Beyond Cladistics: The Branching of a Paradigm 9780520947993

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B E YO N D C L A D I S T I C S

SPECIES AND SYSTEMATICS

www.ucpress.edu/go/spsy The Species and Systematics series will investigate fundamental and practical aspects of systematics and taxonomy in a series of comprehensive volumes aimed at students and researchers in systematic biology and in the history and philosophy of biology. The book series will examine the role of descriptive taxonomy, its fusion with cyber-infrastructure, its future within biodiversity studies, and its importance as an empirical science. The philosophical consequences of classification, as well as its history, will be among the themes explored by this series, including systematic methods, empirical studies of taxonomic groups, the history of homology, and its significance in molecular systematics. Editor in Chief: Malte C. Ebach (University of New South Wales, Australia) Editorial Board Marcelo R. de Carvalho (Universidade de São Paulo, Brazil) Anthony C. Gill (Arizona State University, USA) Andrew L. Hamilton (Arizona State University, USA) Brent D. Mishler (University of California, Berkeley, USA) Juan J. Morrone (Universidad Nacional Autónoma de México, Mexico) Lynne R. Parenti (Smithsonian Institution, USA) Quentin D. Wheeler (Arizona State University, USA) John S. Wilkins (University of Sydney, Australia) Kipling Will (University of California, Berkeley, USA) David M. Williams (Natural History Museum, London, UK) University of California Press Editor: Charles R. Crumly

BEYOND CLADISTICS T H E B R A N C H I N G O F A PA R A D I G M

Edited by David M. Williams and Sandra Knapp

UNIVERSITY OF CALIFORNIA PRESS BERKELEY

LOS ANGELES

LONDON

University of California Press, one of the most distinguished university presses in the United States, enriches lives around the world by advancing scholarship in the humanities, social sciences, and natural sciences. Its activities are supported by the UC Press Foundation and by philanthropic contributions from individuals and institutions. For more information, visit www.ucpress.edu. Species and Systematics, Vol. 3 For online version, see www.ucpress.edu University of California Press Berkeley and Los Angeles, California University of California Press, Ltd. London, England © 2010 by The Regents of the University of California Library of Congress Cataloging-in-Publication Data Beyond cladistics: the branching of a paradigm/edited by David M. Williams and Sandra Knapp. p. cm.—(Species and systematics; v. 3) Includes bibliographical references and index. ISBN 978-0-520-26772-5 (cloth : alk. paper) 1. Cladistic analysis. 2. Biogeography. I. Williams, D. M. II. Knapp, Sandra. QH83.B49 2010 578.01'2—dc22 2010010575 Manufactured in the United States of America 19 10

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The paper used in this publication meets the minimum requirements of ANSI/NISO Z39.48-1992 (R 1997) (Permanence of Paper). Cover illustration: Sunflowers (Helianthus annuus) in Enfield, North London, UK. Photo by Lorraine Williams.

Contents

Contributors

vii

Preface

xi

PA R T O N E

ON CHRIS

Bibliography of Works by Chris Humphries 1

Chris Humphries, Cladistics, and Connections

3 19

David M. Williams, Kåre Bremer, and Sandra Knapp 2

Ontogeny and Systematics Revisited: Developmental Models and Model Organisms

35

Stephen Blackmore and Alexandra H. Wortley 3

Rooted in Cladistics: Chris Humphries, Conservation—and Beyond?

47

Richard I. Vane-Wright 4

Do We Need to Describe, Name, and Classify All Species?

67

Quentin D. Wheeler 5

Floras to Phylogenies: Why Descriptive Taxonomy Matters Sandra Knapp and J. Robert Press

77

vi / CONTENTS

PA R T T W O

B O TA N Y 6

Island Hot Spots: The Challenge of Climate Change

91

David Bramwell 7

Endemism and Evolution of the Macaronesian Flora

101

Mark A. Carine, Arnoldo Santos-Guerra, I. Rosana Guma, and J. Alfredo Reyes-Betancort 8

Early British Collectors and Observers of the Macaronesian Flora: From Sloane to Darwin

125

Javier Francisco-Ortega, Arnoldo Santos-Guerra, Charlie E. Jarvis, Mark A. Carine, Miguel Menezes de Sequeira, and Mike Maunder PA R T T H R E E

CLADISTICS 9

Monophyly and the Two Hierarchies

147

Olivier Rieppel 10

Beyond Belief: The Steady Resurrection of Phenetics

169

David M. Williams, Malte C. Ebach, and Quentin D. Wheeler 11

Monographic Effects on the Stratigraphic Distribution of Brachiopods

197

Gordon B. Curry 12

The Eukaryote Tree of Life

219

Diana Lipscomb PA R T F O U R

BIOGEOGRAPHY 13

Tethys and Teleosts

243

Peter L. Forey 14

East–West Continental Vicariance in Eucalyptus Subgenus Eucalyptus

267

Pauline Y. Ladiges, Michael J. Bayly, and Gareth J. Nelson 15

Wallacea Deconstructed

303

Lynne R. Parenti and Malte C. Ebach

Index

319

About the Editors

331

Contributors

Michael J. Bayly The University of Melbourne, Australia [email protected] Stephen Blackmore Royal Botanic Garden Edinburgh, United Kingdom [email protected] David Bramwell Jardín Botánico Viera y Clavijo, Spain [email protected] Kåre Bremer Stockholm University, Sweden [email protected] Mark A. Carine The Natural History Museum, United Kingdom [email protected] Gordon B. Curry University of Glasgow, United Kingdom [email protected]

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Malte C. Ebach University of New South Wales, Australia [email protected] Javier Francisco-Ortega Florida International University; Fairchild Tropical Botanic Garden [email protected] Peter L. Forey The Natural History Museum, United Kingdom [email protected] I. Rosana Guma Unidad de Botánica Aplicada, Instituto Canario de Investigaciones Agrarias, Jardín de Aclimatación de La Orotava, Spain [email protected] Charlie E. Jarvis The Natural History Museum, United Kingdom [email protected] Sandra Knapp The Natural History Museum, United Kingdom [email protected] Pauline Y. Ladiges The University of Melbourne, Australia [email protected] Diana Lipscomb George Washington University [email protected] Mike Maunder Al Ain Wildlife Park and Resort, Abu Dhabi; Florida International University; Fairchild Tropical Botanic Garden [email protected] Miguel Menezes de Sequeira Universidade da Madeira Campus da Penteada, Portugal [email protected]

CONTRIBUTORS / ix

Gareth J. Nelson The University of Melbourne, Australia [email protected] Lynne R. Parenti National Museum of Natural History, Smithsonian Institution [email protected] J. Robert Press The Natural History Museum, United Kingdom [email protected] J. Alfredo Reyes-Betancort Unidad de Botánica Aplicada, Instituto Canario de Investigaciones Agrarias, Spain [email protected] Olivier Rieppel The Field Museum [email protected] Arnoldo Santos-Guerra Jardín de Aclimatación de La Orotava, Spain [email protected] Richard I. Vane-Wright National Endowment for Science, Technology and the Arts, United Kingdom; Durrell Institute of Conservation and Ecology (DICE), University of Kent, Canterbury; The Natural History Museum, United Kingdom [email protected] Quentin D. Wheeler Arizona State University [email protected] David M. Williams The Natural History Museum, United Kingdom [email protected] Alexandra H. Wortley Royal Botanic Garden Edinburgh, United Kingdom [email protected]

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Preface

This book represents an attempt to document the nature and anticipate the future of cladistics. Inspired by the career and contributions of Chris Humphries, recently retired and now deceased botanist of the Natural History Museum (London), the breadth and depth of this one transformative career reflects decades of scientific advancement as well as the origination and wide acceptance of cladistics and its multifarious applications to botany, conservation, and biogeography. Why Beyond Cladistics? The initial idea came from Gary Nelson (Patterson 1997; Nelson 2000) reporting a statement made by Colin Patterson: The cladistic revolution “began in the late 1960s, accelerated in the 1970s, and was virtually complete by the eighties.” The word virtually leaps out from the page. The statement might be contrasted with another, from a later Gary Nelson chapter title (Nelson 2004): “Cladistics: Its Arrested Development.” Rather than the heavy anticipation captured in the potential meaning of virtually, Nelson’s title implies something altogether different, that there is still a way to go, progress being halted, unnaturally so, and the cause of the arrest obscure and unidentified. Our original intention was to explore the possibilities that lie beyond cladistics, regarding cladistics as the single dominating methodology of systematics. One might view cladistics as part of the fabric of systematics and evolution, but this is not always evident, and, so it seems, from generation to generation “cladistic thinking” needs to be rediscovered: xi

x i i / P R E FA C E

“What, then, of cladistics in relation to the history of systematics? If cladistics is merely a restatement of the principles of natural classification, why has cladistics been the subject of argument? I suspect that the argument is largely misplaced, and that the misplacement stems, as de Candolle suggests, from confounding the goals of artificial and natural systems” (Nelson 1979: 20). Are arguments misplaced? Are there any arguments left at all? Have things changed for the better, or are issues becoming obscure all over again? The contributors here have understood Beyond Cladistics in a variety of ways, its general meaning becoming obscured by different perceptions of the personal past. The chapters herein reflect some of those differences. We consider this a virtue. After some thought, we decided to add a subtitle, The Branching of a Paradigm, the additional words designed, we hope, to convey the many ways in which cladistics has wrought changes in systematics and comparative biology. Although cladistics and botany figure prominently and reflect Chris Humphries’s impact, there are also chapters on species concepts, homology, biological conservation, biogeography (of fishes and flowers), historical matters, and a little on the “presumed-dead-but-apparently-not” subject of phenetics. The sense of change in the past three decades, however, can be appreciated in the titles of two lectures given by Chris: “Systematics—An Optimal Solution Is a Slippery Thing” and “What Is Systematics?” The first lecture was by Chris, the neophyte botanist, in 1985; the second was again by Chris, as professor and the president of the Systematics Association, in 2003. The settings, too, were studies in contrast and trajectory: The 1985 lecture was given in the murky depths of the Natural History Museum’s paleontology seminar room, and, nearly 20 years later, the second lecture was given amid the grandeur of the Linnean lecture hall. Cladistics had come a long way, and so had Chris. Many helped in the creation and execution of this book. The original idea was conceived by Richard Bateman, Paula Rudall, and Dennis and Jan Stevenson; Ruth Temple, David Cutler, and Kate Longhurst at the Linnean Society of London gave freely their help and guidance; and we thank Johannes Vogel from the Natural History Museum for his own and his department’s support, performing as last of the three Keepers of Botany still living that Chris worked with (the other two were Steve Blackmore and Richard Bateman). The creation of this book brought to life old memories

P R E FA C E / x i i i

and began new thoughts—a real tribute to Chris Humphries and his impact on those whose lives he affected and continues to influence. David M. Williams and Sandra Knapp Department of Botany The Natural History Museum Cromwell Road London SW7 5BD United Kingdom

Chris Humphries

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REFERENCES Patterson C. 1997. Molecules and morphology, ten years on. Lecture presented at Molecules and Morphology in Systematics, March 24–28, 1997, Paris. Nelson G. 1979. Cladistic analysis and synthesis: Principles and definitions, with a historical note on Adanson’s Familles des Plantes. Syst. Zool. 28: 1–21. Nelson G. 2000. Ancient perspectives and influence in the theoretical systematics of a bold fisherman. In: Forey P.L., Gardiner B.G., Humphries C.J., editors. Colin Patterson (1933–1998): A celebration of his life. The Linnean, Special Issue No. 2: 9–23. Nelson G.J. 2004. Cladistics: Its arrested development. In: Williams D.M., Forey P.L., editors. Milestones in systematics. Boca Raton (FL): CRC Press pp. 127–147.

PA R T O N E

ON CHRIS

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BIBLIOGRAPHY OF WORKS BY CHRIS HUMPHRIES Divided by Category and Ordered Chronologically

PAPERS 1. Bramwell D., Humphries C.J., Murray B.G., Owens S.J. 1971. Chromosome numbers in plants from the Canary Islands. Bot. Notiser 124: 376–382. 2. Bramwell D., Humphries C.J., Murray B.G., Owens S.J. 1972. Chromosome studies in the flora of Macaronesia. Bot. Notiser 125: 139–152. 3. Humphries C.J. 1974. Plant Conservation. In: Harroy J.-P., Tassi F., Pratesi F., Humphries C.J., editors. National parks of the world. London: Orbis Publishing pp. 121–128. 4. Humphries C.J. 1975. Cytological studies in the Macaronesian genus Argyranthemum. (Compositae: Anthemideae). Bot. Notiser 127: 239–255. 5. Humphries C.J. 1976. A revision of the Macaronesian genus Argyranthemum Webb ex Schultz Bip. Bull. Brit. Mus. (Nat. Hist.), Bot. 5: 145–240. 6. Humphries C.J. 1976. Evolution and endemism in Argyranthemum Webb ex Schultz Bip. (Compositae: Anthemideae). Bot. Macaronesica 1: 25–50. 7. Ehrendorfer F., Schweizer D., Greger H., Humphries C.J. 1977. Chromosome banding and synthetic systematics in Anacyclus (Asteraceae—Anthemideae). Taxon 26: 387–394. 8. Heywood V.H., Humphries C.J. 1977. Anthemideae—systematic review. In: Heywood V.H., Harborne J.B., Turner B., editors. Biology and chemistry of the Compositae. London: Academic Press pp. 818–893. 9. Humphries C.J. 1977. A new genus of Compositae from North Africa. Bot. Notiser 130: 155–161. 10. Humphries C.J. 1978. [Notes on the genera] Phleum, Taeniatherum, Dasypyrum, Aegilops and Triticum. In: Heywood V.H., editor. Flora Europaea Notuleae systematicae ad Floram Europaea pertinantes. 20. Bot. J. Linn. Soc. 76: 337–343, 361–362, 368–369.

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11. Humphries C.J., Murray B.G., Boquet G., Vasudevan K. 1978. Chromosome numbers of phanerogams from Morocco and Algeria. Bot. Notiser 131: 391–406. 12. Humphries C.J. 1978. In: Heywood V.H., editor. Flora Europaea Notuleae systematicae ad Floram Europaea pertinantes. 20. Corrigenda et addenda. Bot. J. Linn. Soc. 78: 236. 13. Humphries C.J. 1979. Endemism and evolution in Macaronesia. In: Bramwell D., editor. Plants and islands. London: Academic Press pp. 171–199. 14. Humphries C.J. 1979. A revision of the genus Anacyclus L. (Compositae: Anthemideae). Bull. Brit. Mus. (Nat. Hist.), Bot. 7: 83–142. 15. Humphries C.J. 1980. Triticum, Koeleria, Hordeum, Hordelymus, Phleum, Dasypyrum, Lolium, Festulolium, Psathyrostachys, Taeniatherum. In: Tutin T.G., Heywood V.H., Burges N.A., Valentine D.H., Walters S.M., Webb D.A., editors. Flora Europaea 5: 153–154, 202–205, 218–220, 239. 16. Tutin T.G., Humphries C.J. 1980. Aegilops. In: Tutin T.G., Heywood V.H., Burges N.A., Valentine D.H., Walters S.M., Webb D.A., editors. Flora Europaea 5: 200–202. 17. Humphries, C. J., Richardson P.M. 1980. Hennig’s methods and phytochemistry. In: Bisby F., Vaughan J.G., Wright C.A., editors. Chemosystematics: Principles and practice. London: Academic Press pp. 353–378. 18. Carter H.B., Diment J.A., Humphries C.J., Wheeler A. 1981. The Banksian natural history collections of the Endeavour voyage and their relevance to modern taxonomy. In: Price J., Wheeler A., editors. History in the service of systematics: Papers from the conference to celebrate the centenary of the British Museum (Natural History) 13–16 April, 1981. Society for the bibliography of natural history, special publications 1 pp. 61–70. 19. Humphries C.J. 1981. Cytogenetic and cladistic studies in Anacyclus (Compositae: Anthemideae). Nord. J. Bot. 1: 83–96. 20. Humphries C.J. 1981. Biogeographical methods and the southern beeches. In: Forey P.L., editor. The evolving biosphere, London: BMNH/Cambridge University Press pp. 282–297 [Chinese translation: Biogeographical methods and the southern beeches. In Chow, M.-C., M.-M. Chang, Y.-Y. Chen, and M. Zhu (eds.), Geli fenhua shenwudilixue yiwenji [Vicariance biogeography: A collected translation], pp. 215–231.] 21. Humphries C.J. 1981. Biogeographical methods and the southern beeches. In: Funk V.A., Brooks D.R., editors. Advances in cladistics: Proceedings of the 1st meeting of the Willi Hennig Society. New York: New York Botanical Garden, pp. 177–207. 22. Humphries C.J. 1983. Primary data in hybrid analysis. In: Platnick N.I., Funk V.A., editors. Advances in cladistics: Proceedings of the 2nd meeting of the Willi Hennig Society. New York: Columbia University Press pp. 89–103. 23. Humphries C.J. 1983. Biogeographical explanations and southern beeches. In: Sims R.W., Price J.H., Whalley P.E.S., editors. Evolution, time and space: The emergence of the biosphere. London: Academic Press. pp. 335–365. [Russian translation published in Progress (Moscow), 1988.] 24. Humphries C.J. 1983. Vicariance biogeography in Mesoamericana. Ann. Missouri Bot. Garden 69: 444–463.

BIBLIOGRAPHY OF WORKS BY CHRIS HUMPHRIES / 5

25. Ladiges P.Y., Humphries C.J. 1983. A cladistic study of Arillastrum, Angophora and Eucalyptus (Myrtaceae). Bot. J. Linn. Soc. 87: 105–134. 26. Ladiges P.Y., Humphries C.J., Brooker M.I.H. 1983. Cladistic relationships and biogeographical patterns in the peppermint group of Eucalyptus (Informal subseries Amygdalinae, subgenus Monocalyptus) and the description of a new species, E. willisii. Austral. J. Bot. 31: 565–584. 27. Humphries C.J. & Funk V.A. 1984. Cladistic methodology. In: Heywood V.H., Moore D.M., editors. Current concepts in plant taxonomy. London: Academic Press pp. 323–362. 28. Diment J.A., Humphries C.J., Newington L., Shaughnessy E. 1984. Catalogue of the Natural History drawings by Joseph Banks on the Endeavour voyage (1768–771) held in the British Museum (Natural History). Bull. Brit. Mus. (Nat. Hist.), Bot. 11: 1–183. 29. Humphries C.J. 1985. Temperate biogeography and an intemperate botanist. Taxon 34: 480–492. 30. Humphries C.J., Camus J. 1986. Contemporary issues in systematics. Cladistics 2: 85–89. 31. Humphries C.J., Nielsen E.S., Cox J. 1986. Nothofagus and its parasites. In: Stone A.R., Hawksworth D.L., editors. Coevolution. Oxford: Oxford University Press pp. 55–76. 32. Ladiges P.Y., Humphries C.J. 1986. Relationships in the stringybarks, Eucalyptus L’Herit. informal subgenus Monocalyptus series Capitellatae and Olsenianae: Phylogenetic hypotheses, biogeography and classification. Austral. J. Bot. 34: 603–631. 33. Bremer K., Humphries C.J., Churchill S., Mishler B. 1987. On cladistic relationships of green plants. Taxon 36: 339–349. 34. Bremer K., Humphries C.J., Jarvis C.E., López González G. 1987. (873) Proposal to conserve 9341 Prolongoa Boissier with a conserved type specimen (Asteraceae: Anthemideae). Taxon 36: 476–477. 35. Diment J.A., Humphries C.J., Newington L., Press J.R., Shaughnessy E. 1987. Catalogue of the natural history drawings by Joseph Banks on the Endeavour voyage (1768–1771) held in the British Museum (Natural History). Bull. Brit. Mus. (Nat. Hist.), Bot. 11: 1–200. 36. Ladiges P.Y., Humphries C.J., Brooker M.I.H. 1987. Cladistic and biogeographic analysis of Western Australian species of Eucalyptus L’Hérit., informal subgenus Monocalyptus Pryor & Johnson. Austral. J. Bot. 35: 251–281. 37. Cranston P.S., Humphries C.J. 1988. Cladistics and computers: A chironomid conundrum? Cladistics 4: 72–92. 38. Humphries C.J., Chappill J. 1988. Science in systematics: A reply to Cronquist. Bot. Rev. (Lancaster) 54: 129–144. 39. Humphries C.J., Ladiges P.Y. 1988. The application of cladistic taxonomy to plants: A reply to Wilson. Taxon 37: 388–390. 40. Humphries C.J., Ladiges P.Y., Roos M., Zandee M. 1988. Cladistic biogeography. In: Myers A., Giller A., editors. Biogeography. An analytical approach. London: Chapman and Hall pp. 371–404. 41. Mishler B.D., Bremer K., Humphries C.J., Churchill S. 1988. The use of nucleic acid sequence data in phylogenetic reconstruction. Taxon 37: 391–395.

