Mother Corn” is often described as the one who originally grew corn. “Father” is associated with the creation of the universe and more materially in the bow and arrow as instruments of protection and provisioning (Curtis, 1921). Fathers as warriors traditionally held influence over the cultural transmission of knowledge, particularly for sons, which included instruction in hunting, scouting, and healing (Shears et al., 2011). For example, among the Dakota, the term Akicita was used to refer to a husband and father who was calm and pacified at camp but a ferocious beast in battle. These men were obliged to keep both camp and warrior personas distinct and never to conflate them (White et al., 2006). Akicita were primary role models of behavior for male children (White et al., 2006). A variety of Native American sleep songs for babies exist from such tribes as the Pawnee, Yuma, Kwakiutl, Arapaho, Cheyenne, and Hopi (Curtis, 1921). These songs reflect the close association between infants and their caregivers, some of whom were fathers (Figure 7.1). The devoted care of Native American infants by both parents was recorded by fur traders with such statements as “If it’s anything a man is plum crazy about, it’s his kid!” (Curtis, 1921). The unconditional love for children expressed by both mothers and fathers among tribal Native American families is well-documented (White et al., 2006). Gogo Societies characterized as herder-agriculturalists differ from foragers in their food-producing behaviors, gender asymmetry, and inheritance of wealth. Still, among the Gogo of Tanzania, traditionally herders of cattle, fathers were affectionate with children, calling a small son “baba,” which translates as father, “and playing with him with remarkable

Figure 7.1. Ojibwa father with son circa 1870.

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patience and gentleness” (Rigby, 1969: 262). Additionally, “a father, together with his wives’ brothers—his children’s mother’s brothers— will go to great lengths to ensure the health and prosperity of his children” (Rigby, 1969: 262).

Biocultural Synthesis of Human Fatherhood These anecdotes provide evidence that father involvement with infants was once widespread among matrifocal and egalitarian societies, particularly those with either foraging or fishing (a type of foraging) as the principle form of subsistence. Yet there are many examples where males did not engage in the caretaking of infants, and some of these such as the Ache and the !Kung are foraging societies (Howell, 1979; Hill and Hurtado, 1996). However, even in these societies, fathers are shown to actively participate in provisioning infants. Genetic fatherhood may be all that is needed to produce a child. However, it is the social factors that tend to promote survival and enhance the quality of infants’ lives in a socially complex and environmentally unpredictable world. These social factors include infant carrying and proximity, particularly during the sensitive first three to four postnatal years. The worldwide distribution of father care, as demonstrated by these ethnographic anecdotes, suggests it was contiguous and perhaps universal in the past, particularly before large-scale agriculture and other intensive forms of food production emerged. The proposed universal nature of father care and father-infant proximity before the Neolithic revolution, some ten thousand years ago, would imply that it is an adaptation of the human species entailing an elongated maturation schedule of a highly encephalized and social brain.

8 Paternal Behavior in Nonhuman Primates and Other Animals

Paternal behavior has been observed in numerous mammalian taxa, including carnivores, rodents, ungulates, and primates (Clutton-Brock, 2016). However, paternal behavior is also noted in invertebrates, fish, amphibians, reptiles, and birds. Across the animal kingdom, there are costs and benefits to staying or leaving the young for both males and females (Clutton-Brock, 1991). Infant care is particularly costly to males because it has the potential to detract so significantly from the ability to secure additional reproductive opportunities elsewhere (Trivers, 1972; Hawkes et al., 1995; Gray and Campbell, 2009). In multiple taxa, fathers increase infant survival by defending the smallest and most vulnerable members of a group from predators and conspecifics, whereas in many birds, social carnivores, rodents, nonhuman primates, and humans, direct provisioning of infants by males is observed. Given its reproductive cost to males, one wonders how father care ever evolved in the first place. The fact that it can be observed across the animal kingdom in different forms, and in humans, suggests that under certain conditions, females prefer to mate with males who demonstrate the potential for infant care. Presumably father care would benefit both the male and the infant (Trivers, 1972). Male care of the young occurs most frequently when offspring survival increases in comparison to uniparental levels, and with respect to the relative net reproductive fitness of males who do not contribute to caretaking (Clutton-Brock, 1991, 2016).

Egg-Laying Animals Paternal behavior, although rare, is observed in invertebrates such as some sea spiders, harvestmen (daddy long-legs), among other taxa, and involves egg carrying by males. Paternal behavior includes direct incu-

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bation via mouth brooding by some fish (Alonso-Alvarez and Velando, 2012). In some species, male fish transport eggs on the ventral surface, on the cranial surface, or using the inferior labial organ (CluttonBrock, 1991). Male sea horses and pipefish carry fertilized eggs in specialized brooding pouch-like organs (Clutton-Brock, 1991). Where fish taxa show caretaking behavior at all, it is often the males who care for or carry the eggs or fry, depending on the species (Clutton-Brock, 1991). Male frogs and toads of some species guard the eggs of one or more females. In poison-arrow frog species, eggs are deposited terrestrially, and females and/or males, depending on the species, carry the tadpoles to water so they may mature into adults (Clutton-Brock, 1991). Parental care involving both sexes is unusual in reptiles, although it has been observed in some snakes and crocodiles (Clutton-Brock, 1991). Paternal behavior has been noted in about 25 percent of birds— particularly large birds with elongated maturation cycles—and includes protection, feeding, and nest construction (Alonso-Alvarez and Velando, 2012). Even uni-male care is typical in some bird species (CluttonBrock, 1991). For example, in some polyandrous birds, such as the Phalaropidae, males are the sole incubators of the eggs and caretakers of the hatchlings (Trivers, 1972). Paternal behavior in birds is influenced by the adult sex ratio and life history, such that longer-lived, pair-bonded species tend to exhibit more intense male parenting efforts (Remeš et al., 2015). Although paternal care is often associated with a monogamous social organization in the animal kingdom, it is also the case that the two are not always coupled (Lukas and Clutton-Brock, 2013).

Mammals Among mammals, paternal behavior is observed in less than 5 percent of taxa, although in primates, carnivores, and perissodactyls (odd-toed ungulates), it is present in 30 to 40 percent of species, particularly in monogamous taxa (Clutton-Brock, 1991, 2016). It occurs at lower levels in mammals that consume foods which are evenly distributed and are uni-male/multifemale, or where the sexes are separated for much of the year, such as most Artiodactyla species (even-toed hooved animals) and cetaceans (Clutton-Brock, 2016). Direct paternal care, including provisioning, carrying, babysitting, and huddling occurs in 6.4 percent of rodents and perhaps more (Kleiman and Malcolm, 1981). For example, deer mice (Peromyscus californicus) males share nests with females and infants, which contribute to thermoregulation, and males of several taxa of muroid rodents, particularly Peromyscus maniculatus, aid

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females in constructing family nests and in oral cleaning of pups, at least in captivity (Hartung and Dewsbury, 1979). Wild male beavers (Castor fiber) work with females to provide a store of food for postweaned offspring (Kleiman and Malcolm, 1981). Monogamous rodents such as pine voles and prairie voles and mound-building mice often exhibit direct paternal care, as do some lagomorphs (rabbits and hares; Clutton-Brock, 2016). The evolution of caretaking among mammalian males seems to be the by-product of a monogamous social organization, rather than vice versa (Lukas and Clutton-Brock, 2013). Paternal behavior occurs most frequently in mammals where sociality is of prime importance, such as in social carnivores. For instance, male canids contribute to the survival of pups once they are weaned and still too young to hunt independently by regurgitating food or carrying prey to the den (Kleiman and Malcolm, 1981). Male canids of nearly all taxa, including foxes, jackals, wolves (e.g., Canis lupus), some coyotes (Canis latrans), and African wild dogs, as well as hyenas, mongooses, and tropical otters, have been noted to carry, retrieve, groom, babysit, socialize, and/or huddle with young (Kleiman and Malcolm, 1981; Clutton-Brock, 2016). The social cohesion of the pack or family group prompts male involvement in the care of young. Primates are also highly social animals, and paternal behavior is often contingent on the degree to which social (proximate) benefits accrue to males from infant care; these actions have evolutionary consequences (Trivers, 1972; Kleiman and Malcolm, 1981; Clutton-Brock, 2016).

Nonhuman Primates Nonhuman primates are a diverse radiation of mammals (Figure 8.1). Primates include prosimians, such as lemurs (Figure 8.2); anthropoid monkeys, such as baboons (Figure 8.3); and apes, such as gorillas (Figure 8.4). As a group, nonhuman primates have extended infancies compared to other mammals, fish, and birds (Robson et al., 2006). There are also comparatively close infant-maternal relationships among nonhuman primates (Sellen, 2006). Prosimian infants (lemurs, lorises, and tarsiers) as well as some anthropoid monkeys are nursed for between three and six months. Other anthropoid monkeys, such as macaques and baboons, are nursed between one to two years, whereas New World capuchin (Cebus or Sapujus) mothers nurse for up to three years. Gorillas are often weaned at two to three years (Figure 8.4), whereas chimpanzees are weaned between three and four years. Orangutans exhibit the longest infancies, with weaning taking place at seven to

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eight years (Robson et al., 2006). During this time, infants increasingly supplement their diets with foods that are softer than those typically consumed by adults (Sellen, 2006). Primate infants exhibit a long and intense period of social bonding with their mothers, given the length of the nursing period and the close proximity of mothers and infants (Figures 8.2, 8.3, and 8.4). The social nature of mother-infant interaction in primates includes nourishment as well as tactile grooming, eye contact, play behavior, and comforting. During this period of attachment, mothers become the first and foremost social partner of infants. It may be that all other sociality between

Figure 8.1. Primate phylogeny. Strepsirrhines include the lemurs and lorises of Africa and Asia. Tarsiers of Indonesia and the Philippines can be grouped with lemurs and lorises as prosimians, or with monkeys and apes in the Haplorhini. Anthropoid monkeys include New World taxa such as capuchins, squirrel monkeys, howlers, tamarins, marmosets, and spider monkeys, as well as Old World monkeys, such as macaques, baboons, leaf monkeys, and guenons. The great apes include those most closely related to humans (Homo), such as gorillas (Gorilla) and chimpanzees (Pan), as well as orangutans (Pongo), which are more distantly related to the African apes (Homininae). The table presents representative genera rather than an exhaustive list.

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group members arose from the initial mother-infant bond in a primordial mammalian ancestor (Jolly, 1985). This social bonding and interaction was later elaborated upon and extended, particularly in the great apes, such as chimpanzees.

Figure 8.2. Lemurs, lorises, and tarsiers, nurse their infants for three to six months depending on the species, which is considerably longer than in similar-sized nonprimate mammals. In spectral tarsiers, where infants are “parked” while the mother forages, infants have been reported to be visited by other group members (Gursky, 1994). In strepsirrhine primates that carry their infants, newborns are kept on the ventrum to nurse on demand. Later infants ride jockey style, as shown here by an older sifaka infant (Propithecus verreauxi), which clings to its mother (far left). Like their nonhuman primate counterparts, human neonates and infants prefer the closeness and proximity that is conferred during carrying in arms. Paternal behavior has been documented in Propithecus verreauxi and other strepsirrhines (Bastian and Brockman, 2007).

Figure 8.3. Monkeys generally maintain close bonds with other troop members, particularly in macaques and baboons. Baboon troops often include multiple females and multiple, but fewer, males. Baboon mothers and infants maintain close proximity and attachment during the first year to year and a half of life (Altmann, 1980). Neonates and young infants are carried on the ventrum for nursing on demand and for protection, whereas older infants ride jockey style on the dorsum. Males have been observed taking an active role in caretaking in many baboon species.

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Figure 8.4. Gorillas often form families comprising multiple females grouped to a single large silverback male. A gorilla female (a) can be half the size of a male (b), and carries neonates ventrally and older infants dorsally. Gorilla mothers must support infants with a hand during the first three months, and therefore walk tripedally until infants can successfully cling (Fossey, 1979). Gorilla fathers have been observed to allow older infants and juveniles to ride dorsally. The silverback regulates play behavior among immatures, which reduces serious injuries and socializes infants.

Comparison between Human and Chimpanzee Neonatal Growth and Cognition Chimpanzees (Pan troglodytes) are closely related to humans. A comparison of chimpanzee and human development trajectories can reveal a wide range of similarities in abilities of neonates and young infants in both taxa. For example, developmental milestones are present in the same sequence and occur roughly at about the same times during the first year in chimpanzees and humans. Profound developmental differences in the two taxa arise only during the second postnatal year when older human infants and young children begin to utilize spoken language and elaborate cultural behavior (Tomasello and Camaioni, 1997). Another difference is size. Chimpanzee infants are smaller in body size than human infants, and their brains are about half the size. These size differences affect caloric demands during gestation and lactation, parturition, and infant carrying. Chimpanzee infants make various vocalizations such as “hoos” in response to maternal cues (Falk, 2004). When chimpanzee infants are about three months old, they begin to intently examine the faces of their mothers (Goodall, 1986). Since chimpanzees, like humans, depend on facial expressions to convey meaning, this intense investigation of their caretaker’s face by infants serves as an enculturation tool. Although bonobos exhibit less verbal communication than do chimpanzees, sev-

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eral nonverbal cues are utilized. For example, bonobo mothers create a particular stance to indicate to infants that it is time to climb onto her for travel (Kano, 1990). Both chimpanzee and bonobo mothers play with their infants by lying prone and balancing their infants on their feet while holding their hands, similar to playing “airplane.”

Alloparenting Observations of close relatives, such as chimpanzees, provide insight into infant behavior of the last common ancestor of chimpanzees and humans (Pan and Homo, respectively), and possibly of all of the apes. Other nonhuman primates share similarities with humans in terms of infant behavior and mother-infant attachment. In addition, many nonhuman primates can be described as cooperative breeders. Cooperative breeding also characterizes human societies (Hrdy, 2009), encapsulated in the phrase “it takes a village to raise a child.” In nonhuman primates, cooperative breeding takes the form of alloparenting, such that other troop members participate in taking care of infants. In nonhuman primates, the most common form of alloparenting, or extramaternal caretaking, is exhibited by maternal siblings, juvenile females, and other adult mothers. These behaviors include grooming, carrying, as well as defending the infant from conspecifics and predators, and maintaining close proximity to the infant. In some small callitrichine New World monkeys, alloparenting also includes provisioning infants with insects and other fauna. In several colobine monkey species, a female will nurse another mother’s infant (Jolly, 1985). Alloparenting in nonhuman primates increases infant survival and affords mothers additional foraging and grooming opportunities. Infants are exposed to the social worlds of other troop members during their relatively long nursing period. Invariably infants become objects of curiosity, particularly for siblings and nulliparous females within social groups. These allomothers provide essential care in many primate species, including carrying and playing with infants. For example, in leaf monkeys of Africa and Asia and patas monkeys (Erythrocebus patas), females of the social group can approach a newborn within the day or week (MacKinnon, 2007). However, in some macaques such as Macaca fuscata, M. fascicularis, M. mulatta, and M. nemistrina, new mothers are reluctant to allow other troop members the opportunity to interact with or even approach a new born for several weeks to months. Females that allow other group members to approach and touch their newborns exhibit less extreme competition

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than those that do not. Among the great apes, which generally lack strong adult female-female bonding among kin and nonkin, alloparenting is expressed most often by the infants’ maternal siblings (Goodall, 1986).

Paternal Behavior Paternal behavior is another form of allomothering and is found in 40 percent of nonhuman primate species (Smuts and Gubernick, 1992). Sociality is an obvious pattern and is found in all of the major radiations of the nonhuman primates, although the role of males as direct caregivers has evolved only a few times (Fernandez-Duque et al., 2009). Among primates, paternal behavior occurs in conjunction with increased sociality and can occur in both the presence and absence of monogamy (Smuts and Gubernick, 1992). However, similar to other mammals, much of male caretaking in primates occurs most often in monogamous taxa (Atzil et al., 2012). Among nonhuman primates, the most intensive paternal behavior of infants occurs in Neotropical Callicebus and Aotus, which are primarily monogamous and live in small family groups (Fernandez-Duque et al., 2009). The paternal behavior of nonhuman primate species shows the importance and effectiveness of paternal behavior as a reproductive strategy. These include direct forms of care, such as carrying, grooming, and playing with infants, as well as food sharing in tamarins and marmosets. Passive forms of paternal behavior are much more widespread and include tolerance or indifference, defending infants from social adversaries and predators, and rescuing fallen infants (Smuts and Gubernick, 1992; MacKinnon, 2007). In capuchin monkeys of the genus Cebus, dominant males passively allow infants to secure the best foraging areas close to them (Jolly, 1985). In savanna baboons, putative fathers or “friends” of the mother often guard and defend infants (Clutton-Brock, 2016). The males of other primate taxa are known to protect vulnerable infants from conspecifics and predators (Muller & Emery Thompson, 2012). Strepsirrhine (prosimian) primates Father-infant proximity and carrying behavior is found across the order Primates, from some of the smallest to some of the largest species. Even strepsirrhine males are known to exhibit paternal behavior, although it is rare. For instance, slender loris males are noted to groom and play with parked infants. Sifaka (Propithecus verreauxi) males have

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been observed grooming and holding infants in the wild and captivity, with individual differences among males (Bastian and Brockman, 2007). In primarily monogamous black lemurs, Eulemur mongoz, adult males, presumably the fathers, participate heavily in infant carrying once the infant is at least two weeks old (Curtis and Zaramody, 1997). In red-bellied lemurs, Eulemur rubriventer, males will carry and hold infants during the first three to four months postnatally (Gould and Sauther, 2007). Infants parked in nests of fat-tailed dwarf lemurs (Cheirogaleus medius) are warmed and guarded by both male and female partners throughout the night (Fietz, 1999). New World Monkeys Paternal behavior occurs in several species of small Neotropical monkeys of Amazonia and subtropical South America. Noteworthy paternal behavior occurs in the small New World tamarin and marmoset monkeys (callitrichines) that normally birth relatively large sets of twins. Titi and owl monkey fathers provide considerable care to single infants, suggesting that this may be an ancestral trait of small neotropical monkeys rather than a feature related to twinning and postpartum estrus in callitrichines. A pronounced degree of paternal behavior occurs in several small monogamous neotropical primates such as owl or night monkeys of the genus Aotus and titi monkeys of the genus Callicebus. In monogamous dusky titi monkeys (Callicebus moloch), infants were more attached to their fathers than their mothers, particularly during the first six months postnatal (Mason and Mendoza, 1996). These monkeys live in small, often pair-bonded social groups, and the adult male of the group maintains significant contact with the infant, often soon after birth. Owl and titi monkeys are active caregivers to infants through play, grooming, and food sharing. A wild birth event of a titi monkey recorded the male touching and grooming the neonate three minutes postnatal (DeLuycker, 2014). The male manually cleaned and licked the infant within the first two hours, and within a day, the male carried the infant. The male was the primary groomer and carrier of the infant for the first four months postpartum. During the first two and half months, the male handed the infant to the mother only to nurse until the infant could direct nursing bouts independently, and the infant began to forage away from the male caretaker only after five months of close contact (DeLuycker, 2014).

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Owl monkey infants exhibit strong attachment and close proximity to their fathers, and approach their fathers for protection when frightened (Juárez et al., 2003). Owl monkey adults are known to change partners with some frequency, so the infant may not be related directly to the lone adult male of the group, although paternal behavior continues regardless. Oftentimes, however, if an infant is weaned and its father is evicted by a nonresident male, the infant will disperse with its father. Additionally, infants and fathers maintain a close relationship in owl monkeys as they mature into juveniles and subadults (FernandezDuque, 2007). Less intense paternal behavior is also noted in brown capuchins, in which infants older than two months are often left with the dominant male while the mother concentrates on foraging. In species of small neotropical primates, such as the tamarins and marmosets of the subfamily Callitrichinae, males approach newborn twins readily and begin to carry them extensively from the first day onward. In some taxa such as Saguinus oedipus (cotton-topped tamarin) and S. fuscicollis (saddle-back tamarin), fathers are primary caretakers of infants, except when infants nurse with their mothers (Goldzien, 1987; Savage et al., 1996). Among nearly all marmosets and tamarins, twins rather than single births are usually born. Each of the twins is relatively large with respect to maternal weight. Alpha female callitrichines (one per social group) are able to increase the frequency of reproduction by ovulating relatively shortly after birth (postpartum ovulation shortly after parturition), since much of the energetic obligation of carrying the twins is given to the father. The alpha female continues to provide milk throughout the six to eight months of lactation. Callitrichine fathers even participate in the delivery of their infants, becoming attached upon birth, accompanied by a rush of prolactin and a decrease in cortisol and testosterone, which may positively influence bonding with the infant. However, given the early postpartum ovulation typical of these small neotropical primates, testosterone levels can increase after parturition without a corresponding decrease in male care (Ziegler et al., 1996, 2000, 2004; Mota et al., 2006; Storey and Ziegler, 2016). Increased prolactin is produced by fathers in several New World taxa, such as owl monkeys (Aotus), titis (Callicebus), marmosets (e.g., Cebuella and Callithrix), and tamarins (Saguinas and Leontopithecus). Prolactin levels in neotropical callitrichine fathers, such as the common marmoset (Callithrix jacchus), double just after the birth of their first offspring (Schradin and Anzenberger, 2004) and remain high with sub-

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sequent births (Mota et al., 2006). These fathers thereafter participate extensively in paternal behavior, suggesting a hormonal profile and biofeedback loop is established (Mota et al., 2006). Prolactin levels also appear to modulate male paternal behavior in cooperatively breeding species of fishes, birds, and mammals (Schoech et al., 1996; Schradin, 2008). Old World Monkeys Male-infant proximity occurs in some Old World monkeys, such as Barbary macaques (Macaca sylvanus), Japanese macaques (Macaca fuscata), Tibetan macaques (Macaca thibetana), Rhesus macaques (Macaca mulatta), several savanna baboons, such as chacma and olive baboons (Papio ursinus and P. anubis, respectively), Hanuman langurs (Semnopithecus entellus), and others (van Schaik and Paul, 1996). Barbary macaques have an extreme interest in infants, and often utilize them as social devices to increase affiliative behavior with other males (Thierry and Aureli, 2006). For example, an infant may be carried when one adult male approaches another and groomed by both males as a prelude to direct adult male-to-male grooming (Deag, 1980; Ogawa, 1995). Juvenile, subadult, and adult male Barbary macaques have all been observed to approach the mother and, after appeasement gestures, such as presenting his lowered hind quarters, lip-smacking, or “teeth chattering” to her, gently gathers her infant (Daeg and Crook, 1971: 191). Sometimes males are the sole caretaker of an infant for up to twenty minutes. All males in the troop care for and look after infants, such as if a jackal attacks or if an infant is in distress. However, some males have particular preferences for certain infants and care for infants as young as a week old. Infants also initiate contact with males and rotate among males of their own accord (Daeg and Crook, 1971). Males carry young infants ventrally, older infants dorsally, and groom them when the group rests (Daeg and Crook, 1971). In Japanese and rhesus macaques, high-ranking males are often observed to engage in infant care such as grooming, carrying, and proximity, suggesting male-infant dyad formation influences or is a consequence of dominance, at least in provisioned troops (Alexander, 1970; Hill, 1986). Paternal behavior occurs in savanna baboons (Papio), particularly among males that have befriended specific females, regardless of actual paternity. It is the relationship between the males and their female associates, or friends, that predicts paternal behavior (Smuts and

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Gubernick, 1992). In a study of yellow baboons (Papio cynocephalus), paternal behavior was predicted more consistently by the existence of an affiliative relationship between the male and female friends prior to the birth of the infant than by paternity (Smuts, 1985). In chacma, or Cape baboons (Papio ursinus) of the Okavango Delta, male “friends” groom with, mate with, are proximate to, and come to the defense of certain females (Palombit et al., 1997). These males often touch and handle infants close to their female “friends” for a long duration, while emitting a context-specific grunt. Males carry these infants dorsally, and protect and socialize them (Palombit et al., 1997). Males of other Old World monkey taxa also contribute to infant care. For example, males of Colobus angolensis, black and white colobus leaf-eating monkeys of Africa, were noted to carry infants throughout five weeks of observation (Fashing, 2007). Paternal care in snub-nosed monkeys (Rhinopithecus bieti) ranges from nearly 4 percent to 1.6 percent of daily activity budgets, with greater direct male care occurring during the late winter. Males carry, groom, and hold infants while foraging—particularly young ones (Xiang et al., 2009). Barbary macaques, Japanese macaques, savanna baboons, as well as geladas (Theropithecus gelada) are known to utilize infants as agonistic buffers or a social tool (van Schaik and Paul, 1996). For example, in multimale/multifemale groups, when a resident adult male encounters a nonresident one, he may grab an infant and place it on his back, jockey style. Whether this is to protect the infant or enhance social positioning is unknown. What is clear is that the infant does not protest or scream for its mother, indicating a familiarity with and affinity for the resident adult male. Among Barbary macaques, the approaching, often subordinate, male presents the infant by lifting its hind quarters, to another, often dominant male (Daeg and Crooks, 1971). The behavior allows a subordinate male to be in the vicinity of a dominant one without risk of an attack (Daeg and Crooks, 1971). Japanese macaque males are able to use infant care to rise in the social hierarchy by avoiding attacks by dominant males while holding infants in the central part of the troop (Itani, 1959). Subadult male hamadryas baboons (Papio hamadryas) have been observed grabbing an infant to thwart aggression from larger males (Kummer, 1967). Gelada baboon (Theropithecus gelada) follower males appear to groom, carry, and hold infants to ingratiate themselves to the infants’ mothers and thereby improve their mating opportunities (van Schaik and Paul, 1996). Agnostic buffering

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and paternal care among Old World monkeys may be learned behaviors and are culturally transmitted within groups (Itani, 1959). Hominoid Apes Siamangs (Symphangus syndactylus) and, to a lesser degree, gibbons (Hylobates spp. and other genera) exhibit substantial paternal behavior after infants are older than one year (van Schaik and Paul, 1996; Fernandez-Duque et al., 2009). Siamang adult males as well as juveniles carry infants extensively (Chivers, 1974; Bartlett, 2007). Paternal carrying may greatly exceed that of the mother after ten months postnatal, particularly in monogamous groups (Lappan, 2008). Males also play with and socialize juveniles, and are observed to share sleeping sites with them once the mother gives birth to a new infant; meanwhile, the other group members sleep separately. These juveniles continue to benefit from the relationship developed with males while they were infants (Lappan, 2008). Carrying behavior and playing with infants has also been observed in gibbons (Bartlett, 2006). Paternal behavior has been documented in great ape males, most notably in western lowland gorillas (Gorilla gorilla gorilla) and mountain gorillas (Gorilla beringei beringei). For instance, mountain gorillas are highly tolerant of infants and are known to nest with orphans (Stewart, 2001; MacKinnon, 2007). During the first two to three years, gorillas are in direct contact with or in close proximity to their mothers. As infants experience greater independence during this period, they spend increasingly more time with the silverback male of the group, often riding on his back and tumbling on him as a form of play behavior (Fletcher, 2001; Robbins, 2007). A chimpanzee male was noted to adopt a weaned orphan when the mother died (Goodall, 1986). This has also been observed in wild bonobos (Ellen Ingmanson, personal communication).

Primate Sociality and Brain Growth The relatively large brain size of nonhuman primates may have arisen from selection for intense sociality, which would facilitate increased cohesion of groups. Group size would have additional benefits for predator-detection systems and foraging efficiency (Dunbar and Shultz, 2007). Growing a large brain with respect to body size requires a lengthening of life history stages, particularly the infant and juvenile periods, when neurological structures develop. Furthermore, the size of the neocortex with respect to total brain volume has a direct rela-

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tionship with the number of individuals within a social group (Dunbar, 1992, 1998). Nonhuman primates that exhibit a relatively large neocortex tend to form grooming relationships, the members of which are later recruited as partners in social disputes (Kudo and Dunbar, 2001). These nonhuman primates also tend to show a greater ability to deceive group members (Dunbar and Shultz, 2007). Enhanced cognitive abilities allow lower-ranking males to circumvent dominance hierarchies through the formation of coalitions and to provide opportunities for females to exercise mate choice (Pawlowski et al., 1998). Nonhuman primates with a large relative brain (and neocortex) size exhibit intensive social play during maturation (Lewis, 2000). With respect to other primates, humans can be described as hypersocial. Humans are adept at maintaining large cohesive social groups, and are masters of deception and manipulation. This is expressed as frequent and immersive social play in infancy and childhood. Humans are bonded through complex social behaviors, such as language— arguably a substitute for the social grooming of nonhuman primates (Dunbar, 1992, 1998). Salient fathers can enhance the sociality of human infants, but that does not mean it is fully necessary in some contexts. Nonetheless, it is the contact, physical proximity, and carrying by both males and females of a pair-bond that best replicate the conditions in which humans evolved. The human brain grows rapidly after birth, in contrast to nonhuman primates, which experience rapid prenatal brain growth but much slower postnatal expansion of brain tissue. The net result is that nonhuman primates experience brain growth primarily during gestation, whereas most of human brain growth occurs in the social extrauterine world. This difference between humans and nonhuman primates can be demonstrated by comparing growth in cranial capacity in humans, chimpanzees, and baboons (Figure 8.5). The first three postnatal years in humans is a period of extensive brain growth corresponding to the development of walking, talking, and hypersociality. Other primates exhibit a shorter period of postnatal brain growth (Figure 8.5), although it is larger than that of most other vertebrates. Human neonates weigh about twice that of the great apes, and the head contributes heavily to this total (Martin, 2013). Neonatal human brains are relatively large, with an average of about 375 grams, and range from 255 to 540 grams, compared to those of chimpanzees, with a mean of approximately 151 grams and a range of 109 to 181 grams (DeSilva and Lesnik, 2008). Furthermore, humans experience a

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much greater increase in white matter during the first three postnatal years compared to nonhuman primates (Schoenemann, 2013). Chimpanzees exhibit a much less dramatic increase in brain size from birth to three years. By three years, chimpanzees have achieved 90 percent of brain growth. In baboons (Papio spp.), the cranial capacity of young infants nearly approximates that of adults (Pereira and Leigh, 2002). In humans, the proximity of infants and caregivers during the years coincident with rapid brain growth has short- and long-term effects on neurological, psychosocial, and physiological development into adulthood (Gray and Anderson, 2010; Champagne, 2014; Halton, 2014).

Figure 8.5. Growth of cranial capacity in humans, chimpanzees (Pan troglodytes), and baboons (Papio spp.) across the first three postnatal years. The equation for cranial capacity is the product of cranial length, breadth, and height raised to the power of a coefficient. This coefficient for Papio (0.38105) was experimentally derived using a combined P. ursinus / P. anubis sample of 70 individuals (unpublished data) and a mean of 155 cm3 for the cranial capacity of adult Papio (Schoenemann, 2013). The coefficient for Pan (0.4218) was also experimentally determined using a sample of 156 individuals (Williams et al., 2002, 2003) and mean of 368 cm3 for adult Pan (Schoeneman, 2013). The coefficient for humans (0.5238) is from Dekaban (1977).

3 Evolutionary Perspectives

9 The Evolution of Carrying Behavior Muscles and bones of the forearm bear a crucial role in supporting the weight of infants held in arms. Carrying infants is only possible when the arms and hands are not involved in locomotion. In this regard, the anatomy of bipedalism allowed for infant carrying in humans to evolve. Alternatively, perhaps long-term infant carrying actually necessitated bipedalism. A number of scholars have described human bipedalism and its anatomical correlates. The pelvis of bipeds shows an ilium bending back toward the sacrum and must have occurred as a distinct novelty, rather than as a juvenilized or adultified version of an apelike pelvis (Williams and Orban, 2007). Carrying may have been particularly important to early apelike human ancestors. Perhaps infants were incapable of mastering the complexity of bipedal locomotion until up to a year, like in modern humans. During group movements, or in the presence of predators, males might have carried young children. Eventually, pair-bonds within a larger social group may have adopted the trait as a behavior that enhanced the survivorship of infants. There are numerous theories available to explain bipedalism, including the savanna hypothesis, man the hunter, woman the gatherer, aquatic ape hypothesis, radiator hypothesis, sexual display, seed-predation and terrestrial-feeding strategies, among others. Squat foraging and scaling the ground for edible roots and insects may have been a precursor to bipedalism, eventually freeing the hands from their locomotor roles (Kingdon, 2004). The idea that bipedality freed the hands to make tools and carry them around is probably not correct because stone tools appear some one to two million years after bipedalism evolved. However, carrying infants may have significantly lowered mortality risks, positively influencing their survival.

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The discovery of Australopithecus demonstrated that bipedalism emerged at least 3–4 Ma, and evidence of early australopiths dating to 6–7 Ma, such as Sahelanthropus tchadensis, suggests bipedality was well underfoot by the late Miocene era (Wells and Stock, 2007). The evolution of larger relative brain sizes beginning approximately 2 Ma was accompanied by an increasingly longer developmental period for juveniles (Smith, 1991), albeit this was distinctly shorter than in modern humans (Dean et al., 2000). Such a profoundly long maturation interval among ancient hunter-gatherers likely provided plenty of impetus for extensive infant carrying. Running, which recruits the enlarged human gluteal muscles, occurred in long-legged Homo erectus from less than 2 Ma (Bramble and Lieberman, 2004). The degree to which these ancient bipedal males carried their infants may be difficult to reconstruct. However, with their arms free from the constraints of locomotion, they certainly could have carried infants. The stresses involved in manual infant transport among bipeds can be assessed by examining the movement of the legs and muscles involved in bearing the weight of infants held in arms.

Functional Constraints Habitual bipedalism involves the function of the muscles and bones of the hind limbs. When habitual bipedalism evolved, a foot devoted to clinging was transformed into a weight-bearing appendage with the added responsibility of steering the body. The repositioning of the head and trunk, from horizontal to vertical, necessitated the evolution of trunk stabilizers and increased pelvis to rib musculature. The shape of the rib cage eventually changed from a more funnel shape characterizing the apes to a barrel form typical of humans (Aiello and Wheeler, 1994). More fundamentally, however, selection for a longer back, as opposed to the short back of apes, reflected the need for hip rotation to occur unimpeded by a wide rib cage. The human skeletomuscular system is adapted from that of a fourlegged ancestor with all limbs positioned underneath the body (Cartmill and Smith, 2009). Advantages for two-legged, or bipedal, locomotion are not immediately apparent in this difficult-to-learn, precarious form of movement. Bipeds are always teetering on the edge of falling, lacking a tail for balance. Much of the time, there is very little contact between the soles of the feet and the ground, particularly with increasing speed. Four-legged mammals, including terrestrial and arboreal quadrupeds, have inherently better balance, speed (at least at short intervals), and

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power, and consequently, the arms and legs of many quadrupeds are similar in length, such as in ungulates and carnivores (Hildebrand, 1988). In chimpanzees and other brachiators, which move efficiently using arm swinging, the arms are longer than the legs. Bipeds, on the other hand, exhibit vast differences in the lengths of the limbs but in the opposite direction, the legs being noticeably longer than the arms (Figure 9.1). A further reduction of the relative lengths of upper to lower limbs (humerus to femur) and the lower to the upper arms (forearm to humerus) may be an adaptation to increased efficiency in carrying

Figure 9.1. Proportional length differences exist between a human upper leg bone, or femur (a), and upper arm bone, or humerus (b), compared to that of a Pan troglodytes (chimpanzees) femur (c) and humerus (d). In apes, the upper arm bones are slightly longer than the upper leg bones, whereas in humans, the femur is much longer than the humerus. Human legs transmit loads from the trunk and arms during static and dynamic postures, while the arms are nonlocomotor and available for other uses, such as carrying. Infant carrying in early humans (hominins) would have provided them with protection from parasites, predators, and hypothermy, and would have enhanced sociality. Scale bar is in centimeters.