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42. Humphries C.J. 1989. Modern data sets for flowering plants. In: Fernholm B., Bremer K., Jornvall H., editors. The hierarchy of life: Molecules and morphology in phylogenetic analysis. Amsterdam: Excerpta Medica pp. 215–226. 43. Humphries C.J. 1989. Any advance on assumption 2? J. Biogeogr. 16: 101–102, 200. 44. Humphries C.J., Blackmore S. 1989. The systematic position of Moraceae. In: Cran, P.R., Blackmore S., editors. The systematics, biology and fossil history of the Hamamelidae. Oxford: Clarendon Press pp. 267–277. 45. Humphries C.J., Seberg O. 1989. Graphs and generalised tracks: some comments on method. Syst. Zool. 38: 69–76. 46. Ladiges P.Y., Newnham M., Humphries C.J. 1989. Systematics and biogeography of the Australian “Green Ash” Eucalypts (Monocalyptus). Cladistics 5: 345–364. 47. Humphries C.J. 1990. The importance of Wallacea to biogeographical thinking. In: Knight W.J., Holloway J.D., editors. Insects and the rain forests of South-east Asia. London: Royal Entomological Society pp. 7–18. 48. Ali P.O., Simpson A.J.G., Waters A.P., Humphries C.J., Rollinson D. 1991. Sequence of a small rRNA gene of Schistosoma mansoni and its use in phylogenetic analysis. Mol. Biochem. Parasitol. 46: 201–208. 49. Humphries C.J. 1991. The implications of pragmatism for systematics. In: Hawksworth D.L., editor. Improving the stability of names: Needs and options. Regnum vegetabile 123. Königstein, Germany: Koeltz Scientific Books pp. 313–322. 50. Humphries C.J., Vane-Wright R.I., Williams P.H. 1991. Biodiversity reserves: Setting new priorities for the conservation of wildlife. Parks (IUCN) 4: 34–37. 51. Vane-Wright R.I., Humphries C.J., Williams P.H. 1991. What to protect? Systematics and the agony of choice. Biol. Conservation 55: 235–254. 52. Williams, P.H., Humphries C.J., Vane-Wright R.I. 1991. Measuring biodiversity: Taxonomic relatedness for conservationists. Austral. Syst. Bot. 4: 665–679. 53. Bremer K., Humphries C.J. 1993. A monograph of the Compositae: Anthemideae. Bull. Brit. Mus. (Nat. Hist.), Bot. 23: 73–179. 54. Cox P.A., Humphries C.J. 1993. Hydrophilous pollination and breeding system evolution in seagrasses: A phylogenetic approach to the evolutionary ecology of Cymodoceaceae. Bot. J. Linn. Soc. 113: 217–226. 55. Patterson C., Williams D.M., Humphries C.J. 1993. Congruence between molecular and morphological phylogenies. Ann. Rev. Ecol. Syst. 24: 153– 188. 56. Pressey R.L., Humphries C.J., Margules C.R., Vane-Wright R.I., Williams P.H. 1993. Beyond opportunism: Key principles for systematic reserve selection. Trends Ecol. Evol. 8: 124–128. 57. Williams P.H., Vane-Wright R.I., Humphries C.J. 1993. Measuring biodiversity for choosing conservation areas. In: LaSalle J., Gauld I.D., editors. Hymenoptera and biodiversity. Oxford: Wallingford pp. 309–328. 58. Humphries C.J., Fisher C.T. 1994. The loss of Banks’ legacy. Philos. Trans. R. Soc. Lond. B 343: 1–7.

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59. Humphries C.J., Williams P.H. 1994. Cladograms and trees in biodiversity. In: Scotland R.W., Siebert D.J., Williams D.M., editors. Models in phylogenetic reconstruction. Oxford: Oxford University Press pp. 335–352. 60. Williams P.H., Humphries C.J. 1994. Measuring taxonomic diversity for conservation evaluation. In: Forey P.L., Humphries C.J., Vane-Wright R.I., editors. Systematics and conservation evaluation. Oxford: Clarendon Press pp. 269–287. 61. Williams P.H., Humphries C.J., Gaston K.J. 1994. Centres of seed-plant diversity: The family way. Proc. R. Soc. Lond. B 256: 67–70. 62. Farris J.S., Källersjö M., Albert V.A., Allard M., Anderberg A., Bowditch B., Bult C., Carpenter J.M., Crowe T.M., De Laet J., Fitzhugh K., Frost D., Goloboff P., Humphries C.J., Jondelius U., Judd D., Karis P.O., Lipscomb D., Luckow M., Mindell D., Muona J., Nixon K., Presch W., Seberg O., Siddall M. E., Struwe L., Tehler A., Wenzel J., Wheeler Q., Wheeler W. 1995. Explanation. Cladistics 11: 211–218. 63. Gaston K.J., Williams P.H., Eggleton P.J., Humphries C.J. 1995. Large-scale patterns of diversity: Spatial variation in family richness. Proc. R. Soc. Lond. B 260: 149–154. 64. Humphries C.J., Williams P.H., Vane-Wright R.I. 1995. Measuring biodiversity value for conservation. Ann. Rev. Ecol. Syst. 26: 93–111. 65. Williams P.H., Gaston K.J., Humphries C.J. 1995. Do conservationists and molecular biologists value differences between organisms in the same way? Biodiv. Letters 2: 67–78. 66. Castro Parga I., Moreno Saiz J.C., Humphries C.J., Williams P.H. 1996. Strengthening the natural and national park system of Iberia to conserve vascular plants. Bot. J. Linn. Soc. 121: 189–206. 67. Moreno Saiz J.C., Castro Parga I., Humphries C.J., Williams P.H. 1996. Strengthening the natural and national park system of Iberia to conserve pteridophytes. In: Camus J.M., Gibby M., Johns R.J., editors. Pteridology in perspective. Richmond: Royal Botanic Gardens, Kew pp. 101–123. 68. Platnick N.I., Humphries C.J., Nelson G., Williams D.M. 1996. Is Farris optimisation perfect? Three-taxon statements and multiple branching. Cladistics 12: 243–252. 69. Williams D.M., Scotland R.W., Humphries C.J., Siebert D.J. 1996. Confusion in philosophy: A comment on Williams (1992). Synthese 108: 127–136. 70. Williams P.H., Gibbons D., Margules C. R., Rebelo A.G., Humphries C.J., Pressey R.L. 1996. Richness hotspots, rarity hotspots and complementary areas—a comparison of three area-selection methods for conserving diversity using British breeding birds. Conservation Biol. 10: 1–17. 71. Williams P.H., Humphries C.J. 1996. Comparing character diversity among biotas. In: Gaston K.J., editor. Biodiversity: A biology of numbers and difference. Oxford: Oxford University Press. pp. 54–76. 72. Williams P.H., Prance G.T., Humphries C.J., Edwards K.S. 1996. Promise and problems in applying quantitative complementarity areas for representing diversity of some Neotropical plants (families, Dichapetalaceae, Lecythidaceae, Caryocaraceae, Chrysobalanaceae and Proteaceae). Biol. J. Linn. Soc. 58: 125–157.

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73. Stork N.E., Barrett J., Chase M., Culver C., Edwards J., Eeley H., Gauld I., Gibby M., Humphries C., Jermy C., Kumari K., Kitching I., Lambshead J., Merrett N., Paterson G., Robertson-Vernhe, J., Rosen B., Sands M., Schneller, J., Scoble M., Siebert D., Stanley H., Vane-Wright R., Vogel J. 1996. Introduction to biodiversity. In: Jermy A.C., Long D., Sands M.J.S., Stork N.E., Winser S., editors. Biodiversity assessment: a guide to good practice: field manual 1. Data and specimen collection of plants, fungi and microorganisms. London: Department of Energy, Her Majesty’s Stationery Office. 74. Williams P.H., Humphries C.J., Vane-Wright R.I., Gaston K.J. 1996. Value in biodiversity, ecological services and consensus. Trends Ecol. Evol. 11: 385. 75. Williams P.H., Gaston K.J., Humphries C.J. 1997. Mapping biodiversity value world-wide: Combining higher-taxon richness from different groups. Proc. R. Soc. Lond. B 264: 141–148. 76. Williams P., Humphries C., Araújo M. 1998. Mapping Europe’s biodiversity. In: Delbaere B.C.W., editor. Facts and figures on Europe’s biodiversity 1998–1999: The state and trends in Europe’s nature and biodiversity. Tilburg, The Netherlands: European Centre for Nature Conservation pp. 12–15. 77. Williams P., Humphries, C.J. 1998. Indicators as a tool for monitoring state and trends in biological diversity. In: Delbaere B.C.W., editor. Facts and figures on Europe’s biodiversity 1998–1999: the state and trends in Europe’s nature and biodiversity. Tilburg, The Netherlands: European Centre for Nature Conservation pp. 20–21. 78. Källersjö M., Farris J.S., Chase M.W., Bremer B., Fay M.F., Humphries C.J., Petersen G., Seberg O., Bremer K. 1998. Simultaneous parsimony jackknife analysis of 2538 rbcL DNA sequences reveals support for major clades of green plants, land plants, seed plants and flowering plants. Pl. Syst. Evol. 213: 259–287. 79. Humphries C., Araújo M., Williams P., Lampinen R., Lahti T., Uotila P. 1999. Plant diversity in Europe: Atlas Florae Europaeae and WORLDMAP. Acta Bot. Fenn. 162: 11–21. 80. Humphries C.J., Huxley R. 1999. Non-vascular plants and fungi. In: Carter D., Walker A.K., editor. Care and conservation of natural history specimens. London: Natural History Museum and Butterworth Heinemann pp. 81–91. 81. Williams P.H., Humphries C.J., Araújo M., Lahti T., Lampinen R., Uotila P., Vane-Wright R.I. 1999 Important Plant Areas of Europe: Exploring the consequences of selection criteria. In: Synge H., editor. Planta Europa: Proceedings of the Second European Conference on the Conservation of Wild Plants, 9–14 June 1998, Uppsala. London: PlantLife pp. 103–109. 82. Humphries C.J. 2000. On friendship. In: Forey P.L., Gardiner B.G., Humphries C.J., editors. Colin Patterson (1933–1998): A celebration of his life. The Linnean. Special Issue No. 2: 67–74. 83. Humphries C.J. 2000. Cladogenesis. In: Levin S.A., editor. Encyclopedia of biodiversity. San Diego, CA: Academic Press pp. 693–707. 84. Humphries C.J. 2000. Vicariance biogeography. In: Levin S.A., editor. Encyclopedia of biodiversity. San Diego, CA: Academic Press pp. 767–779.

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85. Mace G.M., Balmford A., Boitani L., Cowlishaw G., Dobson A.P., Faith D.P., Gaston K.J., Humphries C.J., Lawton J.H., Margules C.R., May R.M., Nicholls A.O., Possingham H.P., Rahbek C., van Jaarsveld A.S., VaneWright R.I., Williams P.H. 2000. From hotspots towards conservation consensus. Nature 405: 393. 86. Williams P., Humphries C., Lampinen R., Hagemeijer W., Gasc J.-P., MitchellJones T. 2000. Endemism and important areas for conserving European biodiversity: Using WORLDMAP to explore atlas maps for plants and terrestrial vertebrates. Belgian J. Entomol. 2: 21–46. 87. Araújo M.B., Humphries C.J., Densham P.J., Lampinen R., Hagemeijer W.J.M., Mitchell-Jones A.J., Gasc J.-P. 2001. Would environmental diversity be a good surrogate for species diversity? Ecography 24: 103–110. 88. Humphries C.J. 2001. Homology, characters and continuous variables. In: Macleod N., Forey P., editors. Morphology, shape, and phylogenetics. London: Taylor and Francis pp. 8–26. 89. Bharatan V., Humphries C.J. 2002. Plant names in homeopathy: An annotated checklist of currently accepted names in common use. Homeopathy 91: 156–161. 90. Ebach M.C., Humphries C.J. 2002. Cladistic biogeography and the art of discovery. J. Biogeogr. 29: 427–444. 91. Araújo M.B., Densham P.J., Humphries C.J. 2003. Predicting species diversity with ED: The quest for evidence. Ecography 26: 380–383. 92. Ebach M.C., Humphries C.J. 2003. Ontology of biogeography. J. Biogeogr. 30: 959–962. 93. Ebach M.C., Humphries C.J., Williams D.M. 2003. Phylogenetic biogeography deconstructed. J. Biogeogr. 30: 1285–1296. 94. Vare H., Lampinen R., Humphries C.J., Williams P. 2003. Taxonomic diversity of vascular plants in the European alpine areas. Ecol. Stud. 167: 133–148. 95. Williams D.M., Humphries C.J. 2003. Component coding, three-item coding and consensus methods. Syst. Biol. 52: 255–259. 96. Seberg O., Humphries C.J., Knapp S., Stevenson D.W., Petersen G., Scharff N., Andersen N.M. 2003. Shortcuts in systematics? A commentary on DNAbased taxonomy. Trends Ecol. Evol. 18: 63–65. 97. Briggs J.C., Humphries C.J. 2004. Early classics. In: Lomolino M.V., Sax D.F., Brown J.H., editors. Foundations in biogeography: Classic papers with commentaries. Chicago: Chicago University Press pp. 5–13. 98. Humphries C.J. 2004. From dispersal to geographic congruence: Comments on cladistic biogeography in the twentieth century. In: Williams, D.M., Forey P.L., editors. Milestones in systematics. Boca Raton, FL: CRC Press pp. 225–260. 99. Parenti L., Humphries C.J. 2004. Historical biogeography, the natural science. Taxon 53: 899–903. 100. Humphries C.J., Ebach M.C. 2004. Biogeography on a dynamic earth. In: Lomolino M.V., Heaney L.R., editors. Frontiers of biogeography: New directions in the geography of nature. Chicago: University of Chicago Press pp. 67–86.

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101. Williams D.M., Humphries C.J. 2004. Homology and character evolution. In: Stuessy T., Hörandl E., Maye V., editors. Deep morphology: toward a renaissance of morphology in plant systematics. Königstein, Germany: Koeltz Scientific Books pp. 119–130. 102. Ebach M.C., Humphries C.J., Newman R.A., Williams D.M., Walsh S.A. 2005. Assumption 2: opaque to intuition? J. Biogeogr. 32: 781–787. 103. Humphries C.J. 2005. Cladistic biogeography. In: Encyclopedia of life sciences online. New York: Wiley Interscience http://www.els.net/ or http:// www3.interscience.wiley.com/user/accessdenied?ID=112615162&Code= 4717&Framed=FALSE&MRWImpl=redesign-2006&MRWAcronym=els &Page=http://mrw.interscience.wiley.com/emrw/9780470015902/els/ article/a0003236/current/html?hd%253DAll%252Ccj%26hd%253DAll %252Chumphries http://mrw.interscience.wiley.com emrw/9780470015902/ home/ 104. Humphries C.J. 2005. Systematics: historical overview. In: Encyclopedia of life sciences online. New York: Wiley Interscience http://www.els.net/ or http://mrw.interscience.wiley.com/emrw/9780470015902/home/ 105. Ladiges P.Y., Kellermann J., Nelson G.J., Humphries C.J., Udovic F. 2005. Historical biogeography of Australian Rhamnaceae, tribe Pomaderreae. J. Biogeogr. 32: 1909–1919. 106. Humphries C.J. 2006. Measuring diversity. In: Leadlay E. Jury S.L., editors. Taxonomy and conservation. Cambridge: Cambridge University Press pp. 141–161. 107. Sutton, D.A., Humphries C.J. 2007. Theophrastus. The father of botany. In: Huxley R., editor. The great naturalists. London: Natural History Museum and Thames and Hudson pp. 28–31. 108. Huxley R., Humphries C.J. 2007. Andrea Cesalpino. Physician, philosopher and botanist. In: Huxley R., editor. The great naturalists. London: Natural History Museum and Thames and Hudson pp. 63–65. 109. Humphries C.J., Huxley, R. 2007. Carl Linneaus. The man who bought order to nature. In: Huxley R., editor. The great naturalists. London: Natural History Museum and Thames and Hudson pp. 132–139. 110. de Carvalho M.R., Bockmann F.A., Amorim D.S., Brandão C.R.F., de Vivo M., de Figueiredo J.L., Britski H.A., de Pinna M.C.C., Menezes N.A., Marques F.P.L., Papavero N., Cancello E.M., Crisci J.V., McEachran J.D., Schelly R.C., Lundberg J.G., Gill A.C., Britz R., Wheeler Q.D., Stiassny M.L.J., Parenti L.R., Page L.M., Wheeler W.C., Faivovich J., Vari R.P., Grande L., Humphries C.J., DeSalle R., Ebach M.C., Nelson G. 2007. Taxonomic impediment or impediment to taxonomy? A commentary on systematics and the cybertaxonomic-automation paradigm. Evol. Biol. 34: 140–143. 111. Carine M.A., Humphries C.J., Guma I.R., Reyes-Betancort J.A., SantosGuerra A. 2009. Areas and algorithms: Evaluating numerical approaches for the delimitation of areas of endemism in the Canary Islands archipelago. J. Biogeogr. 36: 593–611. 112. Reyes-Betancort, J.A., Santos-Guerra, A., Guma, I.R., Humphries, C.J., Carine, M.A. 2009. Diversity, rarity and the evolution and conservation of the Canary Island endemic flora. Anales Jard. Bot. Madrid 65: 25–45.

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BOOKS 1. Humphries C.J. 1973. A taxonomic study of the genus Argyranthemum Webb ex Schultz Bip. PhD diss. University of Reading. 2. Harroy J.-P., Tassi F., Pratesi F., Humphries C.J. (editors) 1974. National parks of the world. London: Orbis. 3. Christiansen M.S. 1979. Grasses, sedges and rushes in colour. Poole: Blandford Press. [Translation of Graesser i farver, edited and adapted for the English language by C.J. Humphries and J.R. Press.]. 4. Humphries C.J., Sutton D.A., Press J.R. 1981. The Hamlyn guide to trees of Britain and Europe. London: Hamlyn. [Reprinted in 1993 and 2000; translated into four other languages: Guía de los Árboles de Europas, Bercelona: Omega, 1982; Der Kosmos-Baumführer. Über 400 europäische Bäume in Farbe, Franckh’sche Verlagshandlung Stuttgart [3 editions] W. Keller, 1982; Le Multiguide nature de tous les arbres d’Europe, Bordas, 1981; Elseviers Nieuwe Bomengids: beschrijvingen van de Europese boomsoorten: met meer dan 1000 afbeeldingen in kleuren, Amsterdam: Elsevier, 1982; see also item 25 below]. 5. Diment J.A., Humphries C.J. (editors) 1981. Banks’ Florilegium. Parts I–IV (90 plates) London: Editions Alecto and British Museum (Natural History). 6. Diment J.A., Humphries C.J. (editors) 1982. Banks’ Florilegium. Parts V–VIII (90 plates). London: Editions Alecto and British Museum (Natural History). 7. Diment J.A., Humphries C.J. (editors) 1983. Banks’ Florilegium. Parts IX– XIV (135 plates). London: Editions Alecto and British Museum (Natural History). 8. Diment J.A., Humphries C.J. (editors) 1983. Banks’ Florilegium. Parts XV– XVIII (135 plates). London: Editions Alecto and British Museum (Natural History). 9. Diment J.A., Humphries C.J. (editors) 1984. Banks’ Florilegium. Parts XIX– XXII (135 plates). London: Editions Alecto and British Museum (Natural History). 10. Diment J.A., Humphries C.J. (editors) 1986. Banks’ Florilegium. Parts XXIII–XXVI (135 plates). London: Editions Alecto and British Museum (Natural History). 11. Humphries C.J., Parenti L. 1986. Cladistic biogeography. Oxford: Clarendon Press [Second printing with corrections, 1987.] 12. Diment J.A., Humphries C.J. (editors) 1987. Banks’ Florilegium. Parts XXVII–XXVIII (45 plates). London: Editions Alecto and British Museum (Natural History). 13. Humphries C.J. (editor) 1988. Ontogeny and systematics. New York: Columbia University Press. 14. Humphries C.J., Diment J.A., Shaughnessy E. (editors) 1990. Catalogue of Banks’ Florilegium. London: The Folio Edition Alecto Historical Editions and The British Museum (Natural History). 15. Ladiges P.Y., Humphries C.J., Martinelli L. 1991. Austral biogeography. [Reprinted from Austral. Syst. Bot. 4(1)] East Melbourne: CSIRO Australia.

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16. Forey P.L., Humphries C.J., Kitching I.J., Scotland R.W., Siebert D.J., Williams D.M. 1992. Cladistics: A practical course in systematics. Oxford: Clarendon Press. 17. Davidse G., Sousa-S. M., Chater A. (editors) Chiang F., Knapp S., Humphries C.J., Sutton D., Huft M.J. (associate editors) 1994. Flora Mesoamericana. Volumen 6, Alismataceae a Cyperaceae. Mexico City: Universidad Nacional Autónoma de México. 18. Forey P.L., Humphries C.J., Vane-Wright R.I. (editors) 1994. Systematics and conservation evaluation. Oxford: Clarendon Press. 19. Rudall P., Cutler D., Cribb P.J., Humphries C.J. (editors) 1995. Systematics and evolution of monocotyledons. Richmond: Royal Botanic Gardens, Kew. 20. Kitching I.J., Forey P.L., Humphries C.J., Williams D.M. 1998. Cladistics: the theory and practice of parsimony analysis. Oxford: Clarendon Press. 21. Humphries C.J., Parenti L. 1999. Cladistic biogeography: Interpreting patterns of plant and animal distributions. 2nd ed. Oxford: Clarendon Press. [Translated into Chinese 2004]. 22. Forey P.L., Gardiner B.G, Humphries C.J. (editors) 2000. Colin Patterson (1933–1998): A celebration of his life. The Linnean, Special Issue No. 2. The Linnean Society of London. 23. Bharatan V., Humphries C.J., Barnett J.R. 2002. Plant names in homeopathy: An annotated checklist of currently accepted names in common use. London: The Natural History Museum. 24. Hamilton J., Humphries C.J. 2005. Native trees and shrubs for your garden. London: Frances Lincoln. 25. Humphries C.J., Sutton D.A., Press J.R. 2006. The Philips guide to trees. New ed. London: Philips. 26. Humphries C.J., Curry G. 2007. Biodiversity databases: Techniques, politics, and applications. Boca Raton, FL: CRC Press.

REVIEWS, OBITUARIES, NOTICES, CORRESPONDENCE, AND SO FORTH 1. Humphries C.J. 1974. An account of the genus Argyranthemum. In: Bramwell D., Bramwell Z., editors. Wild flowers of the Canary Islands. London: Stanley Thornes Ltd. pp. 210–214. 2. Humphries C.J., Jury S.L., Richardson I.B.K. 1975. Botanical expedition to Morocco 1974. Reading: University of Reading. 3. Humphries C. J. 1977. [Review of] Nucleic acids and protein synthesis in plants. L. Bogorod and J.H. Weil (eds). Plenum 1977. New Scientist 75(1063): 306. 4. Humphries C.J. 1977. [Review of] Strasburger’s textbook of Botany. New English Edition. Translated by Pp. Bell and D. Coombe from Lehrbuch der Botanik by D. von Deufter et al. J. Nat. Hist. 11: 118–120. 5. Humphries C.J. 1977. [Review of] Plant taxonomy. 2nd ed. V.H. Heywood. J. Nat. Hist. 11:358–359.

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6. Tosco U. 1978. Mountain flowers [First published in English as The world of mountain flowers, 1974, adapted from a text of Uberto Tosco, with a foreword by Christopher Humphries]. London: Orbis. 7. Humphries C.J., Jermy A.C. 1978. [Review of] British water plants. S. Haslam, C. Sinker and P. Wolseley. Field Studies Council. Watsonia 11: 264–265. 8. Humphries C.J. 1978. [Review of] Biogeography and ecology in the Canary Islands. G. Kunkel (ed.). W. Junk. Watsonia 11: 410–411. 9. Humphries C.J. 1978. [Review of] The power of plants. Brendan Lehane. John Murray, London. J. Nat. Hist. 12: 596–597. 10. Humphries C.J. 1978. [Review of] Pollination mechanisms, reproduction and plant breeding. R. Frankel and E. Gahin. Springer Verlag. J. Nat. Hist. 12: 597–598. 11. Humphries C.J. 1978. [Review of] Die Bedeutung der Polyploidie fur die Evolution der Pflanzen. W. Gottschalk. Gustav Fischer Verlage. J. Nat. Hist. 12: 717–718. 12. Humphries C.J. 1978. [Review of] Plant communities. Anne Bulow-Olsen. Penguin Books. 1978. J. Nat. Hist. 12: 718. 13. Humphries C.J. 1978. [Review of] A flora of the Maltese Islands. S.M. Haslam, P.D. Sell and P.A. Wolseley. 1977. Watsonia 12: 55–56. 14. Humphries C.J. 1978. Bombacaceae, Chenopodiaceae, Casuarinaceae, Erythroxolaceae, Rutaceae, Sarraceniaceae, Zingiberaceae. In: Heywood V. H., editor. Flowering plants of the world. Oxford: Oxford University Press. pp. 93–94, 72–73, 54–55, 62–63, 72–73, 93–94, 202–204, 210, 297–298. 15. Humphries C.J. 1979. [Review of] Flore du Sahara (2nd ed). P. Ozenda. CNRS, Paris. Watsonia 12:181–182. 16. Humphries C.J. 1979. [Review of] The biology and chemistry of the Compositae. V.H. Heywood, J. B. Harborne and B. L. Turner (eds). Academic Press, London and New York. Watsonia 12: 264–265. 17. Humphries C.J. 1980. [Review of] Advances in botanical research, volume 6. H.W. Woolhouse (ed.). Academic Press, London and New York. Watsonia 13: 65. 18. Humphries C.J. 1980. [Review of] Trees and shrubs of the Mediterranean. Helge Vedd. Penguin Books. 1978. J. Nat. Hist. 14: 147–148. 19. Humphries C.J. 1981. [Review of] Plant taxonomy and biosystematics. C.A. Stace. Edward Arnold, London. 1981. J. Nat. Hist. 15: 1062–1065. 20. Humphries C.J. 1981. [Review of] Historical plant geography: an introduction, Stott. George Allen and Unwin. 1980. J. Nat. Hist. 15: 1076–1078. 21. Humphries C.J. 1981. Hornbeams (Carpinus). In: Hora F.B., editor. The Oxford Encyclopedia of trees of the world. Oxford: Oxford University Press. pp. 141–143. 22. Ball H.W. Gray A., Mound L.A., Cannon J.F.M., Humphries C.J., Platt H.M., Clarke G.C.S., James P.W., Price J.H., Eastwood R.F., Jermy A.C., Robson N.K.B, Forey P.L., John D.M., Stringer C.B., George J.D., Jones S.W., Sutton D.A., Gibby M., Miles R.S. Vane-Wright R.I., Whitehead P.J.P. 1981. Darwin’s survival. Nature 290: 82. 23. Humphries C.J. 1982. [Review of] Systematics and biogeography: cladistics and vicariance. G. Nelson and N.I. Platnick. Columbia University Press, New York. J. Nat. Hist. 16: 296–299.

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24. Humphries C.J. 1982. [Review of] Biochemical evolution. H. Gutfreund. Cambridge University Press. 1981. Watsonia 14: 87–88. 25. Humphries C.J. 1982. [Review of] Phylogenetics: the theory and practice of phylogenetic systematics. E. O. Wiley. Wiley Interscience. 1981. Watsonia 14: 209–210. 26. Diment J.A., Humphries C.J. 1982. Banks’ Florilegium. Newsletter Austral. Syst. Bot. Soc. 31: 24–25. 27. Humphries C.J. 1982. Adaptation; isolation; dispersal; and migration. In: Moore, D., editor. Green planet. Cambridge: Cambridge University Press pp. 96–102, 108–111, 142–145. 28. Davidse G., Sousa M., Chater A.O., Humphries C.J. 1982. Flora Mesoamericana: Guia para autores/Guide for authors. London: British Museum (Natural History). 29. Humphries C.J. 1983. [Review of] Darwinism defended: a guide to the evolution controversies. M. Ruse. Addison-Wesley. 1982. Oryx 17: 48. 30. Humphries C.J. 1983. [Review of] Plant extinction: a global crisis. H. Koopowitz and H. Kaye. Stone Wall Press. 1983. Oryx 17: 145. 31. Humphries C.J. 1983. [Review of] Problems of phylogenetic reconstruction (Systematics Association, Special volume 21). Joysey, K. A. and Friday, A. E. (eds) and Methods of phylogenetic reconstruction. Patterson, C. (ed.) Zoological Journal of the Linnean Society 74: 197–334. Syst. Zool. 32: 301–310. 32. Humphries C.J. 1984. [Review of] How flowers work: a guide to plant biology. B. Gibbons. Blandford Press, Poole, Dorset. Times Literary Supplement, September 7. 33. Humphries C.J. 1984. [Review of] Biogeography. J.H. Brown and A.C. Gibson. C.V. Mosby and Co. J. Biogeogr. 11: 363–365. 34. Humphries C.J. 1984. [Review of] Flora of Australia, volumes 1 and 8. AGPS, Canberra. Kew Bull. 39: 661–663. 35. Humphries C.J. 1984. [Review of] Extinct and endangered plants of Australia. J. Leigh, R. Boden and J. Briggs. Macmillan, Australia. Oryx 19: 52. 36. Humphries C.J. 1985. [Review of] Croizat’s Panbiogeography and Principia Botanica: Search for the novel biological synthesis. Tuatara 27. J. Nat. Hist. 19: 1285–1286. 37. Humphries C.J. 1985. A crop of Academic Botany. A review of 4 titles from Academic Press. Plant biosystematics. W. F. Grant; Data bases in systematics. R. Allkin and F. Bisby (eds). Current concepts in plant taxonomy. V. H. Heywood and D. M. Moore (eds). Plant chemosystematics. J.B. Harborne and B. L.Turner. New Scientist 1452 (18 April 1985): 44. 38. Sutton S., Humphries C.J., Hopkinson J. 1985. Tarragon. Garden 110: 237–240. 39. Humphries C.J. 1986. [Review of] Royal Kew. R. King. Constable, London. 1985. New Scientist 1495 (February 13, 1986): 49. 40. Humphries C.J. 1986. [Review of] The problems of evolution. M. Ridley. Oxford University Press. 1985. Arch. Nat. Hist. 13: 87–89. 41. Humphries C.J. 1986. [Review of] The evolutionary process: A critical review of evolutionary theory. V. Grant. Columbia University Press. 1985. Paleontological Newsletter [no page numbers].

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42. Humphries C.J. 1987. [Review of] The enchanted canopy: Secrets from the rainforest roof. A. W. Mitchell. William Collins and Sons Ltd. 1986. Oryx 21: 128. 43. Humphries C.J. 1987. [Review of] The botany of mangroves. P. B. Tomlinson. Cambridge University Press 1986. Oryx 21: 197. 44. Humphries C.J. 1987. [Review of] The synergism hypothesis, P. A. Corning. Blond and Briggs. 1984. Arch. Nat. Hist. 14: 228–230. 45. Humphries C.J. 1988. [Review of] Plants in danger: What do we know? S. D. Davis, S. J. M. Droop, Gregerson, L. Henson, C. J. Leon, J. Lamlein-Villa Lobos, H. Synge & J. Zantovska. IUCN, Gland and Cambridge. Watsonia 17: 106. 46. Humphries C.J. 1988. [Review of] Dimensions of Darwinism: Themes and counterthemes in twentieth-century evolutionary biology. Marjorie Grene (ed.) Cambridge University Press/Editions de la Maison des Sciences de l’Homme. Arch. Nat. Hist. 15: 108–114. 47. Humphries C.J. 1988. [Review of] Biological metaphor and cladistic classification: an interdisciplinary approach. H.M. Hoenigswald and L.F. Wiener (eds). Frances Pinter (Publishers). London. Cladistics 4: 304–308. 48. Humphries C.J. 1988. Patterns before process. Nature 333: 300–301. 49. Humphries C.J. 1989. [Review of] Molecules and morphology in evolution: conflict or compromise? C. Patterson (ed.). Cambridge University Press. Watsonia 17: 372. 50. Humphries C.J. 1989. [Review of] The ages of Gaia. J. Lovelock. Oxford University Press. J. Nat. Hist. 23: 972–973. 51. Humphries C.J. 1989. Was there biogeography before the Quaternary? [Review of] T. C. Whitmore & G. T. Prance (eds.), 1987. Biogeography and Quaternary history of tropical America. Clarendon Press, Oxford. J. Biogeogr. 16: 97–100. 52. Patterson C., Jefferies R.P.S., Sattler K., Wheatcroft P., Clutton-Brock J., Humphries C.J., Hill C.R., Greenwood P.H. 1990. Vote of no confidence (correspondence). Nature 347: 419. 53. Siebert D.J., Humphries C.J. 1991. Comparatively speaking [Review of] Phylogeny, ecology and behavior: a research program in Comparative Biology. Daniel R. Brooks & Deborah A. McLennan. University of Chicago Press and The comparative method in evolutionary biology. Paul Harvey & Mark Pagel. Oxford University Press 1991. Nature 353: 615–616. 54. Humphries C.J. 1991. [Review of] Shamrock. Botany and history of an Irish myth. Charles Nelson. Boethius Press. Linnean 8: 62. 55. Humphries C.J. 1991. [Review of] Aphrodite’s mousetrap: A biography of Venus’s flytrap with facsimiles of an original pamphlet and the manuscripts of John Ellis F.R.S. Charles Nelson. Boethius Press. The Linnean 8: 63. 56. Humphries C.J., Vane-Wright R.I. 1992. Systematic evaluation of the global network of protected areas: Objectives, alternatives, prospects and proposals. Abstract and draft papers presented at IVth World Congress on National Parks and Protected Areas, Caracas, February 1992. [See also McNeely J.A. (editor) 1993. Parks for life, Gland (Switzerland): IUCN pp. 152]. 57. Humphries C.J. 1993. The art of Endeavour. Kew Mag. (Spring): 1–6.

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58. Garwood N.C., Humphries C.J. 1993. Seedling diversity in the Neotropics. NERC News July 1993: 20–23. 59. Humphries C.J. 1994. [Review of] Intermontane Flora. Volume 5. Arthur Cronquist et al. New York Botanical Garden. Bot. J. Linn. Soc. 118: 78. 60. Humphries C.J. 1994. Systematics, biogeography and conservation. Jahrbuch 1993/94, Wissenschaftskolleg, Berlin [herausgegeben von Wolf Lepenies mit berichten und beiträgen von András Bazóki . . . et al.]. Berlin: Wissenshaftskolleg zu Berlin pp. 76–79. 61. Humphries C.J., Vane-Wright R.I. 1994. Priority areas analysis: systematic methods for the conservation of biodiversity/Biodiversity Group colloquium, April 26–27, 1994. Jahrbuch 1993/94, Wissenschaftskolleg, Berlin [herausgegeben von Wolf Lepenies mit berichten und beiträgen von András Bazóki . . . et al.]. Berlin: Wissenshaftskolleg zu Berlin pp. 193–197. 62. Humphries C.J., Vane-Wright R.I., Williams P.H., Kitching, Smith C. 1994. Biology, economics and politics in biodiversity conservation. Biodiversity Group colloquium, 7–8 June 1994. Jahrbuch 1993/94, Wissenschaftskolleg, Berlin [herausgegeben von Wolf Lepenies mit berichten und beiträgen von András Bazóki . . . et al.]. Berlin: Wissenshaftskolleg zu Berlin pp. 198–201. 63. Pressy R.L., Humphries C.J., Vane-Wright R.I., Williams P.H. 1994. Beyond opportunism: Key principles for systematic reserve selection. Jahrbuch 1993/94, Wissenschaftskolleg, Berlin [herausgegeben von Wolf Lepenies mit berichten und beiträgen von András Bazóki . . . et al.]. Berlin: Wissenshaftskolleg zu Berlin pp. 212–226. 64. Humphries C.J. 1995. [Review of] Insect conservation biology. Michael Samways. Chapman and Hall. 1994. J. Nat. Hist. 29: 839–840. 65. Humphries C.J. 1996. Reviews. Biodiversity and Phylogeny: XIII International Meeting of the Willi Hennig Society. Zoological Museum, University of Copenhagen, 23–26 August 1994. Cladistics 11: 385–398. 66. Humphries C.J. 1996. [Review of] Centres of plant diversity. A guide and strategy for their conservation. WWF and IUCN. New Phytol. 135: 567–574. 67. Williams P.H., Gaston K.G., Humphries C.J., Vane-Wright R.I. 1997. Reply to Faith on “Biodiversity, biospecifics, and ecological services” (Correspondence) Trends Ecol. Evol. 12: 66–67. 68. Williams P.H., Humphries C.J., Vane-Wright R.I., Gaston K.G. 1997. Descriptive and predictive approaches to biodiversity measurement. (Correspondence). Trends Ecol. Evol. 12: 444–445. 69. Humphries C.J. 1997. [Review of] Biometry (ed 3), by R.R. Sokal and F.J. Rohlf. W. H. Freeman & Co. Ltd, Oxford. Biol. J. Linn. Soc. 61: 299–300. 70. Humphries C.J. 1997. [Review of] The ecology and biogeography of Nothofagus forests. Thomas T. Veblen, Robert S, Hill and Jennifer Read. Yale University Press. New Haven, 1996. Biodiversity Conserv. 6: 1458–1459. 71. Humphries C.J., Seberg O. 1999. [Review of] The biological monograph: the importance of field studies and functional syndromes for taxonomy and evolution of tropical plants. H.C.F. Hopkins . . . [et al.]. Royal Botanic Gardens Kew, London. 1998. Bot. J. Linn. Soc. 131: 99. 72. Humphries C.J. 2000. Floras on CD Rom. Plant Talk 20: 41.

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73. Humphries C.J. 2001. Hotspots going off the boil? Book Review of Mittermeier, R.A., Myers, N. & Mittermeier, C.G. 2000. Hotspots: earth’s biologically richest and most endangered terrestrial ecoregions. Distributed for CEMEX/Conservation International by the University of Chicago Press, Chicago. Diversity Distrib. 7: 104–105. 74. Humphries C.J. 2001. Chalk and cheese. CD Review of Flora Europaea on CD-ROM, 2000 Cambridge University Press, and Orchids of New Guinea Vol. 1 by A. Schuiteman and E. F. Vogel, 2001, World Database CD-ROM Series published by ETI. Plant Talk 26: 38–39. 75. Humphries C.J. 2002. [Review of] Paleobiogeography: using fossils to study global change, plate tectonics, and evolution. Bruce S. Lieberman. 2000. J. Palaeontol. 76: 1110–1112. 76. Humphries C.J. 2002. William T. Stearn: the Museum Years (1952–1976). Linnean 18: 36–41. 77. Humphries C.J. 2002. Appendix II. In: Blunt, W. Linnaeus: the compleat naturalist. Princeton University Press. 78. Humphries, C.J. 2002. Axis: Conservation just got tougher. Kew (Winter): 56. 79. Knapp, S., R.M. Bateman, N.R. Chalmers, C.J. Humphries, P.S. Rainbow, A.B. Smith, P.D. Taylor, R.I. Vane-Wright and M. Wilkinson. 2002. Taxonomy needs evolution, not revolution. Nature 419:559. 80. Humphries C.J. 2003. [Review of] Captivating life: a naturalist in the age of genetics. John C. Avise, Smithsonian Institution Press. Biol. Conservation 111: 275–276. 81. Ebach M.C., Humphries C.J. 2003. Comments in response to Professor Dobson’s letter. J. Biogeogr. 30: 473. 82. Humphries C.J. 2009. [Letter to Linneaus]. In: Knapp S., Wheeler, Q., editors. Letters to Linneaus. The Linnean Society of London, London.

POPULAR WORKS 1. Humphries C.J. 1978. Spotter’s guide to wild flowers. London: Usborne. 2. Humphries C.J. 1981. In memoriam: stately elms. Living Countryside 3(34): 672–674. 3. Humphries C.J. 1981. Smooth and hybrid elms. Living Countryside 3(37): 732–733. 4. Humphries C.J. 1982. [Approx. 5000 botanical entries]. In: Procter, P., editor. Longman New Universal Dictionary. Harlow, Essex: Longman. 5. Humphries C.J. 1982. Elm bark beetles. Living Countryside 5(53): 1044– 1046. 6. Humphries C.J. 1982. A look at tree classification. Living Countryside 7(79): 1569–1571. 7. Humphries C.J. 1982. Timber and its products. Living Countryside 8(91): 1801–1803. 8. Humphries C.J. 1983. Flowers: what’s in a name? Living Countryside 9(97): 1932–1933.

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9. Humphries C.J. 1983. Eucalypts in Britain. Living Countryside 13(146): 2906–2907. 10. Humphries C.J. 1983. Hybrids: nature’s mongrels. Living Countryside 13(148): 2944–2946. 11. Humphries C.J., Shaughnessy E. 1984. Evergreen pittosporums. Living Countryside 13(155): 3094–3095. 12. Humphries C.J., Shaughnessy E. 1987. Gorse. No. 9. Princes Risborough, Buckinghamshire: Shire Natural History Series.

WEB SITES 1. Williams, P., Humphries, C.J., Vane-Wright, R.I. 1996–et seq. Biodiversity: Measuring the variety of nature and selecting priority areas for conservation. (http://www.nhm.ac.uk/science/projects/worldmap/index.html) 2. Sadka, M., Cassey, D., Humphries, C.J. 1999–2001. Exploring Biodiversity: An interactive introduction to biodiversity concepts and measures. (http:// flood.nhm.ac.uk/eb//index.shtml) 3. Rees, R., Sadka, M., Humphries, C.J., Williams, P., Gee, D. 1997–et seq. Postcodes Plants Database. (http://www.nhm.ac.uk/science/projects/fff/index. htm) 4. Seberg, O., Humphries, C.J., Petersen, G. 2002. What is cladistics? (http:// www.nhbs.com/features/cladistics.html) 5. Yuou-ruen, L., Humphries, C.J., Shultz, L. 2009. Asteraceae, Tribe Anthemideae Cassini, Bull. Soc. Philom. Paris 173. 1815. [Draft], Artemisia, Linnaeus, Sp. Pl. 2: 845. 1753 (http://hua.huh.harvard.edu/china/mss/volume20/AsteraceaeK-Anthemideae-part1_coauthoring.htm)

ONE

D a v i d M . W i l l i a m s , K å r e B r e m e r, a n d S a n d r a K n a p p

CHRIS HUMPHRIES, CLADISTICS, AND CONNECTIONS

INTRODUCTION

By way of introduction, we offer this short piece describing a few subjects that attracted Chris Humphries’s attention during his thirty-plus years as botanist and systematist. While it is impossible to cover all the subjects with which Chris was involved, we have selected a few that seem representative of his breadth: botanical cladistics, cladistics and daisies, and biogeographic cladistics (the conservation studies are ably summarized by Vane-Wright; see Chapter 3, this volume).