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objects. The Nariokotome skeleton of early Homo erectus from 1.6 Ma presents a very short arm compared to leg length, suggesting mechanical efficiency from arm-swinging could only be accounted for by the carrying of objects, such as tools, weapons, food, and infants (Wang et al., 2003; Cartmill and Smith, 2009). Habitual bipedalism must be learned from one generation to the next. Social and environmental knowledge would accumulate in any animal that evolved an elongated maturation process (Gould, 1977). However, until a fast rate of brain growth after birth could evolve, a bipedal pelvis constrained the absolute dimensions of adult brain size. A rapid postnatal (or extrauterine) rate of brain growth may have occurred rather late in human evolution (Gruss and Schmitt, 2015). This has important implications for understanding the evolution of human life history, the emergence of a division of labor based on age and sex, regular food sharing, and patterns of cultural behavior (Lancaster and Lancaster, 1983). Such cultural traditions of learning bipedal locomotion may have arisen with Australopithecus afarensis, represented by the famous “Lucy” fossil from Ethiopia, dated to the middle Pliocene (about 3.3 Ma). These cultural traditions continued in Australopithecus africanus, evidenced by Sts 14 from Sterkfontein Member 4, dated to 2.58 to 2.16 Ma (Herries and Shaw, 2011; Figure 9.2). The smaller anterior-to-posterior dimensions of the pelvis in smaller-brained Australopithecus differ from those of humans (Gruss and Schmitt, 2015). However, A. afarensis, like H. sapiens, had relatively large infants compared to those in P. troglodytes (chimpanzees) and earlier apelike hominins (DeSilva, 2011). In humans, the ratio of mother to infant weights is about 6 percent. Those of A. afarensis have been reconstructed as about 5 percent, whereas those of P. troglodytes are about 3 percent (DeSilva, 2011). These differences suggest that early bipeds would have benefited from pair-bonding and cooperative breeding to assist in carrying such large infants safely in arms during bipedal locomotion.

Anatomy of Bipedalism The pelvis of Australopithecus is compressed anteriorly to posteriorly (front to back) but flares greatly in a lateral direction (Lovejoy, 2005). By any measure, Australopithecus had an exceptionally broad pelvis. The bones of the pelvis in Australopithecus are more similar to those of modern humans than to those of the great apes (Figures 9.2 and 9.3). Chimpanzees, gorillas, and orangutans exhibit a tall upper hip bone,

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or ilium, whereas that of bipeds, including Australopithecus and modern humans, is characterized as short and broad and is separated from the ribs, forming a “waist.” The ilium of apes is oriented more toward the back, whereas it curves from back to front in bipeds (Williams and Orban, 2007). In bipeds, the short and broad ilium supports the gluteal muscles posteriorly, and serves to anchor the flexors of the thigh anteriorly. The ilium in bipeds is essentially bent posteriorly toward the ischium, the lower pelvic bone, creating the sciatic notch, which the apes lack. Bipeds also have a relatively long pubis (front-facing pelvic bone) to position the hip laterally (particularly in Australopithecus) so that the femoral head, or thigh-hip joint, is displaced away from the center of gravity of the lower trunk. The acetabulum, or hip joint, is relatively larger in bipeds to receive the weight of the upper body without the assistance of the forelimbs. The wide hips of Australopithecus and other ancient hominins would have provided a supporting structure upon which to rest older infants while carrying them. It is possible that bipedalism in Australopithecus consisted of fast and slow walking using a waddling gait. This may have been an efficient form of walking in uneven terrain (Cartmill and Smith, 2009). The pubis is absolutely and relatively longer in Australopithecus than in humans, further hinting at the efficiency of bipedalism in australopiths (Williams and Orban, 2007). Like most quadrupeds, apes present a short, thin, and delicate pubis, which provides less stability compared to the thicker and longer bony strut characterizing the pubis of humans and ancient bipeds (Figures 9.2 and 9.3). Adaptations to bipedalism include a short wide sacrum, or bony false vertebrae between the two pelvic bones. In this way, the sacrum forms the back of the pelvis. In apes, the sacrum is long and narrow. The short, broad sacrum maintains a distance between the two pelvis bones, providing more structural support by enlarging the lower trunk (Figure 9.2). Bipeds are also knock-kneed such that the distal femur, or lower portion of the thigh bone, is positioned below the pelvis. The tibial condyles, forming the lower knee joint, are broad to withstand the weight of the entire body, since the fibula, or outer lower leg bone, does not bear significant loads. The large size of the calcaneus, or heel bone, in bipeds also differs from the smaller ones found in nonhuman primates and other mammals, although it is larger in the apes than in monkeys. The strong big toe, or hallux, of bipeds does not diverge from the other digits as it does in nonhuman primates (Figure 9.4). The horizontal and

Figure 9.2. The Sts 14 partial skeletal attributed to Australopithecus africanus is shown with the Sts 5 cranium. Like A. afarensis, Sts 14 exhibits a pelvis that is wide anteroposteriorly and short superoinferiorly. The femur, or thigh bone, is angled inferomedially to place the knees directly under the center of gravity during bipedal locomotion. The broad superior sacrum articulates with a long lumbar portion of the back typical of bipeds and atypical of the apes. The placement of Sts 14 together with Sts 5 was created by Francis Thackeray for a press release announcing the possibility that the two may belong to the same individual.

Figure 9.3. Comparison of pelvic bones of (a) Australopithecus africanus, an early human-like form; (b) Homo sapiens; and (c) Pan troglodytes (chimpanzee). The pelvis of A. africanus resembles that of H. sapiens, but at a smaller size and with a longer relative superior pubic ramus. Apes differ from bipeds primarily in the elongated vertical strut of the ilium that provides support for epaxial muscles of the back during quadrupedal locomotion. The iliac blades in bipedal A. africanus and H. sapiens are much shorter and wider front to back (anteriorly, posteriorly), allowing the hips to partly bear the weight of an older infant held in arms. Scale bar is in centimeters.

Figure 9.4. Human feet have an alignment of the (a) hallux (big toe) with the other pedal digits. Note the thickness of the bones of the hallux in comparison to the other digits, which provides propulsive action during the push-off of bipedism, while the enlarged (b) calcaneus or heel bone offers stability to the foot during the landing stage, or heel strike. Scale bar is in centimeters.

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transverse arches in the foot of bipeds absorb the impact of loads and transmit force from the calcaneus along the lateral margin of the foot, then to the ball of the foot, and finally through the hallux and, to a smaller degree, through the other toes. Bipedalism has also impacted the form of the spine. Most other living and extinct bipedal animals, such as kangaroos, birds, and Tyrannosaurus rex, have tails. But since apes lack tails, early bipeds could not inherit this efficient means to counteract propulsive forces during bipedalism. Instead, the spine assumes a lazy S curvature. The bend in the cervical/thoracic (neck/back) region is slight compared to the particularly pronounced curvature of the lumbar vertebrae of the lower back and sacrum. The foramen magnum at the base of the cranium is positioned anteriorly, or more front-facing, to be closer to the center of gravity of the skull, and the occipital condyles—where the cranium meets the first cervical vertebra—are somewhat flattened and elongated.

Carrying Infants and the Evolution of the Forearm Carrying infants is cumbersome without habitual bipedalism. Infant carrying is common in non-Westernized societies. Foragers carry their infants most of the time for the first several years (Konner, 1977; Blurton Jones et al., 1989; Wall-Scheffler et al., 2007) and for up to five years during travel (Hill and Hurtado, 1996). Manual infant transport occurs in both sexes (Hewlett, 1991; Endicott, 1992) and is costly (Wall-Scheffler et al., 2007). As selection for encephalization intensified, infant body sizes also increased. The alignment of the hallux with the other digits limited the degree to which infants could engage in pedal clinging, as possibly demonstrated by DIK-1–1 (Alemseged et al., 2006). Darwin (1871) was the first to note that bipedalism freed the hands, allowing for nonlocomotor uses to evolve. Other innovative uses for the hands may have been harnessed—namely those related to communication, carrying food, tools, and weapons, display, food procurement, or assisting with arboreal postures. Manual infant transport may be added to this list because it may have directly increased the survivorship of early human infants. African ape mothers carry their infants for the first three months because the infants are unable to cling. It is reasonable to assume that early hominin neonates would have been unable to cling for a similar or longer period of time. Manual infant transport would have been adaptive, given the constraints of hair shaft thickness and the tensile forces generated from the carrying of australopith infants perpendicular to the ground. In fact, the

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constraints of infant weight transmission from clinging to the body hair of early bipeds would have virtually necessitated the evolution of carrying behavior (Amaral, 2008). Manual infant transport would exert pressures on the forearms, as well as on the posterior curvature of the upper hip bone (ilium) and the distance between the superior margin of the ilium and the twelfth rib. The mechanical efficiency of infant carrying has been explored by Cara Wall-Scheffler and colleagues (2007). Assisted infant transport, using carrying devices such as slings, is significantly more efficient than manual transport. Slings may have been utilized by the earliest hominins (Hrdy, 2009; Falk, 2009), or may have occurred later as improvements in technology during the early Pleistocene allowed for animal skins to be incorporated into the behavioral repertoire of early members of the genus Homo. The earliest infant carriers would not be preserved, but manual infant transport most likely preceded the use of carrying devices. The tensile forces produced by a growing infant should be reflected in joints bearing the most direct biomechanical strain—namely the elbow and wrist. With selection for encephalization, infants became larger with respect to adult body weight, further shaping the dimensions and form of the forearm, including (1) decrease in the proportional length of the forearm; (2) modification of the elbow and wrist joints; (3) the alignment of the radius with the ulna, the two bones of the forearm; and (4) the formation of the interosseus crests, which are muscle insertion sites that form along the facing borders of the radius and ulna, from which the long flexors and extensors of the hand arise (Figure 9.5). The radius and ulna of Australopithecus afarensis (A.L. 288–1) are humanlike in their lack of shaft curvature (Johanson et al., 1982: 437; Drapeau et al., 2005). The alignment of the radius with the ulna in humans, in contrast to hominoids, produces a platform upon which infants can be positioned. A.L. 288–1 shows an enlarged insertion of brachialis and the pronator teres muscles like those of humans (Johanson et al., 1982); these muscles are intimately involved in infant carrying, with the weight borne by the forearm. The slight but still present interosseus margin is evident in A.L. 288–1 and humans, but not the great apes, and may have emerged to withstand tensile forces from the weight of infants that would load on the lower forearm bones, operating to separate the radius and ulna from one another during supination (Figure 9.5).

Figure 9.5. Forearm bones include the ulna, shown (a) laterally and (b) superiorly, and (c) radius, shown superiorly; these two bones provide a cantilever to support the weight of infants during manual infant transport. The rather short and broad articular surface of the trochlear notch that accommodates the distal humerus characterizes humans and most fossil hominins, but not the apes. Scale bar is in centimeters.

Figure 9.6. Brachial proportions of humans (H. sapiens), fossil hominins, and the great apes, including gorillas (G. gorilla), chimpanzees (P. troglodytes), and orangutans (P. pygmaeus), demonstrate the relatively short forearms with respect to the upper arms characterizing bipeds, presumably as an adaptation to carrying objects, such as infants. Data are from Cunningham (2005).

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Figure 9.7. The brachial index (radius length/humerus length) shows differences between bipeds, including H. sapiens and fossil hominins and the great apes. The index of Gorilla, the most terrestrial of the apes, is similar to that in humans, although at a much larger size. Australopithecus sediba resembles H. sapiens in its brachial index, whereas A. garhi is decidedly chimpanzee-like. Circles represent means and lines approximate 95% confidence intervals. Data are from Trinkaus (1981), Richmond et al. (2002), Cunningham (2005), and Churchill et al. (2010).

A shortening of the brachial index (radius length / humerus length) decreases the load arm (radius) and minimizes bending energy. Brachial proportions, expressed as a comparison of radius and humerus lengths (Figure 9.6), or the quotient of radius and humerus lengths (Figure 9.7), can be explored across fossil hominins to identify the range of variation in lower to upper forelimb bone lengths across time. There are only a few fossils available to compare to apes and humans, and these include H. erectus, which falls within the distribution of H. sapiens (modern humans), while Neandertals exhibit an extreme human brachial index with a reduction of radius length with respect to humerus length, perhaps indicative of an adaptation to cold stress corresponding to Allen’s rule (Trinkaus, 1981). One reconstruction of H. habilis shows a humanlike form, whereas another is more apelike (Richmond et al., 2002). Australopithecus garhi exhibits chimp-like brachial proportions, suggesting little infant carrying (Figure 9.7). The forelimb of Australopithecus afarensis specimen A.L. 288–1 is relatively well preserved.

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The short brachial proportions of this early human form suggest infant carrying may have been an adaptation coincident with the evolution of bipedalism (Williams et al., 2015).

Skeletal and Muscle Anatomy of Infant Carrying Various muscle systems are required for infant carrying, such as those of the neck, back, upper and lower limbs, abdomen, and pelvis. The musculature of the shoulder that traverses the scapula, proximal humerus, and the chest are also involved in carrying infants. For example, the pectoralis muscles act in opposition to the weight supported by the forelimb. However, the greatest intensity of loading actually occurs along the lengths of the forelimb bones and the joint surfaces of the elbow and wrist (Williams et al., 2015). The elbow serves to withstand the bending energy of the lower forearm upon which the infant rests, while the humerus must remain slightly flexed to bring the center of infant weight underneath the shoulder joint for greater efficiency. Biceps brachialis and biceps radialis are the two muscles that encounter exceptional loads during infant carrying. Biceps brachialis originates on the humeral head proximally and subsequently forms a relatively large muscle body before inserting on the upper radius at the radial tuberosity, while biceps radialis originates at the outward extreme of the lower humerus, called the lateral epicondyle, and is the largest muscle body of the forearm, inserting along the interosseous crest between the radius and ulna, and on the surface of the lower radius. However, the pronator and supinator muscles, along with the long and short flexors of the hand, are also recruited during manual infant transport. Extreme pronation or supination is associated with increased loading pressure (Bade et al., 1996). During infant carrying, the forearm is semisupinated, possibly to counteract joint strain related to bending energy. Bending energy derives from loads encountered by long bones, which are compressive on the front (anterior) and tensile on the back (posterior) of both the radius and ulna during infant carrying. A decrease in the relative length of the radius decreases potential bending energy while carrying infants. Since these forearm traits are found in both males and females, both are well adapted to carry infants (Williams et al., 2015).

10 Hyper-encephalization of Neonates

By being proximal and familiar, fathers and other family members become part of the social group of infants (Hrdy, 2009). Sociality promotes learning, enhances symbolic memory, and is vital in the acquisition of language and complex cognitive processes (Fitneva and Matsui, 2015). Although the material culture and behavior of modern humans is drastically different from that experienced by ancient families, the biology, desires, and interests of infants are perhaps remarkably similar to those in previous time periods (Fuentes, 2014; McKenna, 2014; Morelli, 2014). Culture can change quite rapidly, even within a generation or two. Biology changes much more slowly, over thousands, tens of thousands, hundreds of thousands, and millions of years, given the passive role of natural selection and the vagaries of the environment. Infants during the first six postnatal years can be described as highly encephalized, in that they exhibit a large observed versus expected brain size typical for mammals. It is no coincidence that most innovation, play behavior, and learning of social behavioral patterns occurs during a time period when the brain-to-body ratio is extreme. Play behavior prepares the brain to learn higher-level cognitive processes. Learning is enhanced by social proximity to a known caretaker (Kuhl, 2007), including when infants are carried or proximate when solving problems (e.g., puzzles). Showing interest in infants enhances their motivation to learn and provides a context for the exchange of information involving visual, auditory, and nonverbal communication during the communicative interaction between individuals (Kuhl, 2007). Physical contact with trusted caregivers, such as the parents, and in particular the mother, increases metabolic efficiency, temperature regulation, and weight gain of human and nonhuman infants, all of

Figure 10.1. Infants form close attachments to trusted caregivers early in postnatal ontogeny, as demonstrated by this young infant who is grasping at her father’s shirt sleeve as he carries her.

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which enhances growth (Champagne, 2014). Human infants, like their nonhuman primate counterparts, form a social attachment to primary caregivers (Figure 10.1). This social bond lasts throughout life when circumstances permit (Dettmer et al., 2014). Attachment bonds with caregivers provide infants with the ability to trust others, and trust is a key pillar of all social relationships. .

Social Attachment Attachment theory argues that if children have a trustworthy and conscientious caretaker, they are able to explore the social and physical world more effectively than if care is inconsistent or unreliable (Morelli, 2015). Attachment of infants to their mothers is universal, while close relationships with others are suggested to be secondary, to develop later, and to be weaker or inconsistent. Those who exhibit poor attachment to their caregiver are prone to behavioral disruptions later in life. It has been posited that even one-year-old infants have the capacity to become attached (or not) to their caregivers (Valentino et al., 2014). The reason for this delay in attachment, or why it is not experienced at birth, is the infant must be able to conceptualize himself or herself as a separate entity, as an individual independent or apart from all others (Morelli, 2015). According to attachment theory, this independence provides young infants the confidence to begin exploring their immediate environment. At the same time, the infant must be able to grasp the interdependence of individuals within a group. The infant-caretaker attachment forms by conceptualizing the self as responsive and connected socially to another. A strong attachment forms from long-term feelings of security, whereas weaker attachments arise from a lack of consistency in sensitive care (Valentino et al., 2014; Morelli, 2015). Among foragers, such as the Efe, infants are called upon to adapt to multiple caregivers who can range from nine to twenty different individuals over a few hours. Over time, infants form attachments to several of them (Morelli, 2015). When resources are unpredictable, and there are widespread extrinsic dangers and high rates of mortality, infants must quickly assess and adapt to new social situations, and often to new caretakers. The formation of attachments helps Efe infants survive in these variable social landscapes (Morelli, 2015). The Efe example shows that attachment is culturally constructed, given the variation in the number of individuals with whom infants are attached.

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Much of the care for children is provisioning, which both parents and other group members ultimately provide after the exclusive breastfeeding period. Among the Papua New Guinean Murik foragers, “food is the quintessential expression of relatedness, caring, and belonging” (Barlow, 2013: 107). Indeed, social attachment and its relationship to food are evident across cultures (Morelli, 2015). Positive tactile contact between infants and caregivers is also essential to the development of an attachment bond. Cognitive attachments and interdependent relations between individuals can readily form in such a large-brained species as Homo sapiens. These attachments may have been important during human evolution as sociality became essential for survival.