A SHORT BIOGRAPHY

Chris joined the Department of Botany of the Natural History Museum in 1972 replacing Alexsandr Melderis (1909–1986), then head of the European Herbarium, “whose substantial frame belied his most kindly and benign personality” (Cannon 2001: 128). Chris was hired as assistant curator, a nearly finished PhD student, coming directly from Vernon Heywood’s Department of Botany in Reading University. Flora Europaea (FE) was being brought to a conclusion, and Chris was to help put Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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the project to bed (for a summary of FE achievements, see Walters 1995). But his first task was to finish his thesis and obtain his PhD degree, which he did in 1973. His study was on species of Argyranthemum, a genus of daisy in the family Asteraceae, and is a fine example of a morphological investigation (with a little phytochemistry) and anatomical interpretation, with comments on their relationships and geographic distribution. Most of the morphological part was published as a monograph in the museum’s now-defunct Bulletin series, covering “22 species, grouped into five sections . . . all of which occur in the North Atlantic insular archipelagos of Madeira, the Salvage Islands and the Canary Islands” (Humphries 1976: 147, abstract). Chris would return to the subject of Madeira and the geographic relations of its plants (Carine et al. 2009). Chris—one of the first of Vernon Heywood’s students (David Bramwell [see Chapter 6, this volume] was another)—by moving to the museum began the invasion of what became known as the “Reading Mafia.” Others followed and are represented within the pages of this book: Stephen Blackmore (see Chapter 2) and Charlie Jarvis (see Chapter 8) (see also Leadlay and Jury 2006). With the exception of three sabbaticals— two of them at the University of Melbourne, the first in 1979–1980 and the second in 1986, and a six-month stay at the Wissenschaftskolleg zu Berlin (Institute for Advanced Study Berlin) in 1994—Chris worked in the Department of Botany at the museum. Chris’s studies on Asteraceae to one side (see later), the next period in his career focused almost exclusively on biogeography, and in 1979 he published his first considered paper on the subject, “Endemism and Evolution in Macaronesia” (Humphries 1979a). Between times he published a number of revisions and smaller accounts of other flowering plant families such as Poaceae, but of greater significance were his papers on the southern beeches (Nothofagus) and their relevance to Southern Hemisphere biogeography (Humphries 1981a, 1981b, 1983); a series of papers on Eucalyptus and their geographic dimension (Ladiges and Humphries 1983, 1986; Ladiges et al. 1983, 1987, 1989; see also Ladiges et al., Chapter 14, this volume); an intellectual justification for documenting the Central American flora (Humphries 1983), which blossomed into Flora Mesoamericana (Knapp and Press, Chapter 5, this volume); some early angiosperm molecular papers (Mishler et al. 1988; Humphries 1989); and a textbook summary of cladistic biogeography (Humphries and Parenti 1986, 1999; see also Parenti and Humphries 2004; Parenti and Ebach, Chapter 15, this volume). Most of these topics find biogeography as the unifying theme.

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Around 1990, Chris, Dick Vane-Wright, and Paul Williams put biogeographic matters to a more practical application, addressing what they called the conservationist’s “Agony of Choice” (Vane-Wright et al. 1991) with their “WORLDMAP” approach to conservation biology. As Dick Vane-Wright relates in his chapter in this book (Chapter 3), Chris’s interest in conservation biology goes back to his early days, publishing on the subject with respect to Argyranthemum in 1974 (Humphries 1974). Remarkably, this was only his third publication, his first as a sole author. When asked how he came to write such a paper so early in his career, Chris offered the following: “[T]he paper you asked about was because as a reviewer I didn’t like the original entry—so I rewrote it for them” (C.J. Humphries, pers. comm., March 9, 2009). Chris explored the scientific and policy aspects of biological conservation for nearly a decade until, encouraged by the enthusiasm of Malte Ebach (see Chapters 10 and 15, this volume), he returned to the more fundamental matters of biogeographic investigation (e.g., Ebach and Humphries 2002; Humphries and Ebach 2004; see also the bibliography in this book). Chris received a number of honors: He was awarded the Linnean Society’s Bicentenary Medal in 1980 (Biological Journal of the Linnean Society 2001;14: 456–457); twenty-one years later, in 2001, he received the Linnean Society’s most prestigious award, its Gold Medal (Linnean Society Annual Report 2001: 36–37, with photograph); and in 2002 he became an honorary fellow of the American Association for the Advancement of Science. He has been president of the Systematics Association (2001–2003) and its treasurer (1996–1999), president of the Willi Hennig Society (1989–1991), being elected fellow honoris causa in 1998, and vice president and botanical secretary of the Linnean Society (1994–1998).

BOTANICAL CLADISTICS

Reading Chris’s doctoral thesis today, thirty-six years after it was printed, one gets little direct sense of the future, what was to come, except for the odd sentence here and there, such as this one: The most fruitful systematic evidence for speculation on evolutionary sequence in Argyranthemum stems from the relationship between distribution and eco-geographical specialization. (Humphries 1973, p. 217)

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There were no cladograms, no schemes of relationships, but there was geography—and discussions of its relevance and interpretation, in the sense that “evolutionary sequence[s] . . . stem[s] from the relationship between distribution and eco-geographical specialisation.” Here we take a short digression to consider the beginnings of botanical cladistics, a subject difficult to pin down, largely because cladistics, even in its botanical guise, was—and probably still is—interpreted in a myriad of different ways. For botany, it is generally acknowledged that Warren “Herb” Wagner (1920–2000; see Farrar 2003) and his ground plan divergence method spawned many early contributions to a “cladistic” approach from the mid-1950s through to the late 1960s (see the bibliography published by Funk and Wagner 1982). Wagner’s ground plan divergence method was developed as part of his thesis work on ferns (Wagner 1952; see also Wagner 1980), which was derived from Benedictus Danser (1891–1943; Jansen and Wachter 1943) and his notion of ground plans and their relevance rather than from the works of Willi Hennig (Danser 1950; see also Wagner 1969; for a recent incarnation, see Kukalová-Peck 2008; for commentary, see Béthoux et al. 2008). Wagner’s name did eventually become inextricably linked to one of the earliest and most commonly used parsimony algorithms (Farris 1970), an approach that was later associated with some of Willi Hennig’s ideas (Farris et al. 1970). A more direct connection to Willi Hennig can be found in the work of bryologist Timo Koponen and his study on Mniaceae, which included possibly the first botanical Hennigian argumentation plan (Koponen 1968: 136, Fig. 107). With respect to British botanical cladistics, the first argumentation plan (and probably the first paper in Taxon to use Hennig’s ideas—a few earlier papers mention Hennig but only in passing) was published by Chris in a multiauthored piece entitled “Chromosome banding and synthetic systematics in Anacyclus” (Ehrendorfer et al. 1977: 390, Fig. 4). Much was captured by that title. Chromosome banding and related matters might have sounded like the future in the 1970s, but Chris was to home in on “synthetic systematics”—it was a subtle beginning. We mentioned briefly above Chris’s first biogeography paper, “Endemism and Evolution in Macaronesia” (Humphries 1979a). Although betraying a sense of its time with subheadings such as “Gradual Speciation,” “Morphology and Adaptive Radiation,” and “Abrupt Speciation: Apoendemism,” the discussion treads cautiously

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over new ground, without mentioning Hennig, but using Hennigian terminology: The retention of plesiomorphic features, i.e. ancestral morphological attributes and the same chromosome numbers as sisters groups, together with the fact that many are taxonomically isolated are rather dubious lines of evidence on which to estimate the age of species . . . the fact that many [taxa] possess synapomorphic features (uniquely derived attributes) shared by sister groups is indicative of a monophyletic origin from a single island ancestor. (Humphries 1979a: 194)

Such coded and oblique references may have been difficult for many to comprehend, even if plesiomorphic features and synapomorphic features were both defined (“ancestral morphological attributes” and “uniquely derived attributes,” respectively). Matters were different when Chris published his Anacyclus monograph (Humphries 1979b). By that time, Bremer and Wanntorp had published their summary and review of Hennig’s phylogenetic systematics, boldly stating that they “deplore that phylogenetic systematics has not been introduced into botany and we considered it high time that botanists in general should become aware of this taxonomic approach” (Bremer and Wanntorp 1978: 317–318). Responses to this call were quick and often negative, bordering on the hostile (Burger 1979; F[aegri], 1979; Guédès 1981; Meeuse 1981; further comment and clarification came from Wanntorp 1980, 1983). Such was the climate that Chris could provide a three-page summary of phylogenetic systematics, adding, with some poignancy “. . . the construction of ‘phylogenetic trees’ based on ill-defined principles and the elaboration of nominalistic methods has created considerable disillusionment and disregard of sound phylogenetic discussion” (Humphries 1979b: 102). The relationships among the species of Anacyclus were portrayed in a Hennigian argumentation plan, characters determined by the assessment of relative apomorphy rather than by any computer-aided assistance (Humphries 1979b: 107, Fig. 10). Humphries and Richardson (1980) provided a further overview of phylogenetic systematics in botany in the context of phytochemistry, and, later, Humphries and Funk (1984) wrote a more general piece. Things were not easy: “The adoption of cladistic methodology did not happen without a degree of dogged persistence: Chris Humphries’ paper with Vicki Funk . . . at a subsequent international symposium also held at Reading, Current Concepts in Plant Taxonomy, received a hostile reception from members of the audience” (Blackmore and Wortley, Chapter 2, this volume). Thus, promotion of

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botanical cladistics, in its Hennigian form, truly began with Chris, HansErik Wanntorp, and Kåre Bremer, and that beginning, like the reform of paleontology (Patterson 1981b), may be traced back to the enthusiasms of Lars Brundin (Wanntorp 1993; Brundin 1993, 1995). At a more fundamental level, the more direct impact of phylogenetic systematics on green plant classification was ignited and stimulated by two papers, “A Phylogenetic Analysis of the Land Plants” by Lynne Parenti, an ichthyologist from the American Museum of Natural History (Parenti 1980; a response came from Smoot et al. 1981, with replies from Parenti 1981; Young and Richardson 1982), and “A Cladistic Classification of Green Plants” by Bremer and Wanntorp (Bremer and Wanntorp 1981a, 1981b), along with further commentary from zoologists (Farris and Kluge 1979; Wiley 1980; Mitter 1981). Both the empirical papers (Parenti 1980; Bremer and Wanntorp 1981a, 1981b) inspired further research into green plant relationships. In July 1984, Chris organized a symposium, held at the Natural History Museum, sponsored by the Linnean Society, the Systematics Association, and the Willi Hennig Society. This resulted in a series of papers published in the first volume of the journal Cladistics, a new journal to a large extent established thanks to the efforts of Chris; he was also one of the two first editors. By 1982, Funk and Wagner published a “botanical cladistics” bibliography with 123 items (Funk and Wagner 1982), and, two years later, Baum et al. published a bibliography of “numerical phenetic studies” numbering some 426 items (Baum et al. 1984). These two compilations are of general interest, as the Funk and Wagner bibliography included numerical studies generated by various computer programs alongside noncomputer Hennigian analyses. Thus, one might have imagined at the time it would have been difficult to determine just exactly what cladistics (“phylogenetic systematics”) was—or at least how it was done. If one was to examine the various methodology papers published in Taxon from its beginning (1951) through to the 1970s, most were exploring the various strands of numerical taxonomy, in its broadest interpretation, as understood in Sneath and Sokal (1973) and in Sneath (1995). It might be just to consider that “phylogenetic systematics” (sensu Willi Hennig) progressed almost as if invisible to the desires of numerical taxonomy. That changed, of course, after the debate in Taxon between proponents of parsimony and compatibility (a debate starting with Churchill et al. 1984). That debate is too complex to deal with here, save to note of the combatants early in the botanical discussion, Farris and Kluge suggested that “All authors evidently deemed it desirable to be termed

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‘Hennigian’. . .” (Farris and Kluge 1979: 411). It is important to note that, at least in terms of popularity of use, if not soundness of justification, parsimony triumphed for a while (Farris and Kluge 1986). Part of that triumph was assisted by the Forey et al. (1992) book, another publication eased into existence by Chris, the Systematics Association, and the Natural History Museum (a short history can be found in Williams and Ebach 2009).

CLADISTICS AND DAISIES

In 1975 (July 14–18), Vernon Heywood, Jeffrey Harborne, and Billie Turner arranged a symposium on the biology and chemistry of the Compositae (= Asteraceae), held at the University of Reading (Heywood et al. 1977; reviewed by Humphries 1979c). There was no mention of phylogenetic systematics, even though both Chris and Kåre Bremer were present and both aware of the subject. Both were working on genera in the tribe Anthemideae. Bremer was studying the South African genus Osmitopsis (Bremer 1972), and Chris was working on Argyranthemum (Humphries 1976). The Reading symposium focused on the tribal classification and phytochemistry of the Asteraceae, which with some 25,000 species is one of the largest of flowering plant groups. The classification of Asteraceae in use at that time was essentially George Bentham’s nineteenth century division of the family into about a dozen tribes defined by a variety of morphological characters (Bentham 1873). Much of the discussion at the symposium centered on the delimitation of tribes and the tribal position of various odd genera. Among the “problem” genera discussed at the Reading symposium were Osmitopsis, Cotula, and Ursinia, relative to whether they were or were not part of the Anthemideae (the reason for those discussions are evident today, as the three genera are now placed close to the root of the Anthemideae phylogenetic tree; Osmitopsis may even be sister to all other Anthemideae). In Bentham’s classification, the genera of the tribe Anthemideae were artificially grouped in two subtribes defined by the presence or absence of receptacular scales, respectively. Chris and Vernon Heywood, in their review of the tribe for the Reading symposium (Heywood and Humphries 1977), abandoned this classification and arranged the genera into a number of informal groups based on geographic distribution (again the biogeography connection!). The Mediterranean group

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comprises many familiar genera, such as the closely related Glebionis, Ismelia, and Argyranthemum. Glebionis is the name now applied to the familiar European species Chrysanthemum coronarium, as the generic name Chrysanthemum has been conserved for the horticultural species, whose origins are in Asia. As noted by N.N. Tzvelev, the latter are related to Artemisia and other Asian genera and not to the Mediterranean plants. Anacyclus, another genus Chris worked on (Humphries 1979b), also belongs to the Mediterranean group. The uncertainty of subtribal groupings in the Anthemidae coupled with their expertise in the taxonomy and morphology of key genera in the tribe led Chris and Bremer eventually to work on the phylogeny of the Anthemideae using cladistic methodology. The data were morphological characters and some chemical information. The Anthemideae had around 1,800 species in more than 100 genera (today 111 genera are recognized). Anthemideae are annuals or perennials, mostly with variously dissected leaves. The capitula are white-rayed, yellow-rayed, or discoid, sometimes disciform with central hermaphroditic flowers and peripheral tubular female flowers without a limb. Most importantly, the fruits or cypselas have a very variable morphology with different numbers and arrangements of ribs, sometimes with myxogenic cells or different types of hairs, sometimes being laterally or dorsoventrally compressed. These morphological characters—particularly those of the fruits—were used for the cladistic analysis. After summarizing what was known, or rather believed, about the phylogeny, Chris drew up a provisional cladogram. The diagram, preserved for posterity, was dated March 20, 1982. All characters were scored for all genera, and data matrices for the whole tribe as well as for the individual subtribes were analyzed using Hennig86 (Farris 1988). Finally, in 1993, a generic monograph of the Anthemideae, with phylogenies, a generic and subtribal classification, and lists of all recognized species, was published (Bremer and Humphries 1993). In all, 12 subtribes, 108 genera, and 1,741 species were recognized, based on an analysis of 182 characters. This cladistic classification of the Anthemideae, based on in-depth analysis of morphological data, although completed before access to molecular data, represented a considerable step forward in understanding. The framework provided by Bremer and Humphries (1993) acted as a springboard from which to launch various research programs, some made tractable by the accumulation of DNA sequence data. Bremer and Humphries’s work has now been largely superseded by recent cladistic

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analyses based on nuclear DNA sequences from the internal transcribed spacer (ITS) region for the Mediterranean genera (Oberprieler et al. 2007) and chloroplast DNA sequences from the NADH dehydrogenase F (ndhF) region for the South African ones (Himmelreich et al. 2008).

BIOGEOGRAPHIC CLADISTICS

Historical biogeography experienced a revolution during the 1970s and 1980s similar to that in systematics, also triggered by the work of Willi Hennig. Hennig was an entomologist, and his early works in German were read by the Swedish chironomid midge specialist Lars Brundin. Chironomid midges have an intriguing Southern Hemisphere distribution, and Brundin used Hennig’s argumentation scheme for chironomid relationships to formulate hypotheses about their biogeographic history. Brundin’s biogeographic approach adopted from Hennig may be described as a combination of distribution analysis and dispersal assumptions, the latter being firmly rejected by later generations in developing historical biogeography in a phylogenetic or cladistic context. Among these future developers of historical biogeography were Gareth Nelson, Donn Rosen, and Norman Platnick, all at the American Museum of Natural History in New York, and later, of course, also Chris. Nelson had spent a year during the mid-1960s at the Swedish Museum of Natural History in Stockholm where Brundin was professor, and came across Brundin’s then recently published monumental work on chironomid midges and transantarctic relationships (Brundin 1966). It was the emphasis on geography and relationships implicit in the title of Brundin’s monograph (“Transantarctic Relationships and Their Significance . . .”) that attracted Nelson’s interest. Nelson, an ichthyologist, knew the British fossil fish expert Colin Patterson who introduced the subject of phylogenetic systematics and related biogeographic issues at the Natural History Museum. Zoologists, in particular Rosen, Nelson, and Platnick, developed the new approach to historical biogeography during the 1970s. A seminal paper was the critique by Croizat et al. (1974) of dispersal assumptions in biogeography, “Centers of Origin and Related Concepts.” In 1978, Rosen and Nelson arranged a symposium on vicariance biogeography, the term used at that time to distinguish the new approach with its focus on patterns of distribution, especially vicariance, rather than hypotheses of dispersal (Nelson and Rosen 1981). Later, Nelson and Platnick developed historical biogeography as an explicit analysis of distribution patterns

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and area relationships, purged of any a priori assumptions of underlying processes, be it vicariance or dispersal (Nelson and Platnick 1981). Brundin had been a biology teacher before he came to the museum in Stockholm, and among his pupils was Hans-Erik Wanntorp. It was Bremer and Wanntorp, both at Stockholm University, who first mentioned vicariance biogeography in the context of botanical phylogenetic systematics, at least in the pages of Taxon: “The reconstruction [of the phylogeny] can often be tested against the distribution of the group, where vicariance patterns indicate sister group relations. This has been called the chorological method and it is an important aid in phylogenetic reconstruction” (Bremer and Wanntorp 1978: 320). But it was not until Chris’s study of the southern beeches (Nothofagus) that any serious work on cladistic biogeography was undertaken by a botanist (Humphries 1981a, 1981b, 1983; and, later, on its parasites, Humphries et al. 1986). Progress in vicariance biogeography, or cladistic biogeography as Chris preferred to call it, was enhanced and developed by Chris’s association with two people: Lynne Parenti (see Chapter 15) and Pauline Ladiges (see Chapter 14). As a result of his collaboration with Ladiges, cemented during two sabbaticals in Melbourne and fed by a love of the Australian flora, Chris was involved in a series of papers applying rigorous cladistic biogeographic analyses of several groups of Australian eucalypts (Ladiges et al. 1983, 1987, 1989; Ladiges and Humphries 1986). Lynne Parenti and Chris together published two editions of their textbook Cladistic Biogeography (Humphries and Parenti 1986, 1999)— interpreting patterns of plant and animal distributions and laying out methodology in an explicit way.

CLOSE

Chris blazed a trail for botany at the Natural History Museum and beyond—and his influence extended to other museum departments, becoming a member of another more multidisciplinary Museum gang, a Gang-of-Five (as opposed to the museum’s Gang-of-Four; see Gee 1999), the five being Colin Patterson, Dick Vane-Wright, Brian Gardiner, Peter Forey, and Chris (Forey et al. 2000: 72, for photograph; see also the account in Humphries 2000 and some more details in Blackmore and Wortley, Chapter 2, this volume). Chris recalled being first introduced to Colin Patterson by Dick Vane-Wright in 1975 after Colin had

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lectured to the museum staff on cladistics (Humphries 2000:69). That association developed into friendship once Chris returned from his first trip to Australia in 1981, a friendship cemented over the creation of The Evolving Biosphere (edited by Peter Forey; Forey 1981), the museum’s 1981 bicentennial scientific review, with the biogeography section having critical papers from both Patterson and Chris, and an insightful introduction from Peter Forey (Forey 1981; Humphries 1981a; Patterson 1981a). Chris documented something of the relationships among the five in his article for Colin Patterson’s memorial publication published by the Linnean Society (Humphries 2000: 69). Patterson died in 1998, and both Dick Vane-Wright and Peter Forey (Gardiner and Longbottom 2008; and other papers in Special Publication 295 of the Geological Society of London) are now retired. In spite of times moving on—and rapidly backwards, if some of the more recent contributions to Taxon are anything to go by— the efforts of this group, and Chris for botany, are of some significance and of historical importance. It is often said that cladistics—in general and in particular—helped place systematics on a firmer, more scientific foundation. But reflecting on the past half century (1950–2000), it is of greater importance to recognize that the sweep of systematics, the last two centuries of endeavor, from Candolle to Nelson (Williams and Ebach 2009), from Linnaeus to Hennig (Wheeler 2008), from Goethe to Brady (Ebach 1999), captures the essence of cladistics, a project—or research program—that seems to slip off the tracks every now and then.