Why Did Large Brain Size Evolve in the Genus Homo? Human infants are heavy and require considerable care. Carrying by fathers (or others) could have greatly reduced the caloric loads required of lactating females, freeing valuable nutrients for infant brain growth. The amount of high-quality protein needed to provision large-brained infants and young children may have selected for regular scavenging and/or hunting combined with gathering, food sharing, pair-bonding, and cooperative parenting within small foraging societies (Lancaster and Lancaster, 1983). One possible explanation for why human ancestors evolved large brains is the emergence of higher population densities and the need to internalize the social status of an increasingly larger number of individuals, as well as the social relations among individuals—a multivariate problem. Selection for increased brain size around 2 Ma may have also been selected for by environmental perturbations (Vrba, 1994; Bobe et al., 2002). Another potential driver of human encephalization is the need to utilize ecological information for subsistence (Milton, 1988). Extractive foragers such as chimpanzees and gorillas utilize nearly 150 species of plants and are highly encephalized compared to most other nonhuman primates (Head et al., 2010). Capuchin monkeys (Cebus spp.), orangutans (Pongo pygmaeus), and aye-ayes (Dabentonia madagascariensis) all provide examples of an association between encephalization and extractive foraging (Robson et al., 2006). Some of the most encephalized nonhuman primates are associated with tool use and manipulative capabilities. Larger relative brain size appears in concert with increased capabilities for social learning, cultural transmission of information, and

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longevity in nonhuman primates, long-lived birds such as corvids and parrots, and cetaceans such as toothed whales (Street et al., 2017).

Emergence of the Genus Homo in the Fossil Record Brain size began to increase beyond that observed in the great apes during the evolution of the genus Homo. The earliest evidence for the genus to which humans are classified (Homo) occurs first in East Africa and at a later date is found in South Africa and Eurasia, and attributed to H. habilis and H. rudolfensis, which have relatively small brains, with the exception of KNM-ER 1470. A much larger cranial capacity is found in H. ergaster and H. erectus, although considerable variation is present. In comparison, Australopithecus exhibits a brain size only slightly larger than that of the living great apes, measuring about one-third of that characterizing Homo sapiens. In contradistinction, KNM-ER 1470 had a brain size that was about one half that of modern humans (Leonard et al., 2007). Early Homo dates to 2.4 Ma, but more complete fossils range from 1.9 to 1.6 Ma, and include KNM-ER 1813, KNM-ER 1805, KNM-ER 1470, and slightly later, KNM-ER 3733, KNM-ER 3883, and KNM-WT 15000 (Cartmill and Smith, 2009; Figure 10.2). Remains of early Homo are also found at Dmanisi (Republic of Georgia) and Java (Indonesia). Later Homo erectus (or Homo ergaster) may have evolved rather quickly from early Homo, as only a few hundred thousand years or less separate the emergence of the two taxa (Leonard et al., 2007; Wells and Stock, 2007). A further increase in brain size occurred about 400,000 years ago when archaic H. sapiens (or Homo heidelbergensis) evolved from an H. erectus–like ancestor (Figure 10.3). The pelvic inlet of early bipeds could not afford to expand broadly to birth large-headed infants without compromising the mechanical efficiency of bipedality (Gruss and Schmitt, 2015). Therefore, a large brain size would have to develop outside of the womb. This rapid postnatal growth of the brain evolved, which mimics the rate of brain growth during the prenatal period and allowed for the efficiency of bipedalism to be maintained without increasing the size of the pelvis. Rapid postnatal brain growth may have been selected for during the emergence of the genus Homo or perhaps during the evolution of H. erectus. The pelvis of 1.6-million-year KNM-WT 15000 from Nariokotome is similar to that of Australopithecus, given that it is relatively constricted anteroposteriorly. However, a 900,000-year-old pelvis attributed to Homo erectus demonstrates that a capacious pelvis had evolved by the

Figure 10.2. Comparison of brain size and form in early Homo and Homo erectus (sensu lato). In the early Homo fossil KNM-ER 1470, shown (a) anteriorly and (b) laterally, the brain size is about one half that of modern humans, although the face is demonstrably large and apelike, whereas in KNM-ER 1813, shown (c) anteriorly and (d) laterally, a smaller brain size exists, but cranial shape is similar to that of later Homo. In a H. erectus fossil from Zhoukoudian cave, China, shown anteriorly (e) and laterally ( f ), and in H. erectus (or H. ergaster), KNM-ER 3733, shown anteriorly (g) and laterally (h), the brain size is about three-fourths the size of adult modern humans, albeit with stronger craniofacial superstructures. Scale bar is in centimeters.

Figure 10.3. Comparison between the crania of (a) La Ferrassie (Neandertal) from about 50,000 years ago and (b) KNM-ER 3733 (Homo erectus, sensu lato), dated to approximate 1.78 Ma, and demonstrates the increase in brain size that occurred during the Pleistocene. Scale bar is in centimeters.

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middle Pleistocene period (Simpson et al., 2008). Thus an extension of fetal rates of brain growth into the postnatal period must have occurred between 2 and 1 Ma.

Fetal and Postnatal Rates of Brain Growth In modern humans, fetal rates of brain growth during the last trimester are approximated by the brain growth rate of the first three postnatal months, such that human neonates can be described as extrauterine embryos. This so-called fourth trimester is valuable because of the absolute gain of brain tissue involved at a time when the body remains small and the brain-to-body-size ratio is larger than at any other period of postnatal ontogeny. However, the extension of fetal brain growth rates is not uniform. The pre- and postnatal growth of the frontal bone differs from other cranial regions, while the parietal shows relatively slower postnatal growth than other dimensions of the cranial vault (Figure 10.4).

Figure 10.4. A marked increase in brain tissue postnatally may be the result of an extension of fetal rates of brain growth into the first year of life. However, it is the rate of brain growth during the last trimester that is mimicked during the first three postnatal months, as fetal growth rates for cranial capacity are significantly different from those during the first postnatal year. Rates of growth of cranial capacity were inferred from the slope values of the linear regressions for prenatal remains and infants, and significant differences at the 95% confidence limits were identified using an analysis of covariance. Prenatal cranial capacity = 6.598 + log age × 4.986; neonatal cranial capacity = 6.248 + log age × 1.102.

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Fetal and neonatal rates of brain growth can be estimated by comparing cranial capacity against age (Figure 10.5). The cranial capacity of human neonates is 26 percent to 28 percent of adult size (Robson et al., 2006; Halton, 2014). In comparison, chimpanzees are born with brain sizes that are 30 percent to 39 percent those of adults (Robson et al., 2006). In humans, by the first year of life, about 50 percent to 60 percent of adult brain size is achieved. During this period of rapid human brain growth, the myelination of neural networks develops to enhance the exchange of signals (Robson et al., 2006). The rapid increase in cranial size during gestation and early infancy continues but at a slightly lower rate during the first year postnatal to 18 months. After 18 months, the rate slows again but continues to three years and beyond (Figures 10.5 and 10.6). This period is coincidental with lactation which ceases between 2.5 and 3 years in most non-Westernized cultures (Bogin, 2006). Brain growth cessation in nonhuman primates and other mammals also corresponds to weaning (Robson et al., 2006). In contrast, weaned children still exhibit cranial capacity growth, albeit at a slower rate, between three and six years (Figure 10.6).

Figure 10.5. Human brain growth as reflected in cranial increasing capacity growth is profound during the prenatal period and the first postnatal year. Cranial capacity, derived from the product of cranial length, breadth, and height by a coefficient (0.5238), is compared across age in thirty-nine human fetuses and infants (Williams et al., 2002, 2003). The formula for cranial capacity is from Dekaban (1977).

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Figure 10.6. Rates of cranial growth are significantly slower for postnatal infants and young juveniles to seven years, suggesting that while human brains increase substantially in size during the first postnatal year, the growth rate reduces considerably thereafter. Six-year-olds have attained close to 90 percent of their adult brain size.

The rate of increase is reduced further during the early juvenile period between six and seven years (Figure 10.6). By 2 to 3 years, 80 percent of adult brain size is achieved, and by six years, nearly 90 percent is attained. The cranium continues to grow beyond the juvenile stage into subadulthood and early adulthood. Most individuals have achieved adult cranial capacity by their late teens and early twenties. Adults differ in cranial capacity as a function of body size, but are remarkably similar with respect to brain-to-body-size ratios (Gould, 1981).

Human Neoteny This marked increase in brain tissue is accompanied by changes in the proportion of the face to the jaw. A comparison between human life cycle stages demonstrates an increasing change of face-to-brain proportions as the facial skeleton enlarges to accommodate the eruption of the permanent dentition during dental maturation (Figure 10.7). In nonhuman primates, such as chimpanzees (Pan troglodytes), the growth of the face is much faster than the growth of the brain, producing a forward-jutting set of jaws abutting a relatively small cranium (Figure 10.8). In humans, the face grows at a slower rate and the cranium grows at a faster rate, resulting in relatively neotenic, or juvenilized, small faces and large brains in human adults (Gould, 1977).

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Extreme craniofacial traits are often related to male-male competition in primates, such as in baboons (Papio spp.), where adult males exhibit a pronounced forward projection of the snout coupled with large daggerlike canines. In the human lineage, neoteny could possibly account for a reduction of craniofacial robusticity, particularly in males. Subordinate males who could not compete with highly dominant and robust counterparts could have attracted mates through increased paternal care, which could evolve if the energetic costs for reproduction were relatively low (Key and Aiello, 2000; Kokko and Jenions, 2008). However, the reduction of craniofacial extremes during human evolution probably stemmed from a variety of factors. These include

Figure 10.7. The neurocranium becomes proportionally smaller in relation to the face from infancy to adulthood, as shown in a human (a) three-year-old, (b) six-year-old, and (c) adult. Figure 10.8. In chimpanzees (Pan troglodytes), the growth of the face is pronounced from (a) infancy to (b) adulthood compared to the growth of the cranium.

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increased technological skills, which reduced the need to use the teeth as tools or as a third hand, and decreased selection for larger teeth and jaws through the reduction of rates of shape change over a longer period of masticatory maturation, from infancy to adulthood.

Figure 10.9. Gould (1977) demonstrated the prolongation of juvenile shape into adulthood via neoteny with his clock model. The clock model for humans was somewhat different from what might be expected in “pure” neoteny (a), whereby the shape of the descendant adult resembles that of an ancestral juvenile, but at the same size and maturation as the ancestral adult. According to Gould (1977), human neoteny of the cranium (b) describes similarities between ancestral juveniles and descendant adults achieved by slowing the rate of cranial shape change, coupled with an increased rate of growth and an extended maturation.

11 Becoming Human About 6 to 7 Ma, ape-humans diverged into apes and humans. The branch that became humanity was distinct from the ape branch by its penchant for walking habitually using only the hind limbs. Walking on two legs is a precarious activity requiring coordination, balance, and concentration. Habitual walking on three legs is unknown in vertebrate evolution, given its inherent asymmetry and instability. Tripedal locomotion has been observed in quadrupeds who have lost a leg, as well as in ape mothers of newborn infants. These are exceptions, however, and illustrate the point that tripedal locomotion is a compromising positional behavior. Therefore, the shift from quadrupedalism to bipedalism must have occurred relatively rapidly during human evolution. Beginning about 2 Ma, a larger brain size evolved. Within the past few hundred thousand years, the brain size of humans emerged, coupled with fundamental attributes of culture such as intense sociality, mutual gazing, theory of mind, deception, cooperation, affection, gesticulation, language and its precursor, food sharing, kinship, dancing, music, art, symbolic communication, tool use, and culturally predicated behavioral control. These attributes of culture probably did not arise all at once. Rather, some must have occurred earlier than others. Still others may have arisen in an overlapping or cascading sequence. All of these cultural attributes occur in a predictable sequence during early human development at different times and durations. Some occur rather rapidly, such as the transition from crawling to walking. Others occur relatively slowly, like the acquisition of language. Ontogeny obviously does not recapitulate phylogeny (Gould, 1977), but there still may be some parallels between infant development and human evolution. During the ontogenetic process, infants traverse, or perhaps more appropriately retrace, the emergence of humans. Of course, it is

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an imperfect representation, but the signal of our evolutionary past is nonetheless present.

Prenatal Development Human life begins as a one-celled organism called a zygote, or ovumsperm combination. The earliest life-forms were most likely singlecelled organisms as well, although perhaps resembling bacteria more than eukaryotes. These single-celled organisms reproduced by mitosis. Similarly, zygotes eventually divide multiple times, essentially becoming a multicelled organism. Multicellular organisms are visible in the fossil record from about half a billion years ago during the Cambrian explosion. Analogous to multicelled organisms are biofilms, like plaque or pond scum, in which different species of bacteria conglomerate and differentiate into layers with different functions. During early gestation, the mass of embryonic cells on the outer surface of the blastocyst, the ectoderm, becomes a tubular structure from which emerge caudal (tail) and cephalic (head) ends. Some worms do not have specific heads or tail ends, such as nematodes, whereas others do. Some of the earliest invertebrates probably resembled worms, including the primordial ancestors of humans, which probably had caudal-cephalic ends. In human embryos, nodules along the initial vertebral column are the first bones to be visible, as in all vertebrates. A spinal skeleton is what separates vertebrates from invertebrates. Initially the vertebral column evolved from a notochord, a stiffened structure allowing efficient side-to-side movement to occur. The ancestor of fish, amphibians, reptiles, birds, and mammals exhibited defensive arches branching dorsally from the notochord, enclosed the spinal cord—an extension of the brain—and provided bony muscle attachments to enhance movement potential. The development of the notochord during gestation allows for some independent movement of the human embryo. Ancestral features are also represented in the gill slits that appear late during the first month of embryogenesis. These later migrate cranially to become the ear bones and the mandible. Similarly, during vertebrate evolution, ancestral reptiles are noted for these structures. Grasping hands are found across mammals during embryogenesis, suggesting that all are derived from ancestral mammal-like reptiles with five digits. The five-digit hand and foot are retained in nonhuman primates. Humans also retain the five-digit hand, although it is coupled with an elongated and powerfully built thumb.

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The four limb buds that emerge from the central tubular portion of the embryo are accompanied by a tail, the external part of which later greatly reduced and became internal to the body in the ancestor of apes and humans. Most of the descendants of the earliest vertebrates have tails to aid in locomotion, display, temperature control, protection for the ano-urinal/reproductive tracts, and/or social communication. A layer of fur develops during the second trimester, only to be shed later during the end of the second trimester or later, representing ancestors with body fur before hairlessness evolved. Once a child is born, it is essentially similar to infant chimpanzees in social, locomotor, and cognitive function, although much larger (Martin, 2013). During the ensuing three postnatal years, many traits of our ancestors appear, perhaps in the general sequence in which they emerged in time, with many important exceptions. It is an imperfect sketch of our evolutionary past unfolding between birth and the eruption of the deciduous teeth. In this way, infants resemble our ancestors.

Relative and Absolute Time Sequence for Acquiring Human Locomotion and Sociality Identifying the sequence of human social development can inform behavioral reconstructions in human evolution by allowing for an estimate as to when these traits arose. However, the development of sociality and the acquisition of locomotor skills are not mutually exclusive (Campos et al., 2000). Also, the duration of time needed to master human sociality and bipedalism may differ. Perhaps the duration of time when adult-like functions arise from infancy to early childhood provides an estimate of whether specific traits evolved more rapidly, such as bipedalism, or over a longer period of time, as in the case of empathy and theory of mind.

Intense Sociality Sociality is a survival strategy of all primates. Through sociality and cooperation, humans are able to decrease food scarcity. This is truly a cornerstone of humanity, providing a buffer from the physical world. When does intense sociality arise during postnatal ontogeny, and what is its expression? Humans are intensely social upon the acquisition of language, usually by three years of age or prior. Communication is one proxy of social intensity. Others include mutual gazing and proximity. The earliest of the three to arise postnatally is proximity. Infants often vocalize distress, or cry when they are not held by their known

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caretakers. For instance, it was noted in the small-scale society of the Busama of Papua New Guinea that infants sick from malaria who are normally cared for by multiple relatives resist leaving “their parents’ side” such that “they only want the father and mother at a time like this” as “the other relatives won’t do” (Hogbin, 1963: 66). Human infants held in close proximity derive great social benefits, whereas those kept in carrying devices, separated from caretakers, are deprived of intense sociality (Morris, 1992). Foragers and horticulturalists often carry their infants during the first few years. In some societies, crawling is skipped altogether, and bipedalism is the first and only form of locomotion, at around one year of age. For example, Tracer (2009) analyzed mother-infant dyads in Papua New Guinea. He found that mothers carried their babies with such frequency that the infants skipped any crawling stage as a precursor to full bipedalism. He suggests that infant carrying “is an adaptive parental strategy that made infants less susceptible to predation and also lessened transmission of parasites to offspring by curtailing oral to ground contact” (Tracer 2009: 371). Similarly, Ache mothers, even when engaging in demanding work such as extracting palm fiber, will keep infants in a sling on their backs, rather than placing them on the floor of the forest (Hill and Hurtado, 1999).

Mutual Gazing This is one of the earliest social traits of infants, and can occur periodically or episodically from the moment of birth. Like other social traits, its appearance is sporadic initially, but gains increasing frequency toward four to eight months of age. Mutual gazing is an important human characteristic that separates us from other animals, although bonobos are known to engage in frequent social gazing during some behaviors, such as in mating. However, it is not a consistently maintained form of social communication like it is in humans. The sclera of the eyes, which is white and frames the colored portion of the cornea and pupil, serves to accentuate social interaction between humans. A famous quip from the Battle of Lexington during the Revolutionary War, “Don’t fire ’til you see the whites of their eyes,” emphasizes this point. Sclera are lacking in other animals, although it is observed in some chimpanzees (Hrdy, 2009). Part of its necessity in humans is due to the reliance on language. Social gazing lets the speaker know the listener is attempting to follow; in the absence of mutual gazing, the listener is uncertain whether the signal is being received. Mutual gazing

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has its analogues in studies of primate behavior, where ogling can be both a threat and an invitation, depending on the context of the social interaction. Matrilineal relations among many Old World monkeys such as macaques require mutual glancing to rally solidarity among females and to show to an adversary who supports whom (Jolly, 1985). Staring indicates interest, and the duration of the stare indicates the degree of interest shown. In the absence of positive social relations, or sexual interest, a stare is threatening. So much is communicated through mutual glances among nonhuman primates. Humans have inherited these forms of social communication and intensified them.

Counting Rhythmic patting is practiced by the apes in the wild, so it is obviously an ancient signal. It is used in chimpanzees to reassure social partners after interindividual conflict or danger. Patting and counting are similar in that both demonstrate a sequence of signals tied together by their rhythmic patterning. Patting could be the first aspect of counting behavior to have evolved. Apes in captivity are shown to demonstrate simple means of counting and other cognitive skills related to mathematics (Rumbaugh et al., 1989; Beran, 2004). In infants, patting commences toward the first year of life and as early as ten months postnatally (Gaber and Schlimm, 2015). This behavior is often mimicking the patting of caretakers. The rhythmic cadence is about 4/4 time in both caretakers and infants. However, the duration of patting differs between the two, with infants showing independence in choosing when to end the sequence. This may be the precursor to mathematics, both evolutionarily and developmentally.

Pointing Showing directionality is an activity implying intent. Kanzi, a captive bonobo, was observed pointing toward the direction in which he wished to travel in the arms of a caretaker (Savage-Rumbaugh and Lewin, 1996). Pointing develops in infants around the first year of life (Tomasello and Camaioni, 1997), and can take many forms, including supinated (palms up) pointing, with undifferentiated fingers. Sometime soon after the first postnatal year, pointing becomes slowly stereotyped to include a pronated hand position (palms down), with directionality embodied in an extended second digit (index finger). By thirteen to fourteen months of age, the other digits fold under, creating a characteristic hand position of finger pointing common in North

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America. The eyes of infants can follow another’s visual cues and the pointing of others by one year (Fitneva and Matsui, 2015). At around seventeen months postnatal, infants begin to point and vocalize simultaneously. This dual signaling serves to emphasize and is a precursor to vocal complexity. In human antiquity, such a combination of pointing with indistinct vocalizations may have provided added emphasis and directionality to concepts both abstract as well as proximate, such as a predator in close range or a favored social partner. The intensity and pitch of the vocalization could have been recruited to add emphasis or subtlety in meaning.

Clicking The sudden release of a captured pocket of air by drawing the cupped tongue from fore to back along the roof of the mouth, creating a clicking sound, is a phoneme in several languages, such as Xhosa. Used in conjunction with vowel sounds, clicking can convey a variety of connotations. Clicking may have been one of the earliest means of communication in conjunction with other gestural, nonverbal cues. Clicking emerges near the onset of the second postnatal year.

Language or its Precursor and Gesticulation Gesticulation occurs toward the end of the first postnatal year, at around ten to eleven months or later. In wild chimpanzees, infants begin gesturing to their mothers at around nine months of age (Plooij, 1984); captive apes begin complex gestural communication between ten and fifteen months (Schneider et al., 2012). In humans, one of the earliest gestures with meaning is waving to signify the coming and/ or going greeting that is common universally. Learning how to wave is rapid in comparison to vocal-auditory signaling, and once it is learned, it can easily be elicited. The rapidity in learning this gesture suggests that its evolution was also relatively swift with respect to other complex communicative tools. The acquisition of spoken language occurs slowly during the first two years postnatally or longer. Infants are not proficient at language after the first postnatal year. Much of spoken language acquisition occurs over the second postnatal year, and particularly after eighteen months of age when full, albeit simple, sentences can be communicated. Infants of this age utilize the visual cues and pointing gestures by themselves and others to learn the names of things (Fitneva and Matsui, 2015). By eighteen months, infants may apply the name of a

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pet to extradomicile animals or create categories that can be applied broadly. By twenty-four months, many infants can categorize using higher-order distinctions classifying all dogs and all cats as distinct, and as pets or not pets (Viskontas, 2015). The mimicking of animal noises may have been some of the earliest forms of communication among early humans, perhaps arising from the close observation and mimicry of hunted animals. Infants can learn to mimic the caretaker’s imitation of farm animals after the first year, well before basic linguistic competency. Parts of the body may have also been a part of the protolanguage of humans. These can be learned by asking infants to identify and dissociate themselves from their parts. This dissociation is critical to language acquisition, since abstracting a part of the body and compartmentalizing different call systems are the tools necessary to associate random calls with meaning. Infants beyond a year begin to attribute meanings to symbols in uniquely human ways.

Food and Object Sharing Infants of about a year or more begin to show an interest in sharing objects by passing them back and forth with caretakers. Manifestations of this behavior can occur much earlier in postnatal ontogeny, as soon as infants and caretakers establish turn-taking routines using gestures rather than words (Halton, 2014). For example, such turn-taking rituals can involve the grab and release of fingers or hands, which can occur between six months to a year. However, it is the older infant who can share by giving and receiving. Food sharing is found in all known cultures, as it is probably an ancient tradition of ancestral humans, critical to avoiding starvation (Lancaster and Lancaster, 1983). Food security is a preoccupation among hunter-gatherers (Hill and Hurtado, 1996). Food sharing allows for flexibility in the daily returns of families and groups (Hawkes and Bliege Bird, 2002). Routinely sharing food was absolutely essential for the costly brain of humans to evolve (Kaplan et al., 2000). Batek foragers live in camps with five to eight families. Subsistence depends on food sharing such that “camps had a moral unity that was expressed most vividly in the obligation to share any food—animal, or vegetable, foraged or traded—that people obtained in excess of their daily needs” (Endicott and Endicott, 2014: 110). It was often the special job of children to distribute resources such that they would “[carry] portions of food from one shelter to another, even when the occupants already had their own supply” (Endicott and Endicott, 2014: 110). Young children were particularly called upon to participate

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in “the sharing network of the camp by helping to distribute plates of food to other families in camp” (Endicott and Endicott, 2014: 112). In fact, “this was one of the few jobs young children were actively given” (Endicott and Endicott, 2014: 112). This group provisioning helped provide calories for those least able to contribute to the group, such as children, but also older and unmarried individuals, and those unable to succeed at obtaining food by themselves (Endicott and Endicott, 2014). Such repeated acts served to enculturate children in the importance of sharing as a primary cultural value. The precociousness of object and food sharing may corroborate the antiquity of provisioning (Lancaster and Lancaster, 1983).

Theory of Mind and Deception The earliest sign of deception is the game of peek-a-boo, where infants place a blanket over their heads or in front of their faces and cannot be “seen” because they themselves cannot see. Infants lack a theory of mind in that they can only recognize or understand that which they themselves observe and not what someone else can possibly see. In other words, they cannot put themselves in another’s frame of reference. Infants begin to perform peek-a-boo and other forms of deception at about one year of age, although earlier manifestations of the game may exist by six months (Bigelow and Best, 2013). Theory of mind is how infants obtain what they want from others, essentially becoming mind readers at a young age to engage in the social behavior of the family and community (Hrdy, 2009). Understanding the thoughts and feelings of others is the basic foundation of empathy.

Affection The ability to show affection must also be an ancient trait of humans. This affiliative communication may derive from food-sharing behaviors that engender reciprocity. Frequent expressions of affection are certainly found among family members in small-scale societies. For example, among Batek foragers, relations between children and adults can be characterized as “one of mutual affection and respect” (Endicott and Endicott, 2014: 117). Infants begin to kiss and hug their caretakers before or after the first postnatal year. By thirteen months, infants are often able to kiss their caretakers on request with an open month kiss, perhaps the first kiss of ancient humans. The early acquisition of kissing during the postnatal period suggests it may have evolved before language, but after biped-

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alism, although chimpanzees have been observed “kissing,” suggesting the origin may be older still.

Song and Dance In addition to the habitual use of the hind limbs for walking, bipedalism offered ancient hominins the ability to express sociality using rhythmic movements or dancing (Hart and Sussman, 2005). The appearance of rhythmic behaviors with the hind limbs during the second postnatal year suggests a relatively early origin in human evolution. Infants of about one year of age can dance when enculturated to do so by a caretaker. This can be a simple movement of the head to one side, or rhythmically bouncing in response to music and singing. Later dancing can be initiated upon request of a caretaker in the absence of music, suggesting the behavior can be quickly mastered and abstracted. Singing is widespread across cultures and was probably present in the common ancestors of all human groups. Among the Batek, music utilized with singing, fragrant body decorations, and rhythmic drumming accompanied the beginning of the fruit season when the supernatural world was asked for a bountiful cornucopia and afterward to express gratitude to the “superhuman beings” for the fruit that had been given to the camp (Endicott and Endicott, 2014: 122). Singing promotes positive feelings and group cohesion. Among foragers such as the Batek, singing is utilized in trance as well as in rituals, particularly those involving healing an ill camp member. During rituals pertaining to healing or seasonal events, rhythmic drumming commenced as “a large number of other people would dance around the platform in a circle while singing songs to the superhuman begins” (Endicott and Endicott, 2014: 122). Shamanic trances ensued on a quest to visit the dwellings of the supernatural forces and “the singing might last for the entire night” (Endicott and Endicott, 2014: 123). Singing and dancing to music increased the confidence of camp members (Endicott and Endicott, 2014). Dancing is a parody on the instability of bipedalism. In infants, dancing cannot occur until some degree of habitual bipedalism is mastered. Its first expressions involve using substrates, such as furniture, upon which to balance. At about sixteen to seventeen months, infants can be taught to rhythmically stamp their feet. This further emphasizes the role of dancing as a social expression in infants. However, musical ability can already be seen by infants between thirteen to fourteen months, with much vari-

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ation dependent on the instruments available, such as shakers, noisemakers, tambourines, drums, and guitars. Common household items can be transformed into musical instruments as well, such as pots and pans. More controlled forms of music composition typical of adults occur much later postnatally, between three and seven years old. Infants cross-culturally understand the basic worldview of a culture through song and dance. For example, in Aboriginal Australia as soon as an infant was able to walk independently by about one year, “much time is devoted by both parents to the entertainment, amusement, and instruction of their children” (Montagu, 1974: 346). Much of this engagement is through music. For instance, “in the evenings songs and dances related to the ancestral traits are performed for their benefit, and these songs and dances they are taught and encouraged to acquire” (Montagu, 1974: 346).

Kinship The recognition of close kin and nonkin is an ancient behavior of eukaryotic life. However, to recognize on the basis of visual cues is especially important in monkeys, apes, and humans. Vocally identifying close kin, such as parents, is a universal quality of humans and is attained sporadically beginning between ten months to more than a year postnatally. Siblings and other relatives and nonkin caretakers can also be identified by particular vocalizations in infants beyond a year of age. This is also the age at which infants of Efe foragers are able to gesture or vocalize to familiar camp members, such as kin, establishing social relations independent of the mother (Morelli et al., 2014). How does kinship reckoning arise in one-year-olds? Frequently the mother is recognized by name (“mama”) first, particularly if the baby is breastfed on demand, implying a close proximate relationship between the two. The father can also be recognized by name simultaneously or thereafter, depending on his involvement with the mother-infant pair. Siblings that act as secondary or tertiary caretakers are often named early. Sometimes the name that infants call a caretaker is an approximation of the name others call the individual. These become eventually reconciled by eighteen months of age. An example of kinship learning can be gleaned from breastfeeding Busama mothers of Papua New Guinea, where basic kinship terms are learned directly by imitation. Traditionally, a breastfeeding mother “murmurs bu and na as she suckles the infant, who eventually begins to imitate her” (Hogbin, 1963: 64).

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Later, everyone becomes na to the infant, “but the father soon teaches it to say ma” (Hogbin, 1963: 64). The infant then refers to all family members according to gender, whereby “all females are na and all males ma” (Hogbin, 1963: 64). After children have mastered vocalizations for gender-based kinship words, it still takes time for young children to learn more specific terms for kin. For instance, in Busama, Papua New Guinea, “the children fail to recognize the true meaning of kinship for another year or two” (Hogbin, 1963: 66). Kinship is an important quality of group cohesion that often involves reciprocity and obligation among group members. Status objects are shared among kin who often work together during subsistence activities. Reckoning kin likely arose as a yet another way to avoid, as much as possible, food scarcity. In traditional societies around the world, food sharing is a regular activity between close kin. Children are given food by their kin so much so that in this way children learn who their relatives are. For example, in Busama, Papua New Guinea, “the child hears kinship coupled so often with food that he becomes even more convinced that they always go together” (Hogbin, 1963: 84). Food sharing occurs in infancy such that young children “feel comfortable with someone who gives them meals and finds out afterwards about the relationship” (Hogbin, 1963: 66). Kinship is found in all human societies ever encountered, but the form it takes varies considerably. Like couvade, kinship is necessary for societies to function effectively but is shaped according to the history, ecology, and social world of its participants. Reckoning kinship certainly arose at some point during the evolution of large brain size in ancient humans—but became incrementally more complex between 2 Ma and 400,000 years ago—as such a system of support would be a necessity if children were to be cared for and provisioned for nearly two decades.

Signally Affirmative and Negative Among English-speakers and others, infants can signal “no” with intent, often accompanied by a shrill vocalization, followed by “yes” as early as thirteen to fourteen months. Infants begin to signal “no” by shifting the head side-to-side. This is an easier maneuver than moving the head rhythmically up and down while holding the neck in a stationary position to signal “yes.” Signaling the affirmative often requires the entire upper trunk to move with the head. Eventually, independent movement of the head vis-à-vis the neck and adjoining axial skeleton is achieved. The “no” signal can be exaggerated to be repeated again and

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again as a form of humor, showing further evidence that infants exhibit initial development of a theory of mind.

Art and Symbolic Communication Infants are initially able draw at thirteen to fourteen months postnatally. These are simple and largely uncoordinated movements consisting of a writing implement drawn across a substrate, such as a sheet of paper, but with intent. Infants can choose colors and draw without reference to handedness. The earliest representations of symbolic communication are dated to the Mousterian cultures associated with the Neandertals dating to 115,000 years ago (Hoffmann et al., 2018). Early migrants to Australia also experimented with hand designs as early as 50,000 years ago. Elaborate cave paintings occur in southern France and Spain from about 25,000 years ago, and rock art is found in prehistoric settings in the Cape region of southern Africa (Cartmill and Smith, 2009). Etchings and engravings increase in frequency and skill throughout the Upper Pleistocene time interval, and a florescence is evidenced at Upper Paleolithic sites in Europe and elsewhere, signifying the antiquity of artistic expression.

Intentional Facial Expressions Facial expressions are unique to monkeys, great apes, and humans, which include fear grimaces used to show submission to a dominant animal, pouting as a way to show interest in mating or social interaction, flashing the eyelids to demonstrate possible eminent attack, and the open-mouthed play face of juveniles with the teeth covered by the lips (Jolly, 1985). Apes and humans excel at expressing emotion using the facial musculature. However, chimpanzees and bonobos show a fixed meaning for different facial expressions (Pollick and de Waal, 2007). In contrast, humans are able to express a greater range of facial expressions because of the increased complexity of the facial muscles. Furthermore, humans have co-opted facial expression to signify feelings. By intentionally tensing and relaxing the facial muscles, humans can mimic spontaneous or inadvertent facial expressions. Inadvertent facial expressions include surprise, fear, anger, happiness, pleasure, and pain. Intentional facial expressions suggest the capacity to pretend. The mimicking of inadvertent facial expressions includes a happy face, surprised face, jealous face, sleepy face, and angry face (Figure 11.1). Intentional prolonged blinking can also be learned by infants. Infants can begin to master intentional facial expressions at thirteen to fourteen

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Figure 11.1. Mimicking of inadvertent facial expressions can occur early during the second postnatal year, as demonstrated by this fourteen-month-old infant’s pretend “angry face.”

months and older, indicating that this ability may have arisen relatively early and prior to language. The ability to respond to requests for a particular facial expression signals a more intricate theory of mind, upon which humor is based. Humor may have arisen from intentional facial expressions. Facial expressions are part of showing positive affect, which infants in Japan, Russia, and the United States all master by twelve months (Friedlmeier et al., 2015).

Organization Infants are able to organize objects within their external surroundings between thirteen to fourteen months and older, with a range of eight to twenty months (Swann, 1998). Some of the earliest manifestations of organization are placing objects into occlusion. This can take the form of placing lids on pots initially or stacking blocks. Eventually, when infants are beyond the first postnatal year, they are able to align perforated blocks in place along a vertical substrate. Closer to a year and a half, infants are able to align the blocks according to size. By two years of age, an infant can organize pieces of a jigsaw puzzle in the proper order (Super and Harkness, 2015).

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Hand Holding At about fifteen months, sometimes earlier or later, infants begin to be able to hold hands while walking. This is a way to denote intimacy and togetherness, and for two to act as one. Fossil footprints at Laetoli dated to about 3.6 Ma have been interpreted as two larger individuals holding hands as they walked along an ash-mud surface (Hart and Sussman, 2005; see Figure 1.1). Chimpanzees have been observed holding hands, and bonobos are known to walk using a one-arm embrace. However, these behaviors are sustained only briefly. Hand holding in humans is a universal symbol and is manifested when the infant brain is between 50–60 percent of adult size.

Elimination Signaling Most societies in the world train their infants to respond to cues to eliminate their wastes between one to four months postnatal, with the process complete by one year (Sun and Rugolatto, 2004; Benjasuwantep and Ruangdaraganon, 2011). In Western cultures, caretakers often initiate elimination signals at eighteen months (Sun and Rugolotto, 2004). These choices depend on culture, ecology, status, and wealth, and the idiosyncrasies of the caretaker and the infant. After bipedalism is learned, infants are able to direct their own elimination needs, such as visiting a designated receptacle where waste can be collected, if infants are unrestrained by restrictive clothing (Bauer, 2003). Infants may also learn to emit a verbal signal, such as a vocalization, or use gestural cues to indicate the need to eliminate, between a year and fifteen months. This may be an ancient communicative action that arose when living in cohesive groups necessitated the use of the same living and sleeping places continuously for several nights. Extant great apes, including gorillas, chimpanzees, and orangutans, make fresh sleeping nests each evening. This avoids sleeping in nests that may be soiled during the night or upon waking, such as observed in some gorillas. Humans also sleep in nests, called beds (Jolly, 1985). The precocious understanding of elimination communication in infancy may reflect its antiquity.