REFERENCES Baum B.R., Duncan T., Phillips, R.B. 1984. A bibliography of numerical phenetic studies in systematic botany. Ann. Missouri Bot. Gard. 71: 1044–1060. Bentham G. 1873. Notes on the classification, history, and geographical distribution of Compositae. J. Linn. Soc. Bot. 13: 335–577. Béthoux O, Kristensen N.P., Engel M.S. 2008. Hennigian systematics and the “Groundplan” vs. “Post-Groundplan” approaches: A reply to Kukalová-Peck. Evol. Biol. 35: 317–323. Bremer K. 1972. A revision of the genus Osmitopsis (Asteraceae). Bot. Notiser. 125: 9–48. Bremer K., Wanntorp H.-E. 1978. Phylogenetic systematics in botany. Taxon 27: 317–329. Bremer K., Wanntorp H.-E. 1981a. A cladistic classification of green plants. Nordic J. Bot. 1: 1–3. Bremer K., Wanntorp H.-E. 1981b. The cladistic approach to plant classification. In: Funk V.A., D. R. Brooks, editors. Advances in cladistics: Proceedings of

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the 1st Meeting of the Willi Hennig Society. Bronx : The New York Botanical Garden pp. 87–94. Bremer K., Humphries C.J. 1993. A monograph of the Compositae: Anthemideae. Bull. Brit. Mus. (Nat. Hist.), Bot. 23: 73–179. Brundin L. 1966. Transantarctic relationships and their significance as evidenced by chironomid midges. Kungl. Sv. Vetenskapsakad. Handl. (ser. 4), 11: 1472. Brundin L. 1993. From Grimsgöl to Gondwanaland—Half a century with Chironomids. Cladistics 9: 358–367. Brundin L. 1995. Frå Grimsgöl till Gondwanaland—en smålännings mödor under ett halvsekel som jädermyggsfors [From the Grimsgöl pond to Gondwanaland—Endeavours during half a century as student of chironomid midges] (edited by P. Lindskog). Ent. Tidskr. 116: 1–12. Burger W.C. 1979. Cladistics: Useful tool or rigid dogma? Taxon 28: 385–386. Cannon J.F.M. 2001. Edward Benedict Bangerter (1911–2001) [Obituary]. Watsonia 24: 128–129. Carine M.A., Humphries C.J., Guma I.R., Reyes-Betancort J.A., Santos-Guerra A. 2009. Areas and algorithms: Evaluating numerical approaches for the delimitation of areas of endemism in the Canary Islands archipelago. J. Biogeogr. 36: 593–611. Churchill S.P., Wiley E.O., Hauser L.A. 1984. A critique of Wagner groundplandivergence studies and a comparison with other methods of phylogenetic analysis. Taxon 33: 212–232. Danser B.H. 1950. A theory of systematics. Biblioth. Biotheor. 4: 117–180. Ebach M.C. 1999. Anschauung and the archetype: The role of Goethe’s delicate empiricism in comparative biology. Janus Head 8: 254–270. Ebach M.C., Humphries C.J. 2002. Cladistic biogeography and the art of discovery. J. Biogeogr. 29: 427–444. Ehrendorfer F., Schweizer D., Greger H., Humphries C. J. 1977. Chromosome banding and synthetic systematics in Anacyclus. (Asteraceae–Anthemideae). Taxon 26: 387–394. F[aegri] K. 1979. The emperor’s new taxonomic dress. Taxon 28: 168. Farrar D.R. 2003. Warren H. Wagner, Jr. 1920–2000. Biogr. Mem. Natl. Acad. Sci. U.S.A. 83: 1–20. Farris J.S. 1970. Methods for computing Wagner trees. Syst. Zool. 19: 83–92. Farris J.S. 1988. Hennig86, version 1.5 manual/software and MSDOS program. Port Jefferson Station, NY: Author. Farris J.S., Kluge A.G. 1979. A botanical clique. Syst. Zool. 28: 400–411. Farris J.S., Kluge A.G. 1986. Synapomorphy, parsimony, and evidence. Taxon 35: 298–306. Farris J.S., Kluge A.G., Eckhart, M.J. 1970. A numerical approach to phylogenetic systematics. Syst. Zool. 19: 172–189. Forey P.L. (editor). 1981. The evolving biosphere. London: BMNH/Cambridge University Press. Forey P.L., Humphries C.J., Kitching I.L., Scotland R.W., Siebert D.J., Williams D.M. 1992. Cladistics: A practical course in systematics. Oxford: Clarendon Press. Forey P.L. Gardiner B.G., Humphries C.J. (editors). 2000. Colin Patterson (1933–1998): A celebration of his life. The Linnean, Special Issue No. 2: 1–96.

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Funk V.A., Wagner W.H. Jr. 1982. A bibliography of botanical cladistics: I. 1981. Brittonia 34: 118–124. Gardiner B., Longbottom A. 2008. Peter L. Forey. In: Cavin L., Longbottom A., Richter M., editors. Fishes and the break-up of Pangaea. Special Publication 295. London: Geological Society pp. 1–6. Gee H. 1999: In search of deep time: Beyond the fossil record to a new history of life. New York: Free Press. Guédès M. 1982. Nothing new with cladistics. Taxon 31: 95–96. Heywood V.H., Harborne J.B., Turner B.L., (editors) 1977. The biology and chemistry of the Compositae. London: Academic Press. Heywood V.H., Humphries C.J. 1977. Anthemideae—Systematic review. In: Heywood V.H., Harborne J.B., Turner B.L., editors. The biology and chemistry of the Compositae. London: Academic Press pp. 851–898. Himmelreich S., Källersjö M., Eldenäs P., Oberprieler C. 2008. Phylogeny of southern hemisphere Compositae-Anthemideae based on nrDNA ITS and cpDNA ndhF sequence information. Pl. Syst. Evol. 272: 131–153. Humphries C.J. 1973. A taxonomic study of the genus Argyranthemum Webb ex Schultz Bip. Ph.D. thesis. University of Reading. Humphries C.J. 1974. An account of the genus Argyranthemum. In: Bramwell D., Bramwell Z., editors. Wild flowers of the Canary Islands. London: Stanley Thornes Ltd. pp. 210–214. Humphries C.J. 1976. A revision of the Macaronesian genus Argyranthemum Webb ex Schultz Bip. Bull. Brit. Mus. (Nat. Hist.), Bot. 5: 145–240. Humphries C.J. 1979a. Endemism and evolution in Macaronesia. In: Bramwell D., editor. Plants and islands. London: Academic Press pp. 171–199. Humphries C.J. 1979b. A revision of the genus Anacyclus L. (Compositae: Anthemideae). Bull. Brit. Mus. (Nat. Hist.), Bot. 7: 83–142. Humphries C.J. 1979c. [Review of] The biology and chemistry of the Compositae, V.H. Heywood, J.B. Harborne, B.L. Turner, editors. Watsonia 12: 264–265. Humphries C.J. 1981a. Biogeographical methods and the southern beeches. In: Forey P.L., editor. The evolving biosphere. London: BMNH/Cambridge University Press pp. 282–297. Humphries C.J. 1981b. Biogeographical methods and the southern beeches. In: Funk V.A., Brooks D.R., editors. Advances in cladistics: Proceedings of the 1st Meeting of the Willi Hennig Society. Bronx: New York Botanical Garden, pp. 177–207. Humphries C.J. 1983. Biogeographical explanations and southern beeches. In: Sims R.W., Price J.H., Whalley P.E.S., editors. Evolution, time and space: The emergence of the biosphere. London: Academic Press pp. 335–365. Humphries C.J. 1989. Modern data sets for flowering plants. In: Fernholm B., Bremer K., Jornvall H., editors. The hierarchy of life. Cambridge: Elsevier pp. 215–226. Humphries C.J. 2000. On friendship. In: Forey P.L. Gardiner B.G., Humphries C.J., editors. Colin Patterson (1933–1998): A celebration of his life. The Linnean, Special Issue No. 2: 67–74. Humphries C.J., Ebach M.C. 2004. Biogeography on a dynamic earth. In: Lomolino M.V., Heaney L.R., editors. Frontiers of biogeography: New

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directions in the geography of nature. Chicago: University of Chicago Press pp. 67–86. Humphries C.J., Funk V.A. 1984. Cladistic methodology. In: Heywood V.H., Moore D.M., editors. Current concepts in plant taxonomy. Systematics Association Special Volume 25. London: Academic Press pp. 323–362. Humphries C.J., Parenti L. 1986. Cladistic biogeography. Oxford: Clarendon Press. Humphries C.J., Parenti L. 1999. Cladistic biogeography. Interpreting patterns of plant and animal distributions. 2nd ed. Oxford: Clarendon Press. Humphries C.J., Richardson P.M. 1980. Hennig’s methods and phytochemistry. In: Bisby F., Vaughan J.G., Wright C.A., editors. Chemosystematics: Principles and practice. London: Academic Press pp. 353–378. Humphries C.J., Nielsen E.S., Cox J. 1986. Nothofagus and its parasites. In: Stone A.R., Hawksworth D.L., editors. Coevolution. Oxford: Oxford University Press pp. 55–76. Jansen P., Wachter W.H. 1943. In memoriam. Benedictus Hubertus Danser. Ned. Kruidk. Arch. 53: 129–136. Koponen T. 1968. Generic revision of Mniaceae Mitt. (Bryophyta). Ann. Bot. Fenn. 5: 117–151. [Reprinted in Duncan T., Stuessy T.F., editors. 1985. Cladistic theory and methodology. New York: Van Nostrand Reinhold Company pp. 103–137.] Kukalová-Peck J. 2008. Phylogeny of higher taxa in Insecta: Finding synapomorphies in the extant fauna and separating them from homoplasies. Evol. Biol. 35: 4–51. Ladiges P.Y., Humphries C.J. 1983. A cladistic study of Arillastrum, Angophora and Eucalyptus (Myrtaceae). Bot. J. Linn. Soc. 87: 105–134. Ladiges P.Y., Humphries C.J. 1986. Relationships in the stringybarks, Eucalyptus L’Herit. informal subgenus Monocalyptus series Capitellatae and Olsenianae: Phylogenetic hypotheses, biogeography and classification. Austral. J. Bot. 34: 603–631. Ladiges P.Y., Humphries C.J., Brooker M.I.H. 1983. Cladistic relationships and biogeographical patterns in the peppermint group of Eucalyptus (Informal subseries Amygdalinae, subgenus Monocalyptus) and the description of a new species, E. willisii. Austral. J. Bot. 31: 565–584. Ladiges P.Y., Humphries C.J., Brooker M.I.H. 1987. Cladistic and biogeographic analysis of Western Australian species of Eucalyptus L’Hérit., informal subgenus Monocalyptus Pryor & Johnson. Austral. J. Bot. 35: 251–281. Ladiges P.Y., Newnham M., Humphries C.J. 1989. Systematics and biogeography of the Australian “Green Ash” eucalypts (Monocalyptus). Cladistics 5: 345– 364. Leadlay E., Jury S. 2006. Taxonomy and plant conservation: The cornerstone of the conservation and the sustainable use of plants. Cambridge: Cambridge University Press. Meeuse A.D.J. 1981. Again: Cladistics in botany. Taxon 31: 642–644. Mishler B.D., Bremer K., Humphries C.J., Churchill S.P. 1988. The use of nucleic acid sequence data in phylogenetic reconstructions. Taxon 37: 391–395. Mitter C. 1981. “Cladistics” in botany. Syst. Zool. 31: 373–378.

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Nelson G., Platnick N.I. 1981. Systematics and biogeography—Cladistics and vicariance. New York: Columbia University Press. Nelson G., Rosen D.E. 1981. Vicariance biogeography—A critique. New York: Columbia University Press. Oberprieler C., Himmelreich S., Vogt R. 2007. A new subtribal classification of the Anthemideae (Compositae). Willdenowia 37: 89–114. Parenti L.R. 1980. A phylogenetic analysis of the land plants. Biol. J. Linn. Soc. 13: 225–242. Parenti L. 1981. Cladistics and conventions. Taxon 31: 96–101. Parenti L., Humphries C.J. 2004. Historical biogeography, the natural science. Taxon 53: 899–903. Patterson C. 1981a. The development of the North American fish fauna—A problem of historical biogeography. In: Forey P.L., editor. The evolving biosphere. London: British Museum (Natural History) pp. 265–281. Patterson C. 1981b. Significance of fossils in determining evolutionary relationships. Annual Rev. Ecol. Syst. 12: 195–223. Smoot E.L., Jansen R.K., Taylor T.N. 1981. A phylogenetic analysis of the land plants: A botanical commentary. Taxon 30: 65–57. Sneath P.H.A. 1995. Thirty years of numerical taxonomy. Syst. Zool. 44:281– 298. Sneath P.H.A., Sokal R.R. 1973. Numerical taxonomy. San Francisco: Freeman. Vane-Wright R.I., Humphries C.J., Williams P.H. 1991. What to protect?— Systematics and the agony of choice. Biol. Conservation 55: 235–254. Wagner W.H., Jr. 1952. The fern genus Diellia: Its structure, affinities and taxonomy. Univ. Calif. Publ. Bot. 26: 1–212. Wagner W.H., Jr. 1969. The construction of a classification. In Sibley, G. [chairman], Systematic biology: Proceedings of an international conference, conducted at the University of Michigan, Ann Arbor, June 14–16, 1967, sponsored by the National Research Council. Washington, D.C.: National Academy of Sciences pp. 67–90. Wagner W.H. 1980. Origin and philosophy of the groundplan-divergence method of cladistics. Syst. Bot. 5: 173–193. Wanntorp H.-E. 1980. Theory and dogma in systematics. Taxon 29: 668–670. Wanntorp H.-E. 1983. Cladistics misunderstood—again. Taxon 32: 97–98. Wanntorp H.-E. 1993. Lars Brundin 30 May 1907–17 November 1993. Cladistics 9: 357–367. Walters S.M. 1995. The taxonomy of European vascular plants: A review of the past half-century and the influence of the Flora Europaea project. Biol. Rev. Cambridge Philos. Soc. 70: 361–374. Wheeler Q.D. 2008. Undisciplined thinking: Morphology and Hennig’s unfinished revolution. Syst. Entom. 33: 2–7. Wiley E.O. 1980. Phylogenetic systematics and vicariance biogeography. Syst. Bot. 5: 194–220. Williams D.M., Ebach M.C. 2009. What, exactly, is cladistics? Re-writing the history of systematics and biogeography. Acta Biotheor. 57: 249–268. Young D.A., Richardson P.M. 1982. A phylogenetic analysis of extant seed plants: The need to utilize homologous characters. Taxon 31: 250–254.

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TWO

S t e p h e n B l a c k m o r e a n d A l e x a n d r a H . Wo r t l ey

O N T O G E N Y A N D S Y S T E M AT I C S R E V I S I T E D : D E V E L O P M E N TA L M O D E L S AND MODEL ORGANISMS

It is a distinct pleasure to be invited to contribute to this Festschrift for Chris Humphries, which provides an opportunity to reflect on how much has changed in systematic biology since the 1970s. At that time, Chris and one of us (S.B.) were research students in the Compositae systematics group established by Vernon Heywood in the Botany Department at the University of Reading. The extraordinary level of subsequent progress can well be illustrated by comparing the current state of Compositae systematics with that prevailing in 1975 during the major international symposium at Reading University (Heywood et al. 1977). Those symposium presentations were based upon Cronquist’s (1975) classification of the family. This was, essentially, an informal classification reflecting the overall similarity of taxa and drawing heavily upon earlier treatments, especially the tribal classification of Bentham (1873). Chris Humphries, together with his longtime collaborator, Kåre Bremer, pioneered the application of cladistic methods of phylogeny reconstruction in the Compositae (e.g., Humphries 1979) and soon influenced the systematics of other groups of living and fossil plants. This influence resulted largely from Chris’s

Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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extensive scientific networks and his eagerness to engage with other botanists and to guide them in the interpretation of their data. As this volume testifies, Chris acted as the primary catalyst for the introduction of cladistic thinking into the wider botanical community, especially in the United Kingdom, and, with Vicki Funk, the United States. The adoption of cladistic methodology did not happen without a degree of dogged persistence: Chris Humphries’s paper with Vicki Funk (Humphries and Funk 1984) at a subsequent international symposium also held at Reading, “Current Concepts in Plant Taxonomy,” received a hostile reception from members of the audience. Today, the classification of the Compositae has been turned literally upside-down thanks to the availability of DNA sequence characters and the almost universally adopted procedures of phylogenetic systematics (Funk et al. 2009). The Heliantheae, considered to hold a relatively basal position within the family in 1975, are now known to be among the most derived groups. It is perhaps worth drawing out what these changes have meant for a specialist morphological discipline such as palynology. As Blackmore et al. (2009b) pointed out, in the 1970s evidence from pollen morphology and ultrastructure seemed incongruent with the subtribal classification. This meant that the outstandingly thorough surveys of pollen wall ultrastructure in the family by John Skvarla and colleagues (Skvarla and Larson 1965; Skvarla and Turner 1966; Skvarla et al. 1977) were largely dismissed in terms of their relevance to evolution and systematics. Now that tribal relationships in the Compositae are much more fully understood (Funk et al. 2005), it is clear that the palynological evidence that has been available for some 40 years is in fact highly congruent with the phylogeny (Blackmore et al. 2009b). One dimension of the cladistic revolution, which is not often highlighted, is the way in which it has led to the rehabilitation of morphological studies by providing a fuller phylogenetic framework into which evidence of all kinds can be assimilated on the same principles. There can be little doubt that Chris Humphries’s pivotal role in the promotion of cladistics was greatly enhanced by his appointment to the Department of Botany at the (then) British Museum (Natural History). This placed him at the heart of an important intellectual milieu during its most fruitful and productive period (Hull 1988). In addition to Chris, the regular members of this group included Colin Patterson, Dick Vane-Wright, Peter Forey, Brian Gardiner, and Charlie Jarvis, as well as a regular flow of visiting scientists. Through friendship with Chris, one of us (S.B.) was fortunate to join this circle in the early 1980s and to

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become acquainted with their meeting place, which I liked to call “The Cladist’s Arms.” No doubt this was not the only London pub to have played a seminal role in science and philosophy, but it is not the purpose of this chapter to address that issue in any depth. Looking back over this period, it is notable that, as a member of the “South Kensington Milieu,” Chris Humphries was always to be found at the centre of any emerging topic. His book on biogeography (Humphries and Parenti 1999) provides one such example, but this chapter focuses on his contribution to the field of evolution and development. We will explore this first by focusing on the symposium “Ontogeny and Systematics” that he organized during the Third International Conference on Systematic and Evolutionary Biology (ICSEB III) in Brighton in 1985. We will then consider how the field of ontogeny and systematics has developed through to the present day, with particular emphasis on pollen ontogeny. We conclude that, in part through the 1985 symposium, Chris Humphries played an influential role in the emergence of the discipline now recognized as “evo-devo” (Pennisi and Roush 1997; Cronk et al. 2002). Within systematics as a whole, the impact of this renewed focus on developmental biology has been profound (e.g., Patterson 1983).

ONTOGENY AND SYSTEMATICS REVISITED

The symposium held at ICSEB III resulted in a publication containing seven very different contributions (Humphries 1988). In his introduction to the book, Humphries suggested, “The recent revival in systematics of whole life cycles has its origins in the contributions of Nelson (1978) and Løvtrup (1974, 1978).” He pointed to the resurgence of interest in von Baer’s (1828) biogenetic law, following Nelson’s (1978: 324) restatement in the following form: “Given an ontogenetic character transformation, from a character observed to be more general to a character observed to be less general, the more general character is primitive and the less general advanced.” Several of the contributions to Ontogeny and Systematics explored this theme further (Weston 1988; Kluge 1988; Mishler 1988), with the authors varying in the extent to which they supported Nelson’s restated biogenetic law. The debate at that time revolved around whether the ontogenetic criterion might displace out-group comparison as the preferred method for determining the polarity of character transformations. Other contributions examined the nature of homology (Roth 1988) and of development itself (André 1988; Løvtrup 1988).

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In that same volume, Blackmore and Crane (1988) presented a discussion of pollen and spore ontogeny, attempting to identify systematically informative differences in the basic pattern of pollen and spore development that had been worked out in the 1960s and 1970s. They had a particular interest in developing predictive models for the determination of structure at microscopic and macroscopic levels. Such models have the potential to be useful in exploring the developmental basis and homology of morphological characters. One of their examples concerned the dispersal of pollen grains in permanent tetrads, a syndrome that has been found in over fifty families of flowering plants (Walker and Doyle 1975) and has therefore generally been interpreted as a highly plastic character. At the level of flowering plants, dispersal in tetrads is therefore homoplasious, although it can be informative in more restricted contexts. Based on comparison of several developmental studies, Blackmore and Crane (1988) proposed that variations in the deposition of the callose special cell wall formed following meiosis in anthers can account for the differences in the degree of fusion between individual daughter cells. The abbreviation or deletion of the callose synthesis stage, which was suggested as the basis of fusion in permanent tetrads, was interpreted as being paedomorphic through progenesis in the sense of Alberch et al. (1979). Predictive models are intended to be testable, and since the mid-1980s there has been a significant increase in the extent to which developmental mutants are used to dissect and explore experimental pathways. It was therefore very satisfying when in 1994 Daphne Preuss and colleagues described the qrt mutants in Arabidopsis thaliana (Preuss et al. 1994) and used the model proposed by Blackmore and Crane (1988) to explain the fusion of pollen into permanent tetrads (Figs. 2.1, 2.2). Previously unpublished transmission electron micrographs of developing anthers of the qrt mutants show the direct contact that exists between developing exines, because of the greatly reduced individual special cell walls surrounding the meiotic products. What Preuss et al. (1994) found most valuable about the qrt mutants was the opportunity they provided for analyzing the genetic makeup of the products of meiosis. One observation that can be made from this is that predictive models become more powerful when the underlying mechanisms are understood. Frequently, this understanding comes first from model organisms such as Arabidopsis. Other palynological characters discussed by Blackmore and Crane (1988) included the homologies of exine layers in angiosperms and gymnosperms; the highly reduced exines of certain angiosperms in Zingiberaceae, Lauraceae, Hydrocharitaceae, and Cymodoceaceae; aperture

FIGURE 2.1 Front cover of Science magazine, June 3, 1994; plate from Preuss et al. (1994) showing the first published images of the qrt mutant of Arabidopsis thaliana. Reprinted with permission from AAAS.