Social Cooperation Infants at around fifteen months can lead caretakers to a specific location and sit down to begin playing, expecting the caretaker to take part in the activity. This intentional creation of a social space is a uniquely human quality. Cooperation takes many forms among animals, including group hunting among social carnivores such as hyenas and wolves,

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swarming in birds, group defense among various primates, migration among ungulates and whales, as well as hive and colony establishment and maintenance among social insects. Social cooperation in humans differs in its spontaneity, its variation in form, and its lack of a specific stimulus, such as predators, prey, or cyclical/seasonal cues. Social cooperation implies that a well-developed familiarity has already been established such that individuals reenact specific actions or the repetition of a sequence of events that occurred previously. In infants, this can take the form of moving a car back and forth across the floor, or embodying toys to perform a simulated interaction between individuals. In infants of Efe foragers, social cooperation increases with respect to age during the first three postnatal years and becomes reciprocal by infant-caretaker interactions involving “ask and offer and give and take” processes (Morelli et al., 2014: 91). These learning experiences lay the foundation for future cooperation between group members. This fundamental human quality has likely contributed to the survival of small groups, perhaps throughout the past several hundred thousand to more than a million years.

Communicative Sighing and Blinking Humans utilize a range of intentional breathing and blinking variants with specific meanings. In North America and elsewhere, sighing is a way to express boredom, impatience, or resolve, depending on the context, whereas a forceful exhalation can denote anger or frustration. Fast repetitive breathing and intentional loud exhalations can be interpreted by infants as play behavior when eye contact is maintained. Similarly, intentional blinking, either holding or squeezing the eyes shut or otherwise exaggerating involuntary blinking, can hold meaning depending on the context. Among infants at around fifteen months, such actions can communicate feelings of mutual interest, suggesting exaggerated blinking and breathing could be an ancient means of conveying mood states and interest in the absence of language.

Walking to Running Infants begin to walk bipedally at around the end of the first postnatal year—sometimes earlier, sometimes later. What is remarkable is that the timing of human terrestrial bipedality (the act of habitual locomotion where only the hind limbs have contact with the ground) appears to be a cross-cultural phenomenon (Mead, 1955). Walking occurred as early as 4.4 Ma, as demonstrated by the enlarged knee joint of Australo-

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pithecus (an early human fossil) and the 3.6 Ma fossilized footprints of at least three early humanlike forms. It is likely that Australopithecus also retained some climbing abilities but exhibited the fundamental adaptations of terrestrial locomotion. Although habitual terrestrial bipedality was possible, it has been hypothesized that Australopithecus lacked the ability to run, given the relatively short legs with respect to body size and the limited height of the waist owing to the capacious rib cage. Human infants begin to “run-walk” at around sixteen months by leaning forward during walking. True running, where the feet have only limited contact with the ground and the legs are slightly flexed, begins between 1.5 and 2 years postnatally, consistent with its occurrence in later human evolution during the emergence of the genus Homo (Bramble and Lieberman, 2004).

Acknowledgment of Accidents and Shame Infants between fourteen and eighteen months are able to grasp that an accident has occurred when the word “whoops” is employed (Carpenter et al., 1998). At seventeen months, infants begin to signal acknowledgment of an accident in North America by vocalizing “ut-oh.” The “ut” is strongly aspirated, while the “oh” segment is a softened follow-up. This rather complex concept and accompanying set of vocalizations contrasts with the one-word statements of most infants of this age. There is substantial variation in the age at which infants begin to recognize accidents. Part of this variation is cultural and relates to how the acknowledgment of shame is taught. For instance, in Western Samoa among the Kaluli, shame acknowledgment by caregivers occurs as early as six months (Schieffelin, 1986). Meanwhile, by fourteen months, Japanese infants are often asked by caregivers to acknowledge shame for transgressions that involve, for example, bodily functions, and twoyear-olds are taught to attribute shame to infants younger than themselves for such culturally inappropriate behavior (Fitneva and Matsui, 2015). Shame is perhaps a near-universal quality of the human condition, as it enforces normative behavior. Learning cultural norms and taboos must have become important as culture evolved within ancient hominin social groups.

The Yes/No Game Infants at about eighteen months begin to play the yes/no game, which consists of nodding the head to imply “yes” followed by a “no” signal. These shifts indicate a game whereby the players are showing inde-

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cisiveness and humor simultaneously. The extremes of affirmative and negative are contrasted to demonstrate ambiguity. This kind of nonverbal communicative wordplay is essential to mastering binary opposition and shows an understanding of changes of opinion and uncertainty. Shaking the head to indicate “no” is found in infants by two years across many cultures (Tomasello and Camaioni, 1997).

Singing Infants, prior to their second birthday, generally around twenty months postnatal, can learn to sing a three-tone sequence consisting of a chord or partial scale. For example, using phonemes or simple words such as da, ma, or na, which infants repeat as triplets from high to low tones, represents the form of a song, particularly when it is repeated several times, substituting different phonemes or simple words in the sequence. These “songs” often occur prior to the full use of language. Singing has been hypothesized to have evolved as a way for mothers to communicate with infants when they were “parked” during foraging (Falk, 2009). Humans communicate through language using intonation changes that resemble singing. Singing and music in general, including rhythmic chanting and drumming, could have served some of the same functions as language, such as group cohesion and coordination. Perhaps more importantly, language and singing help reinforce social bonds.

Social Eating As infants begin independent movement during the first year, they gravitate toward social settings, such as eating. Infants begin to desire to eat with the family between 1.5 to 2 years postnatal or earlier. There is evolutionary significance of this interest in group eating. At some point in human evolution, food sharing became an essential component of sociality as it reinforced group cohesion and solidarity at a specific location or home base (Lancaster and Lancaster, 1983). Home bases could have been preceded by caches of stone tools placed strategically across the landscape (Potts, 1988). Food sharing is known in other cooperative breeders such as marmosets and tamarins, in which group members have been observed catching insects for infants; bonobo mothers have been observed sharing fruit with their infants; and male chimpanzees have been noted to share meat with other hunters, estrous females, and favored social partners (Stumpf, 2011).

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However, this is limited in degree among nonhuman primates. Social eating is a daily ritual in human societies past and present.

The “Come Here” Signal Around the age of two years, or earlier, infants begin to signal for caregivers to accompany them elsewhere with an opening and closing of the open-faced palm. Here, infants are utilizing symbolic communication by bringing what is distant close together. The open-palm is an invitation, rather than a go-away signal that is shown in chimpanzees and humans by motioning outward with the back of the hand. In time, infants replace the signal by language, or it is used in conjunction with a vocal command: “come here.” The “come here” hand signal might have been important in protolinguistic ancestral humans to initiate group cohesion and protect individuals from danger, and probably preceded spoken language.

Counting Between eighteen months and two years, infants are capable of counting to one and holding their index finger while the rest of their digits are gripped together. At about two years, infants are able to hold two fingers apart from the others and thumb. Counting to two occurs at the brink of language learning, usually shortly after the second birthday, although sometimes earlier, sometimes later. Counting to ten and beyond is possible when language learning accelerates between 2 and 2.5 years. Counting using the fingers occurs toward the third birthday, when young children gain strength, dexterity, and neurological control of their digits. Indeed, this may be an ancient custom of humanity, as “all over the world the fingers are used as counters” (Lubbock, 1873: 296).

Adorning the Body Beginning at around eighteen months to two years, infants begin to adorn themselves with necklaces, bracelets, hats, and other accoutrements. These kinds of materials are not part of the regular wardrobe. Yet these materials are found in all cultures and often confer the status, identity, and selfhood of the individual, suggesting it is a speciestypical behavior. Early human forms must have adopted these kinds of signifiers to demarcate individuals and forge group identity.

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Language Explosion Between 2 and 2.5 years, a true language explosion occurs. Although some infants are precocious in language learning, particularly firstborn children, most are able to utilize at least fifty words or communicative signals by the second birthday. Shortly after this landmark, two syllable words, such as “bubble,” begin to emerge in the vocabulary of infants. Short phrases using subject-verb combinations arise somewhat later during the first few months after the second birthday. Language learning accelerates somewhere between the first and fifth month beyond the second birthday, when infants begin to utilize full sentences and express themselves using spoken language (Fitneva and Matsui, 2015). Such a rapid transformation from preconversational to fully fledged spoken communication suggests the evolution of language from a protolanguage was a punctuated event. A simple preconversational language system may have existed for quite some time before the rapid emergence of human language. The use of tools could have followed a similar pattern. A long stage of Oldowan pebble tools arose, beginning 3.3 Ma or earlier (Harmand et al., 2015), followed by a developed Oldowan tradition emerging around 2 Ma. More complex tools came later, beginning with the Achuelian hand axe at around 1.4 Ma in Africa, and eventually in western and southern Eurasia, as well as the use of chopper/chopping tool kits in East Asia (Kennedy, 2003). The advancement of stone tool technology and material culture in general may be a proxy for language complexity before the origin of modern humans (Morgan et al., 2015). Infants begin to successfully utilize simple tools, such as a spoon and fork, from about eighteen months postnatal. By about 2.5 years, infants are relatively competent tool users, paralleling their interaction with language. Language is a form of communication that is intimately tied to the abstract association between symbols and meaning, and may have been impossible without a material culture, which implies that it is a uniquely human trait. Furthermore, teaching the varied techniques related to the production of complex stone tool types virtually requires language (Morgan et al., 2015). New ways of thinking, such as memory and self-recognition, became possible when language could be internalized. More effective social groups emerged when males and females could learn the lexicons of both sexes during infancy. Before or after 2.5 years, infants may initiate the negative by nodding “no” and speaking in nonnegative phrases, such as “we are going

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home,” implying that that we are not going home. In this way, the meaning becomes the exact opposite of spoken language by using nonverbal cues. These contrivances must have been particularly useful to early humans as language began to dominate nonverbal communication.

Behavioral Control and Rules Between the ages of eighteen months and three years postnatal, infants begin to control their behavior according to social rules, particularly as they master linguistic cues (Ochs, 1996). For instance, Batek forager infants and toddlers learn social rules about nonaggression characterizing their sociocultural norms (Endicott and Endicott, 2014). Social rules include utilizing the cultural and linguistic cues for politeness (Fitneva and Matsui, 2015). Social status indicators, such as honorifics, must be used in many languages. The use of these forms of speech requires an understanding of the hierarchal structure of a society. These are relatively elaborate and fixed in such places as Western Samoa, and young children from early infancy must internalize these status differentials. Explicit instruction is given to children cross-culturally on the use of polite forms of address, although there is variation concerning when these culturally appropriate speech forms are actively taught. For example, the use of honorifics in Japanese is required. Training children on the correct use of these begins between one and two years. By three years, Japanese children have mastered the correct usage of honorifics (Fitneva and Matsui, 2015). Among the Basotho, explicit instruction in polite forms of address begins between two and three years. Special efforts are made by caretakers to provide detailed explanations and examples of polite forms of address. In contrast, children often do not receive explicit instructions on the correct use of syntax or vocabulary during infancy, intimating the importance of polite forms of address to human sociality (Fitneva and Matsui, 2015). The delay in onset and active teaching of polite forms of address suggest rigid social hierarchies are rather recent. All cultures have socially proscribed rules that follow norms of behavior, whereas the violation of social rules is considered taboo. Learning these social rules requires language use. Therefore, social rules occurred subsequent to the emergence of language. Control of behavior is a key adaptive trait in humans, allowing for hypersociality and extreme population density with minimal violence. For example, if a hundred chimpanzees were locked in a plane from New York to Washington, DC, they would all be killed by one another or seriously

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injured before landing (Hrdy, 2009). Waiting for food to be prepared, cooked, and served requires tremendous behavioral control atypical of most animals. Infants learn to extensively control their behaviors during the third postnatal year and beyond. Although infants can mimic adults in their behavioral control, it is only after the age of seven or eight years that children learn to control much of their behavior, and it can take nearly a decade after reproductive maturation before adult levels of behavioral control can be attained.

Reconstructing Early Hominin Behavior The earliest hominins had relatively small adult brain sizes as compared to those of modern human adults (Leonard et al., 2007). These hominins were not dissimilar in brain size to modern human infants, although differences in complexity and white matter were present (Schoenemann, 2013). Human postnatal acquisition of social behaviors may broadly approximate when these qualities arose in early hominins. Although an imperfect comparison, the cranial capacity of adult early hominins can be juxtaposed to the increasing brain size

Figure 11.2. Comparison of cranial capacity (cm3) versus age in humans with cranial capacity of fossil hominins. The human growth curve was created using a Lowess regression from previously published data (Williams et al., 2002, 2003). The cranial capacities of Pliocene and Pleistocene fossil hominins are from Skinner and Wood (2006) and from a primary cast of a Neandertal child from Teshik-Tash, Uzbekistan, aged to 9.5 years (Williams, 2013).

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typical of modern human infants (Figure 11.2). However, even before birth, modern humans have surpassed the brain size of the earliest known hominin, Sahelanthropus tchadensis (Figure 11.2).

Behavioral Reconstruction of Australopithecus Australopithecus exhibits a third of the brain size of modern human adults. As such, the cranial capacity of Australopithecus is slightly larger than that of a neonatal to a one-year-old human (Figure 11.2). Across cultures, one-year-old humans are able to walk, some early and some later. Similarly, Australopithecus was capable of walking but not running (Bramble and Lieberman, 2004). A form of communication partly like language but partly involving nonverbal cues, hand signals, and nonverbal body communication probably existed in Australopithecus. This protolanguage was used to maintain social ties between mothers and infants, and her kin, perhaps involving males as well, partly resembling the social organization of Pan (Zihlman, 1981). A rudimentary “grammar of action” had already arisen to facilitate the hierarchical arrangement of verbal and nonverbal signals and their motor correlates pertaining to social communication (Greenfield, 1991; Moore, 2011). Indirect care of infants, such as protection from harassment by conspecifics and predators, was likely one of the earliest routine features of paternal behavior in early hominins (Gray and Crittenden, 2014). Infant carrying would have been essential to early hominins, given the number of arboreal, cursorial, aquatic, and avian predators in savannas woodlands and forest fringes (Hart and Sussman, 2005). For example, large hyenas in packs could have attacked small groups of Australopithecus, requiring males and females to quickly grab infants to run to the safety of trees (Hart and Sussman, 2005). Constant vigilance, communicative signaling, and cooperative parenting would have been highly valuable in savanna environments, open woodlands, and forest fringes in which these australopiths lived. With the emergence of larger brain sizes, represented by KNM-ER 1470 attributed to H. rudolfensis or H. habilis, a more complex form of communication was perhaps possible, involving the increased use of phoneme-based communicative signals. Early Homo approximates the brain size of a 1- to 1.5-year-old modern human (Figure 11.2; Leonard et al., 2007). Perhaps early Homo was capable of more advanced nonverbal communication, reflected in an increasingly complex tool industry (Moore, 2011). Meanwhile, verbal names for things may have

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been vocalized to convey meaning and urgency. More elaborate social behaviors perhaps became common as brain size and social complexity increased in H. ergaster/H. erectus.

Behavioral Reconstruction of Homo erectus The brain size of Homo erectus is about three-fourths the size of that in modern human adults and approximates a 2 to 2.5-year-old modern human infant in cranial capacity (Figure 11.2). The range of H. erectus behaviors is known from the fossil record and is evidenced by the production of stone tools, including the developed Oldowan tradition, and later, Acheulian hand-axes and, most likely, complex tools made from bamboo in Eastern Asia (Kennedy, 2003). Obviously two-yearold humans are not capable of such technological feats. However, two-year-olds are able to talk, regardless of culture or subsistence strategy (Mead, 1955). Perhaps H. erectus was also able to utilize verbal communication as indicated by an advanced tool technology (Moore, 2011). It is likely that at least some indirect and direct male care of infants was a routine feature of hominins by about 2 Ma (Gray and Crittenden, 2014).

Behavioral Reconstruction of Archaic Homo sapiens Infants approach a brain size comparable to archaic Homo sapiens upon the third postnatal year and beyond. Archaic humans, such as Neandertals, exhibited an accelerated growth in cranial capacity compared to modern humans (Figure 11.2). This faster rate of growth continued during the juvenile period and into adulthood (Williams, 2013; Williams and Cofran, 2016). Neandertals are the most well-preserved archaic human population, and are found from Iberia to Siberia, from 200,000 to 30,000 (Trinkaus and Shipman, 1992; Cartmill and Smith, 2009; Williams, 2018). Neandertals, like modern humans, also show some advanced behavioral traits. For example, Neandertals utilized naturally occurring pigments, such as yellow and red ochre, which is an iron oxide, perhaps mixed with fat, to smear on the body as deduced from mass spectrometry of Neandertal bones that are reddish in tint. Neandertals also applied ochre to shells and carried them away from where they were originally found (Villa and Roebroeks, 2014). Black mineral pigments, such as manganese oxides, were also used at over seventy Neandertal sites (Bonjean et al., 2015). At the Neandertal site of Pech de l’Azé, more than five hundred black pigment fragments were preserved, and half of them exhibit evidence of use-wear. Although it is disputed, a flutelike

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instrument was reported from Slovenia (Divje Babe) with small holes positioned to match a music scale. In addition to finely made Mousterian stone tools for hunting and for domestic purposes, Neandertals also made nonutilitarian artifacts, which have been recovered from the same contexts as the skeletal remains and tools. These nonutilitarian artifacts show that Neandertals exhibited cognitive functions exceeding those needed for survival. Some of these artifacts appear to have been gathered by virtue of their intrinsic worth or perhaps beauty, rather than for a specific utilitarian use (Moncel et al., 2012). Neandertals built fire hearths in close proximity to their resting and sleeping spaces, indicating domestic areas with repeated use (Vallverdú et al., 2012). These include camps reconstructed as long-term habitation sites, regular hunting camps, and briefly inhabited overnight camps (Daujeard and Moncel, 2010). Although three-year-olds are not capable of these intricate cultural behaviors, they are fully human in their ability to negotiate complex social relationships (Hrdy, 2009). Three-year-old children are also able to walk, talk, eliminate appropriately, run, jump, dance, create humor, share foods and objects, count using all ten fingers and beyond, as well as other behavioral traits typical of living human groups and those in the past, such as archaic H. sapiens, including the Neandertals.

When Did Father Care Evolve? Neandertals probably exhibited an enhanced sense of empathy, given that they buried their dead (Trinkaus and Shipman, 1991). Empathy is the basis of father care, as caretaking is initiated by understanding the needs of others and placing those needs first. There may be several clues as to when facultative fatherhood emerged during human evolution from the development of empathy during infancy, as demonstrated by the acquisition of a theory of mind and the practice of affection (Table 11.1). Intentionality with regard to facial expressions and humor as well as symbolic communication would be important in empathetic behavior, as would food and object sharing. Social eating and spoken language would certainly involve empathy. All of these milestones develop between the first and second postnatal year, suggesting that father care may have been in place during the period when the genus Homo evolved, if not earlier (Figure 11.2). It is challenging to reconstruct the exact point in prehistory when fatherhood first occurred. Others have argued that father care emerged about 1.5 to 2 Ma with the evolution of early Homo and H. erectus

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(Smith and Tomkins, 1995; Gettler, 2010). The relatively large brain size, resting metabolic rate, complex technology, and protracted life history of H. erectus all suggest a role of paternal behavior in the evolution of this taxon (Leonard et al., 2007). However, it is also possible that male involvement in provisioning, caretaking, and infant carrying may have been selected for in Australopithecus (DeSilva, 2015).

Table 11.1. Approximate ages when infant behavioral traits occur Behavior trait

Approximate postnatal age of first occurrence

Intense sociality

At birth (or within the first week)

Mutual gazing

4–8 months

Rhythmic patting

10 months to 1 year

Gesticulation (e.g., waving)

10–11 months or older

Theory of mind and deception

1–3 years

Bipedalism

1 year

Elimination signaling

1 year (or earlier) to 18 months

Affection such as kissing

13 months

Song and dance

13–14 months

Pointing

13–14 months

Signaling affirmative and negative

13–14 months nonverbal; verbal by 18 months

Art and symbolic communication

13–14 months

Intentional facial expressions/humor

14 months and older

Organization/sorting

13–14 months, according to size by 18 months

Initial language such as body parts

After first year (>12 months)

Attaching meaning to symbols

After first year (>12 months)

Food sharing

At or after first year (>12 months)

Behavior trait

Approximate postnatal age of first occurrence

Mimic animal sounds

After first year (>12 months)

Object sharing

After first year (>12 months)

Leading caretakers to location

15 months

Communicative sighing and blinking

15 months

Hand holding

15 months

Walking to “run-walk”

At around 16 months

True running

18 months to 2 years

Rhythm

16–17 months

Pointing with vocalizations

17 months

Acknowledgment of accidents

17 months

The yes/no game

18 months

Kinship

Gradually between 10 and 18 months and 4 years

Social eating

18 months to 2 years

Full sentences

After 18 months

Spoken language

Gradually increasing during the second year

Counting

18 months to 3 years

Singing three-tone sequences

20 months

Clicking

2 years

“Come here” signal

2 years

Language proficiency suddenly arises

2–2.5 years

Behavioral control, rules, and polite address

18 months to 3 years

Epilogue The Role of Father Care Past, Present, and Future

When paternal behavior emerged in fossil hominins, it greatly affected the physiology and behavior of males. Over generations, father care shaped male reproductive biology and life history. Humans are the direct descendants of these ancestral males and have inherited the physiological patterns and life history traits of prior generations, whether or not caretaking of infants by socially recognized fathers is expressed as a cultural norm or family preference. The hormonal profiles of caretaker fathers are well established. For example, the prolactin response of human fathers, particularly stimulated by close association with neonates, and later with young infants and children, is arguably an adaptation of human males (Gettler et al., 2012a). The rise and continued expression of prolactin reduces the effects of testosterone. Without the circadian rise and fall of prolactin levels associated with father care, adult males are subject to unmitigated exposure to high testosterone levels over a reproductive lifetime, potentially increasing the probability of mortality. Fathers who are caregivers are documented to have lower levels of circulating testosterone than nonfathers, whether married or not (Gray et al., 2006), and morning testosterone levels are lower for involved fathers than their less interested counterparts (Gray et al., 2002). Furthermore, continued exposure to elevated levels of testosterone among males who never become fathers or who are detached fathers may possibly lead to higher rates of prostate cancer, given the sensitivity of the prostate gland to androgenic hormones (Alvarado et al., 2015). Married socially recognized fathers are known to experience greater longevity and fewer health problems (Gray and Anderson, 2010). Prolactin production occurs in fish, birds, mammals, and other vertebrates, and promotes reproduction and caretaking, including nest

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building, infant protection, provisioning, and in mammalian females, breast milk production. Elevated prolactin production in males has evolved in about 5 percent of vertebrate species to promote paternal behavior (Gettler et al., 2012a). This hormone was likely recruited at some point in human evolution to promote direct and indirect father care, which increased infant survivorship (Gettler, 2014). At some point in human evolution, females may have begun preferring male partners with the ability to modulate their hormonal profiles by increasing prolactin and decreasing testosterone during father care. Meanwhile, a less robust craniofacial complex was selected for in ancient humans, resulting in reduced phenotypic differences between females and males compared to the great apes (Lovejoy, 2009). Concomitantly, father care, with its reliance on the female-male pair-bond, allowed for the elongation of human life history, which inadvertently led to many of the cultural behaviors characterizing archaic humans, such as the Neandertals and living H. sapiens. These behaviors are largely traversed during the first three postnatal years. Human hunters and gatherers living today and documented in the ethnographic record preserve some of the lifeways inherited from the common ancestor of food producers and foragers (Hewlett, 1991). In many forager groups, these lifeways include a fierce egalitarian social structure, the two-parent family taking precedence over extended kin networks, and coparenting with mothers and socially recognized fathers. In contrast, food production within the past ten thousand years, followed by urbanism during the past five thousand years, increased inequality by limiting access to resources and separating the domestic and public spheres (see Figure 1.3). These factors reduced father-infant bonding among agriculturalists and severed it completely in pastoral economies with scarce resources (Katz and Konner, 1981). However, this is not how humans evolved and survived for tens to hundreds of thousands of years. Forager lifeways fundamentally altered male physiology and life history. Fatherless children fare worse than their counterparts in Western-style and forager societies (Egerton, 1939; Hill and Hurtado, 1996; Hewlett, 1992b). The behavioral flexibility of humans allows for an inactive or absent father to be partially compensated for by the attention of other family members and nonkin, but the lack of a strong positive paternal (or maternal) relationship can never be fully resolved. The extended family of agricultural populations partially replaced the traditional role of fathers among foragers. Farming communities are often multigener-

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ational, with those too old or too feeble to work in the fields contributing to the welfare of the group in other ways, such as infant care. In the absence of the extended family unit, parents often have a limited number of options for infant care. One option is for fathers to contribute heavily to infant care by shifting work schedules to accommodate the labor constraints of mothers and the waking hours of infants. However, this is often not possible or does not happen, resulting in the limiting of father-infant proximity in Western-style societies. Families with young children must often counterbalance the acquisition of status with the demands of infants during the first three years of postnatal development. This limitation has consequences for the reproductive biology of males and females, and may negatively affect the long-term hormonal profile of males who fail to engage in father care of infants. Meanwhile, the wants and needs of developing neonates and infants remain the same as in the evolutionary past (Hrdy, 2009). As primates, infant humans expect nearly constant proximity to their primary caretaker(s) during the first two to three years. These needs are often ignored in parenthood epistemologies that emphasize independence and individualism over cooperation and interdependence during infancy and childhood (Edwards et al., 2015). It may be that much of human personality, character, demeanor, and cognitive potential are determined from the growth of the brain that happens during this time interval (Champagne, 2014). Males can positively enhance infant maturation through infant carrying and caretaking. In industrial or postindustrial societies, fathers remain the only potential voluntary caretaker alternative to the mother in economically independent families.

Implications of Father Care for Humanity The importance of father care is profound. Half of all American children today will be without a biological father in the house sometime before adulthood. Early “socialization” or daycare may increase mental, behavioral, and physical diagnoses and psychoactive treatments of children. Furthermore, a common denominator found in investigations of violent crime, criminal behavior, suicide, depression, and substance abuse is absentee fathers (Lamb, 1981; Veneizano, 2003). Infants and children growing up without fathers are more prone to antisocial behavior in both Western and non-Western societies (Whiting and Whiting, 1975; Thomas et al., 1996; Lamb, 1997; Veneizano, 2000, 2003; Atzil et al., 2012). Furthermore, it is not only paternal proximity that positively impacts such characteristics as interpersonal aggression. On

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the contrary, it appears that it is paternal warmth and affection, rather than proximity alone, that decreases aggressive and hypermasculine behavior. In addition, father-infant interaction leads to an improved father-child relationship, which decreases the incidence of aggressiveness, interpersonal violence, substance abuse, and psychological disorders (Veneizano, 2003; Atzil et al., 2012). Father presence may also delay the reproductive maturation of their children (Ellis, 2004; Gray and Anderson, 2010), providing a greater amount of time for socialization. There is also evidence that paternal involvement in infancy improves the academic performance of children later in life (Williams and Radin, 1993). In mammals generally, infancy is the period between birth and the eruption of the first permanent molar when infants are weaned. This period is the first six years of life in humans (Keller et al., 2005), although most infants are weaned cross-culturally between two and three years (Bogin, 2006). By carrying and caring for infants, mothers and fathers may provide the closest approximation of how infants were successfully raised in the past (Gettler, 2010). From this perspective, social partnerships between spouses to care for infants may be a form of ancestral parenting, and seems to be optimal for infant development (Lamb, 1997; Veneziano, 2003; Apner-Levi et al., 2014). Indeed, father care during the first three years of life may have been a prime mover during the origin of humanity.

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Index Abipones, 48 Acetabular margin of the pelvis, 95 Acetabulum, 141 Ache, 16, 26, 45, 76, 80-86, 103, 118, 163 Achuelian hand axe, 178 Acknowledgment of Accidents and Shame, 175 Adaptation, 5, 8, 14, 66, 95, 118, 139, 141, 146, 175, 187 Adolescents, 15 Adorning the body, 177 Adulthood, 6, 14, 25, 54, 74 Adult mortality, 15 Affiliative behavior, 6, 11, 130 Africa: Central Africa, 14, 108, 109, 114; Congo, 45, 106; East Africa, 76, 105, 153; Gambia, 84; Kenya, 7, 53; Malawi, 114; North Africa, 105; South Africa, 153, 171; West Africa, 105 African apes (Homininae), 122 African wild dogs, 121 Affection, 167 Agnostic buffering, 131 Agriculturally based historic empires, 14 Agta (see also Cagayan Agta), 16, 45, 83, 103, 105, 106 Ainu, 46 Aka, 14-16, 45, 83, 103, 104, 106-108 Akicita, 116 Akuma, 113 Alfoeros, 47 Allantois, 35 Allen’s rule, 147 Alloparenting, 126 Alveolar, 95 Ahomana, 48 Amniotic cavity, 34 Amniotic fluid, 35-39 Amphibians, 161 Ampulla, 27

Ampullary–isthmic junction, 31 Andaman Islanders, 107 Androgens, 24, 27, 52 Angoni, 114 Aneuploidy, 23 Anterior, 39, 93, 140, 143 Anthropoids, 8 Antibodies, 37 Anuta, 110 Anyanja, 114 Arapaho, 116 Arawaks, 196 Arboreal, 4, 144, 181 Arboreal quadrupeds, 138 Archeological record, 17 Arginine vasopressin, 53 Art and Symbolic Communication, 171 Artiodactyla species (even-toed hooved animals), 120 Arunta, 74 Assam, 46 Atlanta, 53 Auricular surface, 93 Attachment, 151 Australia, 55, 74, 86, 109, 169, 171 Australasia, 45 Australopithecus: 138-147,152,175, 181183; A. afarensis, 2, 140, 142, 145, 147; A. africanus, 140, 142, 143; A. garhi, 146; A. afarensis A.L. 288–1, 145; A. africanus Sts 14, Member 4, 140 Archaic Homo sapiens, 182 Ardipithecus ramidus, 10 Aquatic ape Hypothesis, 137 Aye-ayes (Dabentonia madagascariensis), 152 Baby, 46, 56-60, 69 Baculum, 11 Baboon (also see Papio), 7, 11, 77, 78, 121-22, 124, 127, 130-134, 158

214

Index

Bagesu, 45 Balearic Islands, 45 Bangangté, 115 Bank Islands, 47 Bari, 16 Batek, 15-17, 43, 45, 55, 83, 84, 103, 104, 108, 166-168, 179 Beavers (Castor fiber), 121 Bearn, 45 Behavioral control and rules, 179 Behavioral reconstruction of archaic Homo sapiens, 182 Behavioral reconstruction of Homo erectus, 182 Black Sea, 45 Blastocyst, 161 Basque country, 45 Biceps brachialis, 148 Biceps radialis, 148 Biocultural synthesis of human fatherhood, 118 Bipedal locomotion, 4, 65, 137-142 Bonding, 45, 50, 54, 66, 86, 106, 113, 122, 127-129, 140, 152, 188 Brachial index (radius length / humerus length), 147 Brachial proportions, 146 Brachiators, 139 Brain to body ratio, 149 Brain size, 7-9, 13, 37, 132-134, 138, 140, 149, 152-159 Breastfeeding, 41, 169 Boeginese, 47 Bofi, 103, 108, 109 Boloki, 45 Bone cells, 36 Bonobo (Pan paniscus), 37, 80, 85, 125, 132, 163, 164, 171, 173, 176 Borneo, 47, 113 Bontok, 47 Brahmaputra Valley, 46 British Isles, 45 Brothers, 15, 42, 107, 111, 118 Bulbocavernosus muscle, 30 Busama, 19, 42, 46, 62, 68, 115, 163, 164, 170 Caesarian birth, 38 Cagayan Agta, 45, 83, 103, 105 Calcaneus, 141 Calculus, 94 Callitrichinae, 129

Calories, 11, 80-83, 85, 167, Cambrian explosion, 161 Cameroon, 68, 115 Canine, 7, 10, 89, 158 Capuchin (Cebus), 121-22, 127, 129, 152 Caribs, 48 Caribbean, 45, 101, 207 Carnivores, 119-121, 139, 173 Carrying infants, 1-4, 6, 8, 11-19, 60-67, 73, 83-97, 106-113, 118-123, 125-30, 132, 137-163, 181, 190 Caretaker-infant proximity, 55 Cartilaginous skeleton, 35 Catarrhine, 11 Caudal-cephalic ends, 161 Cave art, 9 Celts of Thrace and Scythia, 45 Cervical vertebra, 144 Cervix, 24, 30, 35, 38-39 Cetaceans, 120, 153, Charnov’s Model, 80-81 Cheshire, 45 Cheyenne, 116 Chimpanzees (Pan troglodytes), 10, 37, 78-85, 121-25-126, 133-134, 139-140, 143, 146, 152, 157-158, 162-168, 171, 173-177 China, 51, 129, 154 Chiriguanos, 48 Chorion, 34 Cilia, 27-28 Circadian rhythm, 25, 55 Clicking, 164 Clavicle, 26, 64, 90 Clitoris, 24, 35 Colic, 62 Come Here Signal, 177 Communicative sighing and blinking, 174 Condyle, 95, 141, 144 Conception, 18, 23, 26, 31-37 Conspecifics, 119, 126-127, 181 Cooperative autonomy, 104 Cosleeping, 5 Coronal suture, 91 Corpus luteum, 28 Corsica, 45 Cortisol, 52, 129 Corvids, 153 Counting, 69, 164 Couvade, 5, 44-51, 170 Couvade syndrome, 51

Index Cowper’s gland, 28 Coyotes (Canis latrans), 121 Crania, 153-57, 159 Cranial base flexion, 13 Cranial capacities, 180-82 Cranial vault, 155 Crawling, 64-66, 68, 88, 160, 163 Cries/crying, 16, 53-57 Crowning, 39 Cultural transmission of information, 152 Cursorial, 181 Cryptic ovulation, 10 Cyprus, 45 Dakota, 116 Dancing, 62, 160, 168 Daycare, 189 Deshasht Brahmans, 46 Deciduous dentition, 35, 62, 88-89 Defecation (see also elimination), 58, 59, 67 Delivery, 42-47, 129 Dentition, 35, 88, 157 Dental abscesses, 94 Dental carries, 94 Dental eruption, 78, 88-91 Deer mice (Peromyscus californicus), 120 Diapers, 69 Diaphragm, 13, 39 Dinkas, 45 Diploe, 91 Diploid, 27 Discipline, 73 Dopamine, 52 Dorsal, 63, 125, 130, 161 Dyadic social interactions, 63 Dyaks, 47, 113-114 Eburnation, 93 Ectoderm, 33 Ectocranially, 91 Efe, 15, 41, 58, 82, 103, 109, 151, 169, 174 Egalitarian societies, 104 Egg, 119-120 Egg-Laying animals, 119 Egg production, 24 Ejaculatory ducts, 23 Elbow, 95 Elimination (see also infant hygiene), 16, 55, 58, 61, 67-69, 104, 173 Elimination signaling, 173

215

Eleventh-twelfth week postnatal development, 62 Eighteen months-two years postnatal development, 71 Embodied Capital Hypothesis, 11, 81 Embryo, 161 Embryonic disk, 32 Empathy, 3, 18-19, 50-51, 53, 104, 162, 167, 183 Encephalization, 13 Enculturation, 6, 18, 125 Endocranially, 91 Endometrium, 25 Epaxial musculature, 63 Epididymis, 27 Epiphyses of the lower humerus, 89 Epiphyseal plates, 88-90 Erekulas, 46 Estradiol, 25 Estrogen, 25 Estrous females, 176 Europe, 44, 171 Evolved developmental niche, 55 Exposed pendulous scrotum, 10 Extrauterine, 140 Facial expressions, 171 Fallopian tubes, 24, 30, 35 Fat-tailed dwarf lemurs (Cheirogaleus medius), 128 Father care, 6, 87, 113, 183, 187 Federated States of Micronesia, 110 Feet, 4, 10, 43, 59, 63-67, 73, 126, 138, 143, 168, 175 Feral children, 77 Fertility, 82-86, 88, 96 Female choice, 10 Femoral head, 10, 95, 141, Femur, 93, 139, 141-42 Fetal and postnatal rates of brain growth, 155 Fetus, 36 Fibula, 141 Fifteenth-sixteenth week postnatal development, 63 Filipino, 52, 46 Fire, 5, 9, 42, 183 First trimester of pregnancy, 24 First and second postnatal week, 56 Follicular phase, 25 Food and object sharing, 166