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FIGURE 2.2 Transmission electron micrograph of developing microspore tetrad in the qrt mutant of Arabidopsis thaliana. Specimen fixed with glutaraldehyde and stained with uranyl acetate. Arrows indicate points in a tetrad of microspores where the developing exines form in contact because of the reduced callose special cell wall. Scale bar = 20 μm.

formation; and saccus and cavea formation. Since then, much more has become known about each of these characters, and this additional knowledge comes from several distinct sources: comparative developmental studies of taxa with different pollen morphology, predictive models, and developmental mutants. A recent review of pollen development summarizes the present state of knowledge for flowering plants (Blackmore et al. 2007). One important conclusion from this review is that, while some elements of pollen and spore development are under direct or complex genetic control in which mutations will lead to different phenotypes, other elements are not. In terms of the discussion in Ontogeny and Systematics, the latter are epigenetic phenomena sensu Løvtrup (1988). A narrower use of the word epigenetic is sometimes employed by molecular geneticists; but in Løvtrup’s (1988) sense, it can refer to any aspects of development that are not under direct genetic control. If we revisit the other palynological characters discussed by Blackmore and Crane (1988), as these authors did a decade later (Blackmore and

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Crane 1998), the distinction between genetic and epigenetic events in development becomes clearer. Questions of homology between the pollen wall layers of angiosperms and gymnosperms were initially addressed through comparative developmental studies (discussed further in Blackmore 1990; Rowley 1995) and by reference to phylogenies for seed plants based on other types of data-set. Profound new insights came with the development and expansion of models of pollen wall development that incorporated the concept of self-assembly in colloidal solution (Hemsley et al. 1992, 1994, 1996; Gabarayeva and Hemsley 2006; Hemsley and Gabarayeva 2007). Because the distinctive and complex ultrastructure of the mature pollen wall, which can be characteristic and diagnostic of taxa, is now understood to come about through a process of self-assembly, what were once seen to be stark contrasts between angiosperms and gymnosperms can now be viewed quite differently. So powerful is the current model of self-assembly in pollen walls that it can be used to interpret the vast diversity of forms encountered in the complex pollen walls of the Compositae (Blackmore et al. 2009a), including issues such as the presence or absence of a cavea (void within the outer layer of the pollen wall). As is often the case, the insight from models based on self-assembly is helpful but in itself raises new questions. How, for example, are the fine variations in colloidal properties that produce differently shaped structures created? It might be that there are genes involved in the timing and tuning of such processes. A number of mutations have been associated with pollen wall pattern variants in Arabidopsis (reviewed in Blackmore et al. 2007), but their precise pathway of action is not yet clear. The complex pollen walls of the Compositae often show distinct switches between the deposition of one kind of pattern and another (Blackmore et al. 2009a). These switches are interpreted under current models as being triggered at key concentrations within the colloidal environment of the primexine glycocalyx. We can only speculate, however, about whether gene-directed processes may be involved. The mechanisms of aperture positioning, discussed by Blackmore and Crane (1988), are also now better understood and have been found to correlate closely with the relative timing of events during meiosis and the method of cytoplasmic partitioning between daughter cells at the end of meiosis (e.g., Brown and Lemmon 1985, 1991, 2000; Furness and Rudall 1999). Several genes have been identified that regulate meiosis, as have a large number of mutants, including the qrt mutants, which disrupt the normal processes of meiosis. Again, while we now know how apertures are positioned and understand that in most angiosperms an apertural shield (Heslop-Harrison 1972; Sheldon and Dickinson 1983)

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is involved locally in preventing deposition of the pollen wall at apertural sites, we know nothing about the control of aperture shape or complexity. Thus some of the most important characters, widely used in palynology, cannot yet be explained by theoretical models, let alone confirmed by experimental observation. It is clear that in understanding development at the cellular level in pollen grains, and at the multicellular level in whole organisms, much remains unknown. However, the definition by Chris Humphries and others of a research agenda for systematics and ontogeny in the mid-1980s has borne fruit. Since then, the impact of molecular biology has been profound, both in greatly enhancing our understanding of the molecular genetic control of ontogeny and in revolutionizing phylogenetic systematics.

CONCLUSION

We hope we have shown, through a brief survey of some key features of pollen morphology, how our knowledge of development has progressed in leaps and bounds since the symposium Ontogeny and Systematics. While it might be too great a claim to suggest that by virtue of convening one symposium Chris Humphries single-handedly established the field now known as evo-devo research, it is clear that he was one of a small number of scientists who saw the potential to reconnect developmental data with phylogenetics and systematic biology. Progress over the last three decades has often concentrated on model organisms such as Arabidopsis thaliana. Sometimes this has engendered a sense of frustration that so much attention should be focused on a small number of taxa. But the case of pollen morphology reminds us, as would most other cases, that insights from model organisms can play a central role in interpreting the diversity of ontogenetic pathways that produce the extraordinary diversity of life on Earth. However, unless we set out to explore that full diversity, our horizons are too narrow to provide a full understanding. It is important to recognize that predictive models in ontogeny can provide an interface between the particular form encountered in the model organism and the full phenotypic diversity encountered in its close and more distant relatives. Unusual or distinctive phenotypic characters can point to interesting variations in developmental pathways. Great progress in understanding development has come from molecular genetics; but today, three decades after Ontogeny and Systematics, it is clear that there is much to be done to fully understand epigenetic phenomena

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(Grant-Downton and Dickinson 2005, 2006). We are at an important crossroads as awareness grows that genes do not directly explain everything and that what has been disregarded as noncoding, seemingly junk DNA, actually does things within cells! Clearly, there is still much to look forward to in the field of ontogeny and systematics.

Acknowledgments

The authors are grateful to Louise Allen for preparation of the transmission electron micrographs included here and to Daphne Preuss and Science magazine for permission to reproduce their plates and cover image.

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Brown R.C., Lemmon, B.E. 2000. The cytoskeleton and polarization during pollen development in Carex blanda (Cyperaceae). Amer. J. Bot. 87: 1–11. Cronk Q.C.B., Bateman, R.M., Hawkins, J.A. (editors). 2002. Developmental genetics and plant evolution. London: Taylor and Francis. Cronquist A. 1975. Some thoughts on angiosperm phylogeny and taxonomy. Ann. Missouri Bot. Garden 62: 517–520. Funk V.A., Bayer R.J., Keeley S.C., Chan R., Watson L., Gemeinholzer B., Schilling E., Panero J.L., Baldwin B.G., Garcia-Jacas N., Susanna A., Jansen R.K. 2005. Everywhere but Antarctica: Using a supertree to understand the diversity and distribution of the Compositae. Biol. Skripta 55: 343–374. Funk V.A., Susanna A., Stuessy T., Bayer, R. (editors). 2009. Systematics, evolution and biogeography of the Compositae. Vienna: International Association for Plant Taxonomy. Furness C.A., Rudall P.J. 1999. Microsporogenesis in monocotyledons. Ann. Bot. 84: 475–499. Gabarayeva N., Hemsley A.R. 2006. The role of self-assembly in the development of pollen wall structure. Rev. Palaeobot. Palynol. 138: 121–139. Grant-Downton R.T., Dickinson, H.G. 2005. Epigenetics and its implications for plant biology. 1. The epigenetic network in plants. Ann. Bot. 96: 1143–1164. Grant-Downton R.T., Dickinson, H.G. 2006. Epigenetics and its implications for plant biology. 2. The “epigenetic epiphany”: Epigenetics, evolution and beyond. Ann. Bot. 97: 11–27. Hemsley A.R., Gabarayeva N. 2007. Exine development: The importance of looking through a colloid chemistry “window.” Pl. Syst. Evol. 263: 25–49. Hemsley A.R., Collinson M.E., Brain A.P.R. 1992. Colloidal crystal-like structure of sporopollenin in the megaspore walls of recent Selaginella and similar fossil spores. Bot. J. Linn. Soc. 108: 307–320. Hemsley A.R., Collinson, M.E., Kovach, W.L., Vincent, B., Williams, T. 1994. The role of self-assembly in biological systems: evidence from iridescent colloidal sporopollenin in Selaginella megaspore walls. Phil. Trans. R. Soc. Lond. Series B, Biol. Sci. 345: 163–173. Hemsley A.R., Jenkins P.D., Collinson M.E., Vincent B. 1996. Experimental modelling of exine self-assembly. Bot. J. Linn. Soc. 121: 177–187. Heslop-Harrison J. 1972. Pattern in plant cell walls: Morphogenesis in miniature. Proc. Royal Inst. Great Britain 45: 335–351. Heywood V.H., Harborne J.B., Turner B.L. 1977. An overture to the Compositae. In: Heywood V.H., Harborne J.B., Turner B.L., editors. The biology and chemistry of the Compositae. London: Academic Press pp. 1–20. Hull D.L. 1988. Science as a process: An evolutionary account of the social and conceptual development of science. Chicago: University of Chicago Press. Humphries C.J. 1979. A revision of the genus Anacyclus (Compositae: Anthemideae). Bull. Brit. Mus. (Nat. Hist.), Bot. 7: 83–142. Humphries C.J. (editor). 1988. Ontogeny and systematics. New York: Columbia University Press, New York. Humphries C.J., Funk V.A. 1984. Cladistic methodology. In: Heywood V.H., Moore D.M., editors. Current concepts in plant taxonomy. Systematics Association Special Volume 25. London: Academic Press pp. 323–362.

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Humphries C.J., Parenti L. 1999. Cladistic biogeography. Interpreting patterns of plant and animal distributions. 2nd ed. Oxford: Clarendon Press. Kluge A.G. 1988. The characterization of ontogeny. In: Humphries C.J. editor. Ontogeny and systematics. New York: Columbia University Press pp. 57–82. Løvtrup S. 1974. Epigenetics. Hoboken, NJ: Wiley. Løvtrup S. 1978. Ontogeny and phylogeny. Syst. Zool. 27: 125–130. Løvtrup S. 1988. Epigenetics. In: Humphries C.J., editor. Ontogeny and systematics. New York: Columbia University Press pp. 189–227. Mishler B.D. 1988. Relationships between ontogeny and phylogeny, with reference to bryophytes. In: Humphries C.J., editor. Ontogeny and systematics. New York: Columbia University Press pp. 117–136. Nelson G. 1978. Ontogeny, phylogeny, paleontology, and the biogenetic law. Syst. Zool. 27: 324–345. Patterson C. 1983. How does ontogeny differ from phylogeny? In: Goodwin B. C., Holder N., Wylie C. C., editors. Development and evolution. Cambridge: Cambridge University Press pp. 1–31. Pennisi E., Roush W. 1997. Developing a new view of evolution. Science 277: 34–37. Preuss D., Rhee S.Y., Davis R.W. 1994. Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264: 1458–1460. Roth V.L. 1988. The biological basis of homology. In: Humphries C.J., editor. Ontogeny and systematics. New York: Columbia University Press pp. 1–26. Rowley, J.R. 1995. Are the endexines of pteridophytes, gymnosperms and angiosperms structurally equivalent? Rev. Palaeobot. Palynol. 85: 13–24. Sheldon J.M., Dickinson H.G. 1983. Determination of patterning in the pollen wall of Lilium henryi. J. Cell Science 63: 191–208. Skvarla J., Larson D.A. 1965. An electron microscopic study of pollen morphology in the Compositae with special reference to the Ambrosiinae. Grana 6: 210–269. Skvarla J., Turner B.L. 1966. Systematic implications from electron microscopic studies of Compositae pollen – A review. Ann. Missouri Bot. Gard. 53: 220–256. Skvarla J., Turner B.L., Patel V.C., Tomb A.S. 1977. Pollen morphology in the Compositae and in morphologically related families. In: Heywood V.H., Harborne J.B., Turner B.L., editors. The biology and chemistry of the Compositae. London: Academic Press pp. 141–248. Von Baer K.E. 1828. Über Entwickelungsgeschichte der Thiere (volume 1). Königsberg, Germany: Den Gebrüdern Bornträger. Walker J.W., Doyle, J.A. 1975. The bases of angiosperm phylogeny: Palynology. Ann. Missouri Bot. Gard. 62: 664–723. Weston P.H. 1988. Indirect and direct methods in systematics. In: Humphries C.J., editor. Ontogeny and systematics. New York: Columbia University Press pp. 27–56.

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THREE

R i c h a r d I . Va n e - W r i g h t

ROOTED IN CLADISTICS Chris Humphries, Conservation—and Beyond? In the eyes of many people the conservation of plants means the preservation of rare and beautiful species from depletion and destruction by the activities of humans. Such a concept still has considerable importance today, but there has been a tremendous increase in ecological understanding and conservation must now go much further than the mere protection of individual plant species. We must understand the essential role that all plants play in the survival of the interrelating entirety of the living world. . . . The only way for the ensured protection of wildlife is for mankind to resolve to understand his place in the world and to make the very necessary efforts towards conservation. Humphries (1974: 121–122)

The various contributions that Chris Humphries made to the biodiversity conservation movement during the early 1990s were literally and severally “rooted in cladistics”—and my purpose here is to give some flavor of that. However, I also wish to make a personal reflection on the “beyond”—the holistic approach to life—something already identifiable

Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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as “the interrelating entirety of the living world” in the first published comments that Chris ever made on the general issue of conservation (Humphries 1974, quotation above). Soon after finishing his PhD, Chris arrived in the Botany Department of the Natural History Museum, London. In that rarefied atmosphere, he had an impact somewhat akin to a tornado. At that time I was very interested in coevolution—I wanted to try to understand the evolution of mimicry by comparing cladograms for mimetic butterflies, their models, and their host plants. In reality, little of this happened. I remember, maybe a couple of years later, Chris and I made a bid for a joint Natural History Museum PhD studentship, in which the lucky appointee would be expected to study the phylogenetics of both the Passifloraceae and the butterfly genus Heliconius. This idea was turned down on the grounds that it was “too difficult”—not meaning that the science was too difficult, but the radical notion of collaboration between two Natural History Museum departments was too difficult to manage! Despite this setback, I kept talking to the brilliant new man on the botanical block, especially as most botanists at the time still rejected any phylogenetic approach to systematics (also “too difficult,” maybe?), in favor of evolutionary or phenetic classification. Little did I realize that my naïve enthusiasm for Willi Hennig would have such an impact: Chris’s contributions to what became cladistics soon far outstripped my own—and have done so ever since.

THE CALL FOR A “CALCULUS OF BIODIVERSITY”

One of Chris’s earliest publications (he first published in 1971) was his chapter on plant conservation in the 1974 book National Parks of the World, already noted. In those days Chris was an enthusiastic supporter of the conservation movement, notably the direct-action variety championed by the Fauna Preservation Society (now Fauna and Flora International). However, I think it is true to say that Chris did not get involved in methodological research on conservation issues until he and I got together right at the end of the 1980s, to refine and develop the notion of “critical faunas analysis” that had been introduced by Ackery and Vane-Wright (1984), and subsequently followed up by Collins and Morris (1985). Chris and I shared a sense of frustration at the ad hoc and inflexible nature of contemporary approaches to determining conservation area

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networks. Believe it or not, we were also inspired by a major speech made by Margaret Thatcher to the United Nations General Assembly (Thatcher 1989 [in part drafted by Sir Crispin Tickell]). We felt that a systematic approach would have to embrace knowledge of both the geographic distribution of taxa (space/form) and their phylogenetic interrelationships (time). And thus the Biogeography and Conservation Laboratory was formed—a little group founded by Chris and myself, but sustained through most of its 15 years’ existence by the brilliant Paul Williams. Chris’s crucial input came during the first 5 years or so. Another female Tory politician was also important in giving direction to our work. In her opening address to a conference hosted by the Friends of the Earth in 1990, Lynda Chalker stated that we needed “agreement on a global list of centres of biological diversity for priority conservation” (Chalker 1990). We felt confident that the spatial element was covered by the “complementarity principle” (the term complementarity was introduced in the conservation context by Vane-Wright et al. 1991), a procedure for area selection already embraced by critical faunas analysis (and, as we were only to realize later, in methods proposed by several others at much the same time, notably Jamie Fitzpatrick—see Pressey 2002). The novelty that Chris was to bring rested on the idea that cladograms could be used to model taxonomic distinctness and that two measures— one reflecting the distribution of taxa in known geographic space, the other their genealogical relationships through time—could be combined to assess the contribution of any given area to overall biodiversity, in relation to any existing or potential network. We felt we had the beginnings of what Robert May (1990) called for: a “calculus of biodiversity” (for a definition of this concept, see Nee and May 1997). Over a period of weeks we had several false starts. Then Chris arrived in our little laboratory one day and proposed a solution that led to our initial measure—which came to be known as “root weight.” Although now largely superseded in the literature, this measure still has some interesting properties. It was introduced with the following objective in mind: “Our purpose . . . is to introduce the idea of a novel index for measurement of biological diversity which . . . reflects information encoded by cladistic (as distinct from phylogenetic) relationships, and then to apply this index of taxic diversity to wildlife conservation evaluation . . . specifically[,] the problem of how to optimise the use of resources for conservation of biodiversity” (Vane-Wright et al. 1991: 236; all emphases original). However, within a short time, the simplicity of this wholly taxic approach based on cladograms was abandoned, in favor of modeling.

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Although based in part on cladograms, subsequent methods have also embraced branch-length data (empirical and/or modeled), with the aim of maximizing a notional underlying “currency” of diversity—variously described as genetic, feature, or especially, character diversity (e.g., Williams and Humphries, 1994; Williams et al. 1995; for reviews, see Humphries et al. 1995; Humphries 2006). Following, in particular, the work of Dan Faith (e.g. 1992, 1994a, 1994b; Faith and Baker 2006), these new metrics came to be known as phylogenetic diversity measures (PD). This was in distinct contrast to the approach that we had advocated in 1991, as the preceding quote demonstrates, but it was a switch that we and almost all others working in the conservation field at the time came to accept—although some cladists interested in these issues continued for a while with root weight (e.g., Stiassny 1992; Stiassny and de Pinna 1994). With one major exception, the use of root weight in conservation evaluation is now a rarity, and (according to some) it may be misplaced (e.g., Arponen et al. 2005, critiqued by Wolman 2006: 1632–1633). The major exception is its incorporation into the rationale that underpins the outstanding EDGE program (e.g., Isaac et al. 2007; Sitas et al. 2009) being championed by Jonathan Baillie at London’s Institute of Zoology (http://www. edgeofexistence.org/index.php). As with all modeling procedures, once the box was opened, a plethora of different methods started to emerge, all with claims and counterclaims to produce the best or most appropriate results. My point here is not to judge or justify the development and diversification of PD measures. Instead, I want to go back to Chris Humphries’s original formulation of the root weight measure—and try to link that, in a rather philosophical, even metaphysical way, to thinking about what lies “beyond cladistics” (and even beyond science in the narrow sense) for the conservation of biodiversity. In 1990 a concern was, in part, to deal with taxonomic rank and the related issue of taxonomic inflation (see Isaac et al. 2004). Having expanded the circle of ethical concern (more or less but not quite in the sense of Singer 1981) from some humans, to all of humanity, and now to all life, biodiversity conservation and “species rights” had given rise to the problem that all species were then to be seen as equal (before man, if not before God)—including “subspecies,” if upped in rank to full species. But extant species, as perceived in the context of cladograms, are terminal taxa; and, depending on their location in the hierarchy, they are patently not equal in that context, any more than they are equal in other

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ways (e.g., ecological function, population size, population structure, distribution, rarity). We don’t do “billiard ball” atoms anymore, and we shouldn’t do billiard ball species, either. Species are not all equal, in any meaningful way (other than some empty formalism).

THE ROOT WEIGHT MEASURE

Chris’s approach was based on the idea of measuring the amount of information conveyed in a hierarchy, and it drew heavily on a paper by Mickevich and Platnick (1989) entitled “On the Information Content of Classifications,” in which the authors focused on two primary information measures: terms and components. Chris proposed a variant in which terms and components were combined to reflect, very simply and elegantly, the number of taxonomic statements that could be made about each terminal taxon represented in a cladogram (or hierarchical classification). Thus the total information conveyed varies with cladogram topology, even for the same number of terminals. To demonstrate the principles, it is sufficient to look at a single example. Figure 3.1 shows just one of the twelve hierarchies needed to express all possible cladistic relationships for five terminal taxa—including the totally unresolved “bush” (see Vane-Wright et al. 1991: fig. 3, A–L). For the two taxa in the crown group in Figure 3.1, it is possible to make four taxonomic statements about each of them: they form a pair of sister taxa, and these two together form part of three successively

FIGURE 3.1 Derivation of index of taxonomic distinctness, or weight, for a pectinate classification of five terminal taxa. See text for explanation. (Based on Vane-Wright et al. 1991: fig. 2.)

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larger groups. For the taxon that forms the sister to these two, it is only possible to make three statements; likewise for the taxon that is sister to these three only two statements are possible; and finally, only one statement is possible about the stem taxon (i.e., it can only be said of it that it is a member of the group of five taxa). The total number of statements that can be made about each terminal taxon is noted in column I (“Information”), and the total number of informative statements (fourteen in this example) is summed at the foot of this column. “Give a biologist two numbers and she/he will divide one into the other” is an old joke, but column Q (“Quotient”) of Figure 3.1 represents exactly that! The Q value given for each terminal represents the quotient for total I (fourteen in this example) divided by its own, specific value for I. In this example the Q values range from 3.5 (crown) to 14 (root). Column W (“Weight,” or “Root Weight”) simply represents these values standardized by dividing through by the smallest Q value (3.5 in this example). The total for the five root weights in column W adds up to (in this example) to 9.33, and the final column (P, or %) just gives the W values as a percentage of this total. Thus columns Q, W, and P (%) are all essentially the same. The P column gives the best sense of the relative contribution of each terminal taxon to the group as a whole, while W is the most practical formulation for diversity calculations based on this approach. What is the justification for this procedure? Such terminal scores or weights, based directly on an information measure of the hierarchic classification, have the type of properties we desire. Taxonomic equivalence (equal rank) results in the same score. Taxonomic distinctness results in a graded variation of score—not all species [terminal taxa] are equal. For unequal sister group pairs, the group with the higher number of terminal taxa will always have a higher aggregate score than the smaller group. Aggregated scores of (monophyletic) groups of species will thus depend on both [relative] rank and number.” (Vane-Wright et al. 1991: 239–240)

Thus the argument for this approach is that it was a coherent attempt to quantify taxonomic distinctness. As such it was a response to an idea already well articulated by conservation biologist Ian Atkinson: “Given two threatened taxa, one a species not closely related to other living species and the other a subspecies of an otherwise widespread and common species, it seems reasonable to give priority to the taxonomically distinct form” (Atkinson 1989: 66).

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Of course, in hindsight, this can be criticized as very simplistic. Whittaker (1972) had earlier suggested that no single measurement of diversity, because it is a product of evolution, can serve all purposes, noting at the same time that, however desirable it might be to include them, there were inherent difficulties in measuring such properties as organic complexity, intelligence, and phylogenetic relationships (as noted by VaneWright et al. 1991: 237). However, my purpose here is not to rehearse the complex and often confused arguments surrounding these issues, but to point out that something about “root weight” seems to have got lost in translation to phylogenetic diversity. One of the key things about the approach that Chris Humphries proposed, and out of which I suggest that PD developed, is that it is holistic—it is the totality of hierarchical relationships, and only that totality, that determines the weight, or relative value, to be accorded to each terminal taxon—and thus the potential relative contribution it can make to the conservation of biodiversity as a whole. In another sense, it can be said to be a top-down approach, in a way somewhat comparable to Løvtrup’s (1987) views on species and subspecies as terminal taxa. PD, however, is not holistic, in that branch lengths, and especially terminal branch lengths, are not obviously constrained by or related to the whole. In part at least, PD measures are bottom-up, influenced by autapomorphies, and thus phenetic. I personally believe this reflects a fundamental dichotomy in thinking about reality and our consequent approach to the scientific method—the same dichotomy explored by Olivier Rieppel at the very beginning of his much-neglected work, Fundamentals of Comparative Biology (Rieppel 1988: 3), as “Holism versus Atomism.” This, of course, reflects the familiar debate that continues in various ways to this day, as part of the old pattern versus process divide in systematics. At this point, however, it is necessary to remember that the root weight index was to be applied within the context of area selection algorithms that acted on notionally complete area × terminal-taxon matrices, using the complementarity principle as already noted—the latter now widely recognized as essential for efficient priority selection (e.g., Sarkar et al. 2006). As biological form determines the topology of a cladogram, which can be read as reflecting evolutionary time, in some rudimentary way form, space, and time were all satisfied. However, as Chris pointed out elsewhere (Humphries 2000), form and space are directly open to observation, whereas (evolutionary) time is always an

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inference (whether based on gene sequence data or not)—and this gives rise to a problem.

THE LABILITY PROBLEM

Given “reliable” knowledge of cladistic relationships, root weight works well. However, cladistic relationships, insofar as they can be interpreted as phyletic relationships through time, are an inference, as just discussed. These inferences of cladistic (or phylogenetic) relationship are partly based on knowledge of the distribution of organisms in space, and especially on their form (including DNA sequences). Change of form through time can be directly observed in ontogeny (Humphries 1988), but extrapolation of this knowledge to cladistic relationships is also an inference. It always struck me how vulnerable the root weight index is, because it is so dependent on cladogram topology. The relationship between character matrix and cladogram can be very labile, as the following simple example (based on Vane-Wright 2001) reminds us. Consider Table 3.1, which shows the distribution of four attributes (characters 1–4) across a sample of four taxa (A–D). A cladistic analysis of these data implies the hierarchical relationship D (C (A, B)); a phenetic analysis gives the arrangement (C, D) (A, B). However, the discovery of two more characters (5 and 6) that occur in C and D but not in A and B (Table 3.2) alters this outcome: both cladistic and phenetic analyses now agree that the correct topology is (C, D) (A, B). The critical, ambiguous element in all of this

matrix showing coincidences of four positive attributes (1–4) among four taxa (a–d)

TABLE 3.1.

Characters Taxa

1

2

3

4

A B C D

+ + – –

+ + – –

+ + – –

+ + + –

note: Based on Vane-Wright (2001, Table 3). Solid box indicates how character 4 is interpreted as a synapomorphy for (A + B + C). See text for further details.

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extended matrix showing coincidences of six positive attributes (1–6) among four taxa (a–d) (cf. table 3.1)

TABLE 3.2.

Characters Taxa

1

2

3

4

5

6

A B C D

+ + – –

+ + – –

+ + – –

+ + + –

– – + +

– – + +

note: Based on Vane-Wright (2001, Table 4). Solid boxes indicate how character 4 is now to be interpreted either as homoplasious or nonhomologous in taxon C (upper box) or as a loss-apomorphy in taxon D (lower box). See text for further details.

is character 4 (Tables 3.1 and 3.2). In the original four-character matrix we readily interpret attribute 4 as a synapomorphy for (A + B + C) (Table 3.1, enclosed in solid box); but, with the knowledge of additional characters 5 and 6, character 4 can be reinterpreted as a homoplasy in taxon C (nonhomologous with the similar character state observed in taxa A and B), or as a loss-apomorphy of taxon D (i.e., possession of character 4 is “really” a symplesiomorphy of the group as a whole that has been lost in D) (Table 3.2, where solid boxes indicate how character 4 can be interpreted either homoplasious or nonhomologous in taxon C [upper box] or a loss-apomorphy in taxon D [lower box]). The expectation of phenetics was that, as the number of characters added to the data matrix increased, analysis of the data would converge on a stable result—but this proved to be a forlorn hope. But arguably cladograms are at least as unstable in the face of additional data—be this in the form of new characters (as in the aforementioned example), the discovery of new taxa, or the elimination of so-called rogue taxa. All can have a dramatic effect on cladogram topology. These uncertainties seem attendant on all our attempts to derive wholes (e.g., cladograms) from parts (e.g., abstracted characters or attributes). In the example given earlier, the observations (measurements) for character 4 have not changed, but their qualitative interpretation has. Thus root weight measures are dependent on topology and risk being artifacts caused by the “fallacy of misplaced concreteness”—the error of mistaking the abstract for the real, of disregarding the actual connections between things (Whitehead 1925: 75, 77).

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Thus we typically use an imperfect sample of attributes to infer a cladogram, and then we behave as if that cladogram is real, not abstract, and finally propose to make conservation decisions based on numerics derived from that abstraction. “Simple as well as sophisticated methodologies for prioritizing conservation efforts and acquisitions . . . may produce conservation choices justified by numerical artifact rather than empirical evidence” (Wolman 2006: 1633—not that empiricism is beyond criticism; see Godfrey-Smith 2003: 227–30). Of course, the same is equally true for PD. Indeed, you could argue that it is even worse— from the same data set we infer both topology and branch lengths—to me rather like “having one’s cake and eating it, too.” After all, branch lengths only make sense if they are the lengths of branches, and the reality of the branches is entirely dependent on the topology. Is it really acceptable to use the data once to arrive at the topology, and then again to put lengths on the branches?

CHANGING MIND-SETS

Of course, all such criticisms need to be understood in the context of 1990, when the need to create an effective “calculus of biodiversity” felt very urgent. Quite apart from Robert May in Nature, and Lynda Chalker at ODA, Margaret Thatcher (1989) at the UN had just reminded us that “as we travel through space, as we pass one dead planet after another, we look back on our earth, a speck of life in an infinite void. It is life itself, incomparably precious, that distinguishes us from the other planets. It is life itself—human life, the innumerable species of our planet—that we wantonly destroy. It is life itself that we must battle to preserve.” In my view, our desire to maximize (phylo-)genetic diversity, or functional diversity, was based on human utilitarian value systems—not on an overt commitment to recognizing the intrinsic value of all living species (indeed, this was widely resisted by many, including numerous conservation professionals). Nor during the 1990s did we acknowledge Lovelock’s Gaia theory (e.g., Margulis 1999) as an overarching principle—that life on Earth is fundamentally synergistic (Corning 2005) and all interconnected (a holon, in the sense of Wilber 2000). Our approach, like most others at the time, was ultimately atomistic—even though it had the great merit of being systematic—and thus concerned with virtually the entire genetic hierarchy, running from expressed codons up to all known life on Earth (Eldredge and Salthe 1985).

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In retrospect, I submit that the whole PD enterprise as it became, important though it was and still is in some contexts, was reductionist. Even though most of us involved (I feel sure this applied to Chris as well as to myself) would have claimed distance from neo-Darwinists and the views of, for example, Richard Dawkins, we were essentially acting out of that same mindset. We were acting as if, by some bottom-up causation, “genes ruled the world”—a deterministic and mechanistic model that is no longer even biologically realistic, let alone philosophically attractive (e.g., Corning 2005; Walsh 2006; Midgley 2007; Goodwin 2007).

NEW REALITY OF CONSERVATION

However important the biology (and I accept that it is important, of course, for any chance of successful remedial action), the need for conservation is fundamentally an epiphenomenon of human culture, perspective, and activity. Why do we pollute our environment with litter and toxic chemicals? Why do we allow huge areas of wilderness to be converted into monocultures, the oceans and seabeds to be depleted and disrupted on epic scales, whole landscapes to be destroyed by mining? We might also ask why we allow one billion people, one-sixth of all humanity, to live in slums and be excluded from national and global economies (Davis 2007). This is, of course, the technology-based neoliberal economy that has driven so much of the dramatic change in human behavior and impact that has occurred since the industrial revolution, and has brought us to this, the sixth and possibly greatest of all extinction spasms to afflict life on Earth (Leakey and Lewin 1995). We can, of course, break down (I am tempted to say atomize) the causes of this global biodiversity catastrophe into such factors as climate change, poverty, overexploitation, wholesale “resource” conversion, pollution, habitat fragmentation, appropriation of net primary productivity and of fresh water, translocation of species and genes, massive population growth, urbanization, alienation, indifference to nature, and so on. But to do so risks laying the blame on some particular section of society, be it individuals, corporations, or governments, when the reality is that it is a collective failure—and very much a collective problem. In my view, it comes down, in the end, not to a technological problem or a technological fix (such as the conservation area networks that have long been the sticking-plaster response of professional conservationists, including the area selection technology to which Chris and I contributed) but to an ethical issue about

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our proper relationship to each other, to all other living things, and to the planet as a whole—in other words, to the relationship between worldviews (among which religions, whether we like it or not, are especially powerful), our understanding of life on Earth, and our emergent concepts of morality and environmental ethics—all of which, perhaps, could be summed up as “environmental philosophy” (Zimmerman et al. 2005). “Perhaps the best thing libertarians can [do] is put their dreams of changing the world on hold while they attempt simply to understand it” (Friedman 1992: 443). Or, as John Passmore (1995: 141) has put it, “The emergence of new moral attitudes to nature is bound up . . . with the emergence of a more realistic philosophy of nature.” All of this leads me to the conclusion that the beyond—the future of conservation—lies not in science because it can provide yet more technology to heal (and also destroy) the living planet, but in science because it is now the most powerful force in bringing to our attention and to our understanding what it is we are doing and what is at stake.

THREE GREAT REVOLUTIONS IN OUR PERSPECTIVE OF LIFE ON EARTH

As I have already presented the following in a number of places (e.g., Vane-Wright 2008, 2009a,b), I will not go into detail here. Suffice to say in this context that it is possible to identify three great revolutions in our scientific understanding of the Earth and our place in the cosmos: . The Copernican revolution (1543–present): the Earth is not at the center of universe (astronomy, physics, relativity, quantum theory, parallel universes). . The Darwinian revolution (1859–present): we (Homo sapiens) were not separately created (systematics, evolution, and genetics: all known life on this planet is interconnected back through time in an uninterrupted stream). . The Lovelockian revolution (1979–present): all Earth systems are self-organizing and interdependent, and our actions are consequential (systems ecology, involving networks, flows, nested systems, cycles, development, and dynamic equilibria). Of course, these giants built on the work of others before them. Nicolaus Copernicus was not the first to suggest that the Earth was not at

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the center of the solar system, Charles Darwin was not the first to have the idea of organic evolution (and was not even alone in proposing the mechanism of natural selection), and Jim Lovelock’s insights were built on fundamental ecological understandings and cybernetic concepts established by others before him—and the significance of these insights has been promulgated by numerous other major figures in science and culture (Isaac Newton, Albert Einstein, Rachel Carson, Ed Wilson, to mention but four). The point of picking on these “critical points” or landmarks that can be associated with Copernicus, Darwin, and Lovelock is simply to suggest that they represent cumulative shifts in our collective perspective, from humanity being set above or apart from the world to being simply an integral part of it, and they appear to herald a transformation in the way in which a growing number of people (not just scientists—that is very important) feel about Nature and our place within it. Here I will just note four quotations that express this emergent sense that is based on the growing collective understanding of earthly reality, and the implications of that understanding: . “We are aware that the earth was born and is borne by a delicate dynamic of forces which have converged to become the integrity of our planet. We are enchanted by the splendor of its life emergence, of which we are but a part” (Bassett et al. 2000: 7). . “In striving for harmony with nature, we need to seek not just a more physically secure and prosperous society, but one marked as well by moral and spiritual wellbeing” (Kellert 2008: 53). . “Environmentalism largely remains a reform movement committed to the assumption that the environmental crisis can be solved within the current political and economic system, without challenging underlying values or questioning contemporary life styles” (Leiserowitz and Fernandez 2008: 28). . “To the Okanagan people, as to all peoples practicing bioregional self-sufficient economies, the realization that the total community must be engaged in order to attain sustainability comes as a result of surviving together for thousands of years” (Armstrong 2005: 12). The fourth quotation also reminds us that, in our race to apply the fruits of science to our technologically driven neoliberal world economy, we have also lost or thrown away enormous wisdom that, had

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our arrogance not been so great, we would have given more respect and thought. We need to reconnect with the living Earth—to become “ecologically literate” (Stone and Barlow 2005).

CONCLUSION

So, what lies beyond cladistics when it comes to conservation? Perhaps faith in the notion that the huge understanding that systematics has given us, of which cladistics has been only a recent but now very important part, laid the foundation for the second of the three great scientific revolutions: Darwin and Wallace would not have got very far if Linnaeus and his followers had not already brought “order out of chaos” (Jarvis 2007). However, we must not allow our old “pattern versus process” debate, so wisely seen by Rieppel (1988) as complementary ways of seeing rather than fundamentally different paradigms in conflict, to blind us from the crucial importance of systems theory and systems ecology for understanding how our planet actually works. Finally, insofar as all three scientific revolutions continue to grow and advance, what lies beyond cladistics is surely more cladistics—and whatever cladistics becomes as part of the great movement of evolutionary biology and evolutionary thinking. But in that ongoing process, we should do all we can to resist the libertarian call that our work be justified only by serving utilitarian, wealth-generating, and technological ends. We need to regain confidence in our contribution to science, and in science as a whole as one of the four cornerstones of “The Fourfold Wisdom” needed for the future (Berry 1999): indigenous wisdom, the wisdom of women, the wisdom of classical traditions, and the wisdom of science—including the need to know and understand “the story of the universe” (Swimme and Berry 1992), and where cladistics has its own special part to play. Chris Humphries summed up the particular contribution to conservation biology with which he is most closely associated with these words: An examination of the currency of conservation—which we believe basically is best seen as the characters of organisms—has allowed us to put together a surrogacy scheme that can satisfy the usual requirements of NGOs of representing genetic, specific and ecosystem levels of measurement. Indeed our efforts have tried to bring together the entire broad range of surrogates into a single scheme that can form the basis of new developments in the future. (Humphries 2006, p. 159)

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While it is clear from the first part of this chapter that I personally no longer entirely agree with this statement, Chris’s contributions to conservation have to be placed in a context that has seen the focus shift, in just a few decades, and as all too summarily treated in the second half of this chapter, from atomism and anthropocentrism, via representational and phylogenetic goals, to an increasingly integrated ecocentric approach to sustaining planetary biodiversity. These changes have been paralleled, in seeking a rational basis for developing a viable human–Earth relationship, by shifts in perception from reductionism to holism. Conservation biology has, in the process, moved from being the preoccupation of self-selecting elites to an increasingly vital concern for all people. It is now going beyond science and conventional economics as it enters what may best be described as a cultural phase, in which the motivational values that guide human action (Schwartz 1994), and the ways in which they can potentially evolve (Dietz et al. 2005) and appear to be changing (O’Dea 2007), can play and will play an increasingly important role. We really need to understand the world before having the audacity to change it; and once we understand it, if we ever do, maybe our desire to alter it will be gone. That, of course, is not a prescription for inactivity— but whatever activity we do engage in needs to be informed by many things, not least the precautionary principle, and the realization that our current knowledge is incomplete, insecure, and very uncertain. One thing I can be sure of, however, is that as an avid and fearless seeker after truth, Chris Humphries has not only been a great contributor to the progress of science, but his work will also be part of the foundation for whatever lies “beyond cladistics.” Acknowledgments

I am most grateful to Sandy Knapp and David Williams for the invitation to take part in the original celebration of Chris Humphries’s work. I have greatly benefited from David’s input to the editorial process. I am thankful that the two anonymous reviewers clearly recognized that this contribution is a mixture of reminiscence and “a personal perspective rather than a thorough scientific discussion.” Indeed it is so. Finally, I wish to thank my old buddy Chris for his remarkable engagement in the work that we did together, and his great passion for systematics, biogeography, and conservation biology. He was and is an inspiration. He also had a wonderful ear for good music.

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FOUR

Q u e n t i n D. W h e e l e r

DO WE NEED TO DESCRIBE, NAME, AND CLASSIFY ALL SPECIES?

All science is either physics or stamp collecting. Ernest Rutherford

Rutherford was more candid about his bias than most experimental biologists are in sharing their view of taxonomy (see quotation). To the outsider, taxonomy may look a bit like philately. We do want to collect every species, but the similarity stops there. Our motive is to explore unique characters and all their subsequent modifications through evolutionary history (Platnick 1979), to determine what they mean in terms of species, relative recency of common ancestry among species, and as the basis for informative and predictive classifications. This is achieved through painstaking comparative studies and analyses of patterns of distributions of characters and through the creation and critical testing of hypotheses on many levels, from homologues to synapomorphies, clades, and geographic distributions. These hypotheses are almost invariably more rigorous than experiments. The fact that the outcome of most experiments can be any of a universe of possible outcomes means that we must resort to statistics to determine whether our results are significant. For the vast majority of Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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hypotheses in taxonomy, the predicted outcomes are precise and clear. In the frame of reference described by Karl Popper (1959), taxonomic hypotheses are all-or-nothing claims about the world. No claims are more vulnerable to refutation than such statements. All insects have six legs. All Rosaceae have flowers with five petals. All populations of this species share a specified and unique combination of characters. All species of that clade share the following synapomorphies. All species of Nothofagus occur in the Southern hemisphere. In each case, our observations of hundreds or thousands of specimens have revealed a pattern that we now generalize as an all-or-nothing prediction. As new specimens are seen and characters newly discovered, each is an opportunity to test the prediction. These tests are so severe that a single observation can refute the hypothesis (Gaffney 1979). One eight-legged butterfly, one leech with a vertebral column, one Nothofagus in Canada, and no statistical test is needed to reject the hypothesis. Ecosystem scientists can measure the capacity of frozen tundra as a carbon sink without knowing or caring what species of mosses or lichens are growing on the rocks or what species of microbes are living in the soil. Many laboratory experimentalists need to minimize variations and so focus on one or a few model organisms and feel no need for the ability to identify species in the field, even those closely related to the model species. Conservation biologists and land managers overseeing a large national park are winning and losing battles to stave off poachers and keep development at bay around the perimeter of the park and do not see a great need to have a complete inventory of the species in the park to succeed at either. Agriculturalists primarily work with a handful of crop species and a known and limited set of primary pest species for each of those crops and thus may have a narrow interest in biodiversity. Convincing the world of the fact of evolution in the latter half of the nineteenth century was a beginning, not an end. From that beginning we set out to unravel the mysteries of inheritance, gene expression, and selection right down to the molecular level. Similarly, we have begun to reconstruct the origin and diversification of species and characters that are the evidence for understanding evolutionary history. For centuries no one questioned the importance of taxonomy. It was as self-evidently important to explore the world’s species as it was to map its continents and ocean floors, chart the stars of the Milky Way, or probe the structure of atoms. Somehow, simply knowing that evolution

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was responsible for species massively shifted funds and attention to mechanisms of microevolution and away from studying the results of evolution itself. This is bizarre. Believing that the Universe arose from the Big Bang did not deter exploration of galaxies; knowing there were seven continents did not retard our exploration of the four corners of those landmasses; and realizing that atoms are comprised of particles did not discourage physicists from continuing to enumerate and discover these particles and their properties. Descriptive science remains revered and funded in most fields of science (Grimaldi and Engel 1997). Only taxonomy is seemingly singled out. Maybe it is because all other biologists depend on taxonomy for identifications of species, names, and classifications, and therefore have come to look on it as a service rather than respect it as a science. Only disrespecting taxonomy could lead anyone to ask whether we need to discover, describe, and name species. Species exploration can appear from the outside to be a largely onetime activity. You discover a new species; and if you do a reasonably good job describing it, then the taxonomy is more or less complete, and we can turn our attention to other biological pursuits. Not so. Discovering and describing a species is also a beginning, not an end. Every specimen collected in the future may be compared to known specimens to test and corroborate or reject its status as a species; and every newly found character, whether molecular, fossil, developmental, or morphological, is another test. There is a perennial suggestion from users of taxonomic information that we not bother with formal descriptions and Latinized names, that we could make ever so much more headway by simply sorting out the species, calling them by some numeric or arbitrary label—most recently and creatively using their DNA barcode as a unique identifier in place of a name. This approach sounds good, but whether it is a viable alternative to descriptive taxonomy depends in part on how far you are willing to lower your standards and whether you want the species in your study to be based on science—that is, founded on testable hypotheses. To credibly sort out the number of species, one must do the kind of careful comparative work that has always characterized taxonomy. This is the hard and time-consuming part. Once relevant characters have been compared across hundreds or thousands of specimens, the actual writing of a description and assigning a name are relatively trivial. Not to record the information that supports the hypothesis of species status or not supply a name so that data can be reliably tracked, analyzed, and

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communicated is irresponsible and short-sighted; to settle for fast and dirty guesses at species in the place of rigorously testable hypotheses is just sloppy and bad science. As pointed out by Will et al. (2005), the part of DNA barcoding that is useful is not new and the part that is new is not useful. DNA barcoding has a limited but important role to play as an identification tool. Objective empirical evidence so far suggests that it is useful when a DNA library of known species exists, and even then it is no more reliable than traditional identification methods (see Little and Stevenson 2007). Among the exciting applications, however, are rapid associations of semaphoronts to open new sources of morphological data (see Miller et al. 2005), the ability to identify fragments of specimens of endangered species being trafficked across borders, and the ability to verify products derived from species are what they are sold as such as seafood in a fish market. The most serious shortcoming is the way in which DNA barcoding treats species as arbitrary (Prendini 2005). The way species are defined as an arbitrary or average genetic distance is philosophically nothing more than a rehash of the failed phenetics paradigm of the 1970s, and the new “species” discovered are not testable hypotheses and therefore are not strictly scientific (Wheeler 2005). Even if DNA barcodes did allow us to identify all species, we would know nothing more about them than their identities; it is “taxonomy” as a service, not a science. Some of the vocal nontaxonomist advocates of DNA barcodes and classifications seem not to understand that studying morphology is a worthy end in itself and was not used for centuries only because we did not yet have access to DNA (Wheeler 2007). Taxonomy is about much more than identifications and names, but DNA barcoding is not. As Richard Feynman said, “I learned very early the difference between knowing the name of something and knowing something.” Unless we are carefully analyzing characters and recording natural history information, then even accurate identifications are of limited value. The prospect of having access to a handheld DNA barcoding device gets its proponents starry eyed, but such “barcoders” will no more make their users taxonomists than a pocket calculator makes an elementary school child a mathematician. One argument from conservation biologists is that we should focus our resources on saving species and only worry about describing and naming them later. I would find this argument more compelling were I more optimistic. I find it inconceivable that thousands if not millions of species will not go extinct before the end of this century. It is thus a

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“now or never” proposition to chart the species of the biosphere relatively completely. In reality, we need to make tough choices and set priorities, and we can only do so intelligently if we have a foundation of taxonomic information to work from. Many experimental biologists conclude that if they cannot access live specimens of species to experiment on, why should they care that they are ever known, described, or named? The same biologists find it fashionable to point to phylogenetic “trees” (overlooking for the moment that most are at best phenograms and not cladograms, much less phylogenetic trees: see Nelson and Platnick 1981 for relevant definitions). The same phylogenetic context they espouse as important is enriched, tested, and improved by including as many species and characters as possible. Phylogeneticists (and even molecular pheneticists) can benefit for generations to come by having access to extinct species that are members of clades that become of interest. And ecologists should be interested in documentation of the species diversity that existed before the great environmental changes of the new century. That these arguments have to be made to fellow biologists is most depressing. As Enrico Fermi put it: “Ignorance is never better than knowledge.” I do not need or seek the approval of experimental biologists any more than they need or seek mine, and I offer these reasons to support species exploration for their consideration in their own selfinterest. To me the most powerful reasons lie within taxonomy itself. Taxonomists ask some of the most basic, important, and interesting questions about biological diversity (see Cracraft 2002): What are species? What species exist? What is the history of the origin and transformation of their characters? What are their phylogenetic relationships? What are their distributions? And how are they predictively and most informatively classified? The arrogance of ignorance among some ecologists is simply stunning. To openly argue that ignorance of what unique combination of species comprises some complex ecosystem is preferable to credible taxonomic knowledge is intellectually indefensible, yet this attitude has been surprisingly widespread in the ecological community for decades. Clearly we can make the best public policy decisions when they are informed by science, including taxonomy—and we have not yet discussed the phylogenetic measures that can contribute to logical conservation prioritization (e.g., Vane-Wright et al. 1991; Nixon and Wheeler 1992). Fundamental science has always been admired for its purity. John Ray concluded that species exist because he observed distinct kinds with distinct combinations of characters that produced more of like kind.

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Carl Linnaeus described the many kinds of plants and animals around him because they were there. Richard Owen marveled at bones because of the correspondence of homologous parts in spite of structural differences. Charles Darwin theorized natural selection because species and their unique patterns of characters were so evident that they demanded an explanation. Willi Hennig made good on Darwin’s promise that classifications would become genealogies because of his deep curiosity about biodiversity and its history. Exploring the origin and diversification of the millions of kinds of living organisms on the face of a planet and reconstructing the histories of the origins and diversification of all their billions of characters and charting their distributions through time and in geographic and ecological space is big science, is deeply intellectually challenging to do, and is equally deeply rewarding when done. That this grand science should have to justify itself before a few trivial experiments and model organisms is absurd and points out that the neglect of taxonomy and of collections has far more to do with politics and sociology than it has with science (Wheeler 1995, 2004, 2008). We need to describe, name, and classify species because they are there. We need to do so because we belong to one of them and are innately curious about our roots. We need to do so because we are curious about the pattern of similarities and differences among kinds of living things, a puzzle that is well worth our effort to solve in order to reveal the wondrous story of the evolution of life on Earth. We need to inventory species and grow and develop our museums and herbaria because we are the last generation with the capacity to do so to a reasonable level of comprehensiveness. We need to name species so that we enrich the vocabulary with which we can store and retrieve observations about millions of species and communicate to one another and across generations to reach yet unborn curious colleagues. We need to describe and name species to establish a basis of comparison against which we can detect introductions of nonnative species, declines or increases in local species diversity, successes and failures of conservation, impacts of changes in global climate, and suspected rapid changes in worldwide ecosystems. We need to chart the world’s species and make them known to recharge the reservoir of fundamental knowledge of biodiversity from which biochemicals, materials, designs, medicines, crops, fibers, foods, and countless other goods that contribute to the well-being of humans may be derived. We need to describe and name and classify species because we are an intelligent, curious species that will never set foot on another planet with comparable evidence of billions of years of

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evolution. We are ethical beings and should feel a responsibility to future generations to explore and document life on Earth. We explore species because they are there and can teach us much of the history of our world. We are at a pivotal point in the history of taxonomy. Phylogenetic theory and analysis, pioneered specifically for taxonomy so that classifications could serve as a general reference system (Hennig 1966), have been hijacked to provide stick figures for biologists with little knowledge or appreciation of the history, epistemology, or potential of taxonomy and with utter disdain for classification and nomenclature (see a rebuttal of Felsenstein’s arguments by Franz 2005). And now efforts are afoot to similarly derail species level taxonomy by turning to one data source rather than integrating and synthesizing all relevant sources of evidence. Nelson (2004) has pointed out an eerie similarity between the status of molecular data today and fossil data in the early twentieth century. Fossils were once thought to reveal phylogeny through the stratigraphic appearance of species in the record. Today molecules are treated as if they reveal phylogeny when they, like fossils, are simply data. It is time that we revive the Hennigian revolution, return our focus to the study of characters, and rejoin one of the most audacious life science projects ever conceived, the exploration of all species. In the works of Professor Humphries, we can see many of the most compelling reasons to do taxonomy. Chris has made superb descriptive taxonomic and anatomical contributions, advanced the theories needed to analyze characters and complete cladistic analyses, proposed innovative tools to use evolutionary history to set conservation priorities, transformed historical biogeography, and served as a constant source of support and encouragement to his colleagues and generations of students. His works are a testament to the excitement and rewards of a life in taxonomy, and I have no doubt that bright young scientists in many generations to come will challenge themselves to follow in his footsteps. I have always found meaning in working for something bigger than myself. Sir Isaac Newton famously said that had if he had seen farther, it was because he had stood on the shoulders of giants. No science more consistently reminds its students of this fact than taxonomy. The rules of nomenclature make it very evident that each generation receives a body of taxonomic work and has the challenge to pass it on to the next generation expanded and improved. Chris has done so impressively not only in various angiosperm groups but also in taxonomic theory. Great scientific vistas will be seen from his shoulders by generations of botanists and cladists to come.

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Acknowledgments

I thank David Williams and Sandra Knapp for their kind invitation to participate in this Festschrift for my dear friend and colleague Chris Humphries. My talk at the symposium was an exploration of quotations and lyrics from jazz musicians and a (loose) interpretation of what they teach us about taxonomy. This was an effort at fusion of two of Chris’s passions: plant taxonomy and jazz music. It was a stretch as a talk and would have been incomprehensible as a paper. So I mercifully abandoned the effort. I thank also the other speakers and the audience at the symposium, which was stimulating, edifying, and thoroughly enjoyable—which is precisely how I would characterize the many years I have known and admired Professor Humphries.

REFERENCES Cracraft J. 2002. The seven great questions of systematic biology: An essential foundation for conservation and the sustainable use of biodiversity. Ann. Missouri Bot. Gard. 89: 127–144. Franz N. 2005. On the lack of good scientific reasons for the growing phylogeny/ classification gap. Cladistics 21: 495–500. Gaffney E. 1979. An introduction to the logic of phylogeny reconstruction. In: Cracraft J., Eldredge N., editors. Phylogenetic analysis and paleontology. New York: Columbia University Press pp. 79–111. Grimaldi D.A., Engel M.S. 2007. Why descriptive science still matters. BioScience 57: 646–647. Hennig W. 1966. Phylogenetic systematics. Urbana: University of Illinois Press. Little D.P., Stevenson D.W. 2007. A comparison of algorithms for identification of specimens using DNA barcodes: Examples from gymnosperms. Cladistics 23: 1–21. Miller K.B., Alarie Y., Wolfe G.W., Whiting M.F. 2005. Association of insect life stages using DNA sequences: the larvae of Philodytes umbrinus (Motschulsky) (Coleoptera: Dytiscidae). Syst. Entomol. 30: 499–509. Nelson G. 2004. Cladistics: Its arrested development. In: Williams D.M., Forey P.L., editors. Milestones in systematics. Boca Raton: CRC Press pp. 127–147. Nelson G., Platnick N. 1981. Systematics and biogeography: Cladistics and vicariance. New York: Columbia University Press. Nixon K.C., Wheeler Q.D. 1992. Measures of phylogenetic diversity. In: Novacek M.J., Wheeler Q.D., editors. Extinction and phylogeny. New York: Columbia University Press pp. 216–234. Platnick N.I. 1979. Philosophy and the transformation of cladistics. Syst. Zool. 28: 537–546.

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Popper K. 1959. The logic of scientific discovery. New York: Basic Books. Prendini L. 2005. Comments on “Identifying spiders through DNA barcodes.” Canad. J. Zool. 83: 498–504. Wheeler Q.D. 1995. The “Old Systematics”: Classification and phylogeny. In: Pakaluk J., Slipinski A.S., editors. Biology, phylogeny and classification of Coleoptera. Warsaw: Muzeum i Instytut Zoologii PAN pp. 31–62. Wheeler Q.D. 2004. Taxonomic triage and the poverty of phylogeny. Phil. Trans. R. Soc. Lond., B 359: 571–583. Wheeler Q.D. 2005. Losing the plot: DNA “barcoding” and taxonomy. Cladistics 21: 405–407. Wheeler Q.D. 2007. Undisciplined thinking: Morphology and Hennig’s unfinished revolution. Syst. Entomol. 33: 2–7. Wheeler Q.D. 2008. Introductory: Toward the new taxonomy. In: Wheeler Q.D., editor. The new taxonomy. Boca Raton, FL: CRC Press pp. 1–17. Will K.W., Mishler B.D., Wheeler Q.D. 2005. The perils of DNA barcoding and the need for integrative taxonomy. Syst. Biol. 54:844–851. Vane-Wright R.I., Humphries C.J., Williams P.H. 1991. What to protect? Systematics and the agony of choice. Biol. Conservation 55: 235–254.

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FIVE

Sandra Knapp and J. Rober t Press

FLORAS TO PHYLOGENIES Why Descriptive Taxonomy Matters

The centrality of taxonomy (or systematics; we will here use these two terms as synonymous) to the study of diversity is often taken for granted, but the decline in the discipline decline has been highlighted through various reports (House of Lords 1992, 2002, 2008) and funding initiatives (such as the U.S. National Science Foundation’s Partnerships for Enhancing Expertise in Taxonomy [PEET]—see Rodman and Cody 2003; and the Planetary Biodiversity Inventory Program [PBI]—see Wheeler 2004, Page 2008; the UK’s BBSRC Co-Syst program—see http://www.linnean. org/co-syst). The field of taxonomy appears to be entering a time of unprecedented change and perhaps renovation (Godfray and Knapp 2004), but what needs change, how that change can be affected, and just what sort of taxonomy we might need for the future are still under discussion (e.g., European Distributed Institute of Taxonomy [EDIT] 2007). If the field of taxonomy can be characterized as interlocking spheres of endeavor, we can divide it in many different ways—a report charting the science assembled by the community in the mid-1990s (see Anonymous 1991) suggested that the tasks of “systematics” could be seen as three central “missions”: (1) “survey, discover, inventory and describe global species diversity accurately, efficiently, and rapidly; (2) analyze

Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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and synthesize the information derived from this global discovery effort into a predictive classification system that reflects the history of life; and (3) organize the information derived from this global program in an efficiently retrievable form that best meets the needs of science and society (Systematics Agenda 2000). Put more simply, Systematics Agenda 2000 laid out a set of priorities where species were catalogued, the tree of life was constructed, and the resulting information was made accessible in many ways. Taxonomy has also been characterized as description, phylogeny, and identification (Knapp 2008a). Description is central to most visions of what the science of taxonomy should be, but the importance and prominence of descriptive taxonomy as an enterprise has been in sharp decline, particularly relative to the advances made in phylogenetics with the adoption of molecular techniques (Wheeler 2004, 2008). Moreover, most current summaries of what taxonomy needs to best enter into the twenty-first century are largely limited to synopsis or inventory—the naming and listing of species of organisms. Logically extended, this definition of descriptive taxonomy suggests that the role of description is to give names to the terminals in a cladogram or tree, and principally to allow communication about the entities we designate as worth naming in nature. In this conception, description is the same as naming and listing. This view owes much to the erroneous characterization of the discipline as “essentialist” and “typological” (Winsor 2006); which has contributed to the narrowing of our appreciation of what taxonomy can contribute to the rest of biology. Much discussion and effort have recently been put into the provision of names lists (see Godfray 2002; EDIT 2007; papers in Wheeler 2008) for use in assessment and monitoring. Global databases such as the Global Biodiversity Information Facility (GBIF, www.gbif.org), Integrated Taxonomic Information System (ITIS, www.itis.gov), and Catalogue of Life (www. catalogueoflife.org) all provide names lists with minimal descriptive information. Names lists, especially rigorously synonymized ones, are of course essential for counting exercises and for establishing the scale of the numerical diversity of life on Earth. Less discussion has centered on the importance of the provision of comparable descriptive information about species and its future utility for organismal science, although some taxon based databases are working toward this goal (see Creating a Taxonomic E-Science [CATE], www.cate-project.org; Solanaceae Source, www.solanaceaesource.org). The recently established Encyclopedia of Life (www.eol.org) where names lists will be reinforced by the addition of a wide variety of content is a step toward the provision of

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more descriptive information online, but much of the discussion as to what constitutes “descriptive taxonomy” still centers on the provision, on paper or electronically, of names and lists. We would contend that description is more than naming; descriptive taxonomy needs to be seen as more than the “mere” naming of species. A good taxonomic description is just that, a description of the organism— what it looks like, where it lives, sometimes even the base sequence of portions of its DNA. The characters used in both phylogeny and identification are part of a description and are every bit as important as the name itself. In fact, the name is really just a shorthand way of accessing the information contained in the description itself, just as a person’s name is easier to use than repeating a physical description each time one wants to refer to an individual. Description can be thought of as the Cinderella of taxonomy because it is largely invisible but critical to the functioning of both phylogenetics and identification—thought by some to be more obviously practical, the other components of the taxonomic whole (Knapp 2008b). Without it, however, the rest would collapse—how can you construct a phylogeny without knowing what you are constructing a phylogeny of, or how can you identify an organism without its having an identity and way to recognize it in the first place? Any decision as to the specific or other taxonomic status of an organism is an hypothesis (Wheeler 2004; Knapp 2008a, 2008b), subject to test using new data or new interpretation of data. Taxonomic practice in botany involves setting the boundaries for that hypothesis, typically by consulting specimens for a variety of characters (morphological and molecular), then assigning a name by applying the rules as laid down in the International Code of Botanical Nomenclature (McNeill et al. 2006), and finally the preparation of a synthetic description taking into account variation across the set of objects (specimens) hypothesized to be included in the species. Models of how this process works have been developed with the intention of capturing taxon concept circumscription and automating description generation (Pullan et al. 2000, 2005), but the sheer scale of data entry required may make these impractical in the near term (Berendsohn 1995). In the context of the future of cladistics, descriptive taxonomy takes on a new importance and relevance as the evidence on which reciprocal illumination is based. Hennig’s (1966) concept of reciprocal illumination is often not articulated, but it has become (or should have become!) the background wallpaper against which all hypotheses of relationships, whether based on molecules or morphology, are assessed. Reciprocal

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illumination has been characterized as the reevaluation of characters (= homology assessments; see later discussion) in order to minimize character conflict (Hawkins 2000) and has generally been seen in the context of matrix development or manipulation through such methods as character weighting or transformation series analysis (Siebert 1992; Patterson and Johnson 1997; but see Rudall 2000). Coding of characters has long been of interest to those undertaking analysis using morphological data (Stevens 2000), but it is arguably less problematic when using DNA sequence data in phylogeny reconstruction. Since the advent of widespread use of DNA sequence data in phylogenetic reconstruction, the idea of reciprocal illumination and character reevaluation has become less prominent. This is based on the truism that the character states themselves are unambiguous (the bases are A, G, C, or T—no overlap exists) and that no intermediate states exist (Brower and Schawarach 1996; Brower 2000), but that the characters (i.e., the positions in the alignment) can be problematic to align (i.e., to infer their homology) (Stevens 2000). Reciprocal illumination, however, is just as applicable with molecular data as with morphological, as alignments, which can be thought of as the characters (Stevens 2000) or homology assessments using sequence data, are subject to error and/or misinterpretation. It is not our purpose here to evaluate the perils and pitfalls of homology assessment or to compare molecular with morphological data (see Wortley and Scotland 2006 for an analysis), but instead to explore some of the reasons descriptive taxonomy is critically important for both the generation and evaluation of further data on the biology of organisms. We here use the term description to mean a synthetic word picture of an organism, encompassing morphological characteristics drawn from specimens, both living and preserved. The body of work from which we draw our ideas is the botanical tradition of floristics and monography, but the description as an essential building block for future hypothesis development is applicable in many groups of organisms.

FLORAS AND MONOGRAPHS

Plants play a fundamental role in all ecosystems; thus their characterization and identification have long been of interest. Other biologists often need to identify plants in order to describe the habitats in which their particular organisms operate; to facilitate these sorts of tasks, botanists

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have long written descriptive guides to the plants of particular places (Knapp 2008a). What distinguishes such descriptive guides, floras, from mere names lists are keys for identification and descriptions with which to compare specimens. Floristics has a long history in botany, beginning with the herbals (Arber 1912). Linnaeus (1751) in Philosophia Botanica said a flora was “the vegetation growing naturally in one place.” Floristics can be distinguished from monography (but see later discussion) by being place, rather than taxon, focused. The flora as identification guide was developed first by Lamarck in his landmark Flore françoise (1779) in which dichotomous keys and French language descriptions were provided for all known French plants, allowing a wide variety of people to learn about plants (Scharf 2009). Later editions (Candolle 1805) were sophisticated developments of explicitly artificial systems aimed at facilitating identification, rather than natural systems aiming to describe relationships (Scharf 2009). Throughout the nineteenth and twentieth centuries, botanists have documented the floras of regions of the globe, often taking many decades (see Knapp 2008b) and causing taxonomic problems when regions treated were small and global views not taken (Knapp et al. 2001). Since floras are usually explicitly about facilitating identification and not about the phylogenetic relationships of plants, they are sometimes seen as less “scientific” or less rigorous than taxon-based monographs (Grimes 1998). Carefully researched floristic accounts, however, can approach a monograph in scope and quality, and blur the somewhat artificial (if not completely absent!) dividing line between floras and monographs (Maxted 1992). A flora is a multipurpose tool and can be considered the baseline for understanding national, regional, and local plant diversity. Monographs are traditionally defined as taxonomic (systematic) works presenting global coverage of a particular (monophyletic) plant group. Relationships among the members of the treated group are generally considered a cornerstone of a monograph, and this focus on a “natural” rather than “artificial” system of classification (see Scharf 2009) has led some (Grimes 1998) to suggest that regional treatments of plant groups are premature before a complete phylogenetic understanding is achieved. Grimes (1998) suggests that monographs more correctly delineate species than do floras and in addition provide a phylogenetic scaffolding on which other hypotheses can be hung. Others (Funk 1993) have argued that floras can be effectively used to construct phylogenetic hypotheses for use in a wide range of disciplines, and that the time necessary to complete in-depth monographic treatments of all plant groups is just not

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available to us in the current situation (Knapp et al. 2001; EDIT 2007). Regardless of whether one feels monography or floristics should take priority (we feel both have an important role to play), both these types of work share a core of descriptions—word pictures of the plants being treated. A monograph is not just a phylogenetic tree or a cladogram, just as a flora is not just a list of the names of the plants growing in a particular region. The descriptive core of both monographs and floras