216

Index

Fossil record, 3, 17, 24, 153, 161, 182 Foragers, 26, 41, 53-58, 74-75, 79-84, 95, 101-106, 113-16 Foramen magnum, 144 Fourth-sixth weeks in postnatal development, 59 Fourth-sixth month postnatal development, 64 Fox, 121 France, 76, 171 Fusion of the ovum-sperm nuclei, 31 Gelada baboon (Theropithecus gelada), 131 Gestation, 14, 23-24, 37-38, 45, 50-52, 77-78, 125, 133, 157, 161 Gesticulation, 164 Gibbons (Hylobates), 132 Gidra, 76 Glenoid fossa of the scapula, 95 Gluteal muscles, 138 Gogo, 76, 116 Gonads, 24 Gonadotropin, 27 Gorilla: 7, 37, 79, 86, 121, 125, 132, 140, 146, 152, 173; G. gorilla gorilla (western lowland gorilla), 132; G. beringei beringei (mountain gorilla), 132 Gould, S. J., 18, 159 Gracile, 18 Grammars of action, 13 Grandmothers, 6, 11-12, 80-81 Grandmother hypothesis, 11, 80 Granulosa cells, 28 Great Nicobar, 46 Grooming, 56, 122, 126-128, 130, 132, 133 Group identity, 177 Growth spurt, 26 Guenons, 122 Guiana, 47, 49 Hadza, 3, 11, 12, 16, 53, 76, 80, 83 Haeckel’s Law, 18 Hand signals, 65 Hanuman langurs (Semnopithecus entellus), 130 Hallux, 141 Hand holding, 173 Haploid, 27 Haplorhini (monkeys and apes), 122 Hearths, 183

Heel bone (see also calcaneus), 141, 143 Height, 13, 75, 93, 134, 156, 175 Herders, 14, 101, 116 Hind limbs, 160 Hindu, 46 Hiwi, 16, 81, 83, 85 Homo erectus (ergaster): 1, 14, 138, 182, 153-54, 18; KNM-ER 1470, 153154, 181; KNM-ER 1813, 153-154; KNM-ER 1805, 153; KNM-ER 1470, 153-154, 181; KNM-ER 3733, 153154, 181; KNM-WT 15000 (see also Nariokotome boy), 140, 153, 181; KNM-ER 3883, 153, 181 Homo habilis, 147, 153, 181 Homo heidelbergensis, 153, 181 Hopi, 105, 115, 116 Hormonal profiles, 187 Horticulturalists, 14, 101, 105, 110, 163 Howlers (Alouatta), 122 Human neoteny, 157 Humerus, 89, 95, 139, 146-148, 151, 181 Humerus length, 146 Hunting, 15, 45, 49, 54, 76, 81-87, 96, 101, 106, 110-116, 152, 173, 182 Hunter-gatherers, 5, 11, 15, 87, 103, 108, 109, 138, 166 Hyenas, 121 Hyoid, 13 Hyper-encephalization, 14, 149, 151-159 Hyper-encephalization of neonates, 149 Hypothalamus, 24-25, 27-28, 35, 55 Iberian Peninsula, 45, 181 Ilium, 92, 137, 141, 143, 145 Ifaluk, 110 Imitation, 13, 70, 73, 166, 169 Implantation, 32 Incisors, 62, 87-89, 189 India, 46, 102 Industrial economies, 14 Infant carrying (see carrying), 66, 73, 83, 118, 125, 128, 137, 144-148, 163, 181-189 Infant distress, 6, 53 Infant hygiene, 6, 62, 67 Infant mortality, 103 Intense sociality, 162 Intentional facial expressions, 171 Interbirth interval, 85 Interosseous crest, 145 Interosseus margin, 145

Index Invertebrates, 119 In vitro fertilization, 26 Ischium, 141 Jackals, 121 Jivaro, 48 Joint attention, 66 Juri, 48 Juvenilized morphology, 18 Kaluli, 69 Kamchatka, 46 Kasanje, 45 Knees, 42, 65, 83, 95, 115, 141-142, 174 Kin, 81, 87, 105 Kinship, 169 Kiss, 167 Knock-kneed, 141 Koramas, 46 Koravar, 46 !Kung, 5, 16, 65, 76, 82, 84, 103, 118 Kwakiutl, 116 Lactation, 52, 125, 129, 157 Labor, 38 Lagomorphs, 121 Lake Victoria, 45 Language, 12 Language explosion, 178 Lanugo, 37 Larynx, 13 Lateral epicondyle (see also lower humerus), 148 Laetoli footprints, 2 Leaf monkeys, 122, 126 Leg bone epiphyses, 90 Lemur, 122 Lesse, 103-104 Lesu, 103, 114 Leper’s Island, 47 Life history Theory, 77 Life-span, 11, 78-79 Limb bud swellings, 35 Leontopithecus (golden lion tamarin), 129 Lips, 65 Liver, 34 Longevity, 76-82, 86, 96, 153, 187 Longitudinal abdominal muscles, 64 Lordosis of the spine, 60, 66 Lorises, 57, 85, 121-123 Lower epiphysis of the radius, 89

217

Lower sacral vertebrae, 90 Lower segment of the rib cage, 64 Luteinizing hormone, 27 Luteal phase, 25 Lying-in, 44 Macassarese, 47 Macaques: 11, 74, 121-122, 124, 126, 130-131, 164: M. Sylvanus (Barbary macaque), 130; M. fuscata (Japanese macaques), 126, 130; M. fascicularis (crab-eating macaque), 126; M. mulatta (Rhesus macaque), 126; M. nemistrina (pig-tailed macaque), 126; M. thibetana (Tibetan macaques), 130 Macroporosity, 93 Macusis, 47 Magi, 110 Malaria, 163 Malaysian peninsula, 47 Malinowski, B., 50, 110-113 Male-infant proximity, 14, 106 Male-male competition, 158 Male social obligations, 1 Male reproductive careers, 82 Man the hunter hypothesis, 137 Married and unmarried male hormone differences, 53 Marmosets: 11, 122, 127, 129, 176; Callithrix jacchus (common marmoset), 129 Masticatory maturation, 159 Matrifocal, 105 Maasai, 86 Masculinized cultures, 16 Maturation, 18, 24-28, 46, 57, 62, 76-77, 80-82, 87-91, 95, 107, 118, 120, 133, 138, 140, 157-159, 180, 189, 190 Meiotic division, 28 Melanesia, 47 Menarche, 25 Mentawi Islands, 47 Mesoderm, 34 Midwife, 42-43 Milk teeth, 35, 62 Mimicking, 57 Mitosis, 161 Miri, 46 Medial epicondyle, 90 Molars, 77-78, 86, 88-89 Mongoose, 121 Monogamous, 53, 113, 120-121, 127-128, 132

218

Index

Monomorphism, 10 Mortality rates, 79- 81 Morula, 32 Mousterian cultures (see Neandertals), 171 Mouth brooding, 120 Mumbai, 46 Multimale/multifemale groups, 131 Müllerian ducts, 24, 35 Mundzucu, 48 Musical instruments, 169 Mutual gazing, 163 Myelination, 37 Nayadis, 46 Neandertals (Homo sapiens neandertalensis), 8-9, 14, 147, 154, 171, 180-183, 188 Negative emotional states, 63 Nematodes, 161 Neolithic revolution, 118 Neolocal, 87 Neonate, 6, 12, 15, 37-42, 44, 50, 54-60, 86, 123-125, 128, 133, 144, 149, 155159, 187 Neonatal period, 56 Nest, 49, 120-121, 128, 132, 173 Neotenic, 18, 157 Neoteny, 157-159 Neural arches, 63 Neurons, 34-37 Neural tube, 33 New Ireland, 114 New Mexico, 48, 80 New World monkeys, 126, 128 New Zealand, 74 Ngecha, Kenya, 7 Night season, 5 Ninth-tenth week postnatal development, 62 Nipples, 24 Nonhuman primates, 2-3, 7, 10, 17-18, 38, 55-56, 60, 74-79, 85, 87, 119-41, 152, 157 Nonhuman primate mothers, 18 Notochord, 161 Nutrients, 161 Occipital bone, 63 Ojibwa, 117 Old World monkeys, 14 Ontogeny, 13, 18, 150, 155, 160, 162, 166

Oocyte, 28 Orangutans (Pongo pygmaeous), 37, 79, 80, 86, 121-122, 140, 146, 152, 173 Ossification, 88-90 Osteoarthritic lipping, 93 Osteophytes, 94 Organization, 172 Orphans, 132 Ovary cells, 35 Oviduct infundibulum, 28 Ovulation, 10, 25, 28, 30, 129 Ovum, 161 Owl monkey (Aotus), 7, 128-129 Oxfordshire, 45 Oxytocin, 6, 52, 53 Pair bond, 7-12, 38, 52, 82-87, 112-113, 120, 128, 133, 137, 140, 152, 188 Paleodemographic, 82 Papio: 130, 131, 134, 158; P. anubis (olive baboons), 130, 134; P. cynocephalus (yellow baboon), 130; P. hamadryas (hamadryas baboon), 131; P. ursinus (Cape baboon), 131 Paternal proximity, 189 Papua New Guinea, 42, 62, 68, 76, 105, 110, 111, 115, 152, 163, 169, 170 Passem, 48 Paraguay, 16, 48 Paraiyan, 46 Parietal bones, 91 Parturition, 41-42, 48, 125, 129 Patas monkeys (Erythrocebus patas), 126 Paternal behavior, 3, 14-15, 18, 23, 86, 101, 105- 110, 113, 119 Paternal involvement, 132, 183, 187-188 Pawnee, 116 Pech de l’Azé (see also Neandertal), 182 Pectoralis muscles, 148 Perineum, 39 Peromyscus maniculatus. 120 Penis, 7, 11, 24, 30, 35, 39, 97 Perissodactyls (odd-toed ungulates), 120 Peromyscus maniculatus, 120 Petivares, 48 Phalaropidae, 120 Philippine Islands, 47 Phonemes, 72 Phylogeny, 18, 122, 160 Piojes, 48 Placenta, 37 Play, 73

Index Pleistocene, 145 Pituitary glands, 35 Pointing, 164 Poison-arrow frog, 120 Polygamous, 10, 104 Polygynous, 15, 86 Polynesia, 111 Pomla, 46 Pongo pygmaeus (orangutan), 37, 46, 79, 80, 86, 121-122, 140, 146, 152, 173 Postconception, 36, 37 Posteriorly, 37, 93, 140, 143 Postmenopausal, 11, 80-81 Postnatal, 49, 55-59, 61-69, 71-75, 83-89, 97, 111-118, 125-128, 132-134, 140157, 162-189 Postpartum, 41, 45, 50-51, 128-129 Post-reproductive life, 79, 96 Post reproductive longevity, 79 Precontact California, 48 Predators, 174 Premolars, 89 Prenatal Development, 161 Prey, 174 Primates, 2-3, 7-11, 17-18, 38, 55-66, 74, 77, 85, 119-133, 141, 152-158, 161-164, 174-177, 189 Primate behavioral ecology, 17 Primate sociality and brain growth, 132 Primiparous, 39 Primordial gonadal streak, 35 Prenatal cranial capacity, 156 Progesterone, 25, 28 Prolactin, 4, 40, 52-53, 129, 130, 187, 188 Pronator muscles, 145, 148 Prosimian infants, 121 Prostate, 24, 27, 30, 35, 187 Protein, 11, 80-81, 152 Provisioning, 7, 11, 49, 54, 80-87, 96, 106, 116, 120, 126, 152, 167, 183, 188 Proximate mechanisms of father care, 86 Puberty, 24, 25-27, 36, 77, 89 Pubic hair, 25 Pubic symphysis, 92-93 Pubis, 141 Putumayo, 48 Quickening, 36 Radiator hypothesis, 137 Radius length, 147

219

Reproduction, 30 Reproductive fitness, 60, 119 Reproductive physiology, 36 Reptiles, 120, 161 Rio Yupura, 48 Rodents, 119-120 Russia, 51, 172 Sacrum, 92-93, 137, 141-144 Sacroiliac joints, 92 Sagittal suture, 91 Sahelanthropus tchadensis, 138, 180 Samoa, 69, 175, 179 San Christobol, 47 Santa Fe, 48 Sargon of Akkad, 9 Savanna hypothesis, 137 Scapula, 64 Sciatic notch, 141 Scotland, 44 Sea horses, 120 Secondary sexual characteristics, 23 Second trimester, 36, 162 Seed-predation hypothesis, 137 Self-soothe, 62 Seminal vesicles, 10, 24, 27, 30, 97 Sertoli/Leydig cells, 24, 27 Seventh-eighth weeks postnatal development, 61 Seventh-ninth month postnatal development, 65 Sex chromosomes, 23 Sexual display hypothesis, 137 Sexual intercourse, 30, 38, 113 Sex-linked genetic traits, 23 Sexual maturation, 24-26 Shame, 175 Sharing, 166 Shared gazing, 163 Shoulders, 66, 95, 113, 115 Siamangs (Symphangus syndactylus), 132 Siblings, 6, 73, 79, 106, 112, 126-127, 169 Siberia, 182 Sifaka (Propithecus verreauxi), 57, 123, 127 Signally affirmative and negative, 170 Silverback male, 132 Singing, 176 Sisters, 15, 111 Sling, 4, 60-62, 64, 65, 107, 108, 145, 163 Skeletal decline, 91

220

Index

Skull, 35, 144 Sleep, 5-6, 17, 116, 36-37, 42, 51, 55, 60-63, 132, 173, 183 Slovenia, 18 Skeletal and muscle anatomy of infant carrying, 148 Pronation, 148 Sociality, 162 Social eating, 176 Social emotions, 18 Social status, 15, 111, 152, 179 Socially recognized fathers, 187 Social reciprocity, 11 Solomon Islands, 110 Somatic growth, 60, 77 Somites, 36 Sonjhara caste, 46 South Asia, 46 Southeast Asia, 46 Sperm, 10, 24-26, 28, 30, 31, 32, 35, 38, 97, 161 Spermatogenesis, 25, 27, 52 Spermatozoa, 26-28, 30-31 Spermatogonia, 27 Spermatid, 27 Sperm counts, 10 Sperm-producing cells, 35 Spinal column, 93 Spinal cord, 30, 34-36, 64, 161 Spinous processes, 93 Sternocleidomastoid muscles, 64 Sternum, 64 St. Iago, 48 Storytelling, 65 Strepsirrhine, 123 Stone tools, 8-13, 137, 176, 182 Swartkrans, 9 Sweat glands, 25 Subadulthood, 77, 81, 157 Subsistence farmers, 11, 15, 26, 111, 115 Sudan, 45 Sumatra, 47 Supination, 145, 148 Supinator muscles, 148 Superior neurocranium, 92 Superior pubic ramus, 143 Suprachiasmatic nucleus, 55 Suriname, 48 Squat foraging, 137 Squirrel monkeys (Samiri sciureus), 122 Symbols, 8, 9, 12, 70, 166, 178, 184 Symbolic thought, 13

Syntax, 12, 69, 73, 179 Synapses, 35-36 Tagals, 47 Tail, 27, 31, 35-36 Tamarins: 11, 122, 127, 129, 176; Leontopithicus (golden lion tamarin), 129; S. fuscicollis (saddle-back tamarin), 129; Saguinus oedipus (cotton-topped tamarin), 129 Tangkhuls, 46 Tarsiers, 57, 121-123 Tarumas, 48 Testes, 10, 24- 27, 30, 35, 53 Testosterone, 4, 24, 25, 27, 35, 36, 52, 53, 97, 129, 187, 188 Terrestrial-feeding strategies hypothesis, 137 Thailand, 51, 68 Theory of mind and deception, 167 Third trimester, 37 Third week post-natal development, 57 Thirteenth and fourteenth week post-natal development, 63 Thumb, 161 Thumb-sucking, 57 Tibia, 95, 141 Titis (Callicebus), 129 Tikopia, 111 Time-out /Time-in, 74 Timor Laut, 47 Toilet training, 67 Tools, 178 Twelve-eighteen months postnatal development, 70 Twins, 42, 128 Two to 2.5 Years postnatal development, 73 Two and a half -three years postnatal development, 70 Tracking, 59 Transverse processes, 93 Trobriand Islanders, 111-113 Trochlear notch, 95 Tropical otters, 121 Trophoblast-derived cells, 33 Trunk, 36, 64, 66, 93, 138-139, 141 Turkestan, 46 Turn-taking, 166 Tupe, 48 Tyrannosaurus rex, 144

Index Umbilicus/ umbilical cord, 34, 40-43 Ungulates, 119-120, 139, 174 Ulna, 4, 95, 145-148 United States, 51, 102, 115, 172 Upper Paleolithic, 171 Upper Pleistocene, 171 Upper radius, 148 Urban, 80, 87, 101-102, 188 Urinary organs, 35 Urethra, 27, 30 Uterine wall, 28, 32, 34, 39-40 Uterus, 28-41 Vagina, 30, 35, 38-39 Vas deferens, 10, 24, 27, 30, 35 Vasopressin, 54 Verbs, 46 Ventral, 40, 63, 92- 93, 120, 125, 130 Ventral rampart, 93 Vertebrate species, 2, 188 Vertebral, 36, 64, 83, 90-94, 161 Vertical postures, 57 Vernix caseosa, 37 Vocabulary, 70-73, 178 Vocalizations, 48, 57-58, 71, 125, 165, 169- 170, 175, 185

221

Waist, 141 Walking to running, 174 Warrior states, 14 Weaning, 60, 73, 77, 79, 89, 109, 121, 157 West Indies, 48 Wisdom tooth, 89 Wolves (Canis lupus), 3, 121, 173 Woman the gatherer hypothesis, 137 Words, 67 Wrist, 145, 148 X chromosome, 23 Xhosa, 70, 165 Yao, 114 Yanomanö (Amazon basin), 82, 84, 114 Y chromosome, 23 Yes/No Game, 175 Yolk sac, 34 Yuma, 116 Zardandau, 46 Zhoukoudian cave, 154 Zona pellucida, 30 Zygote, 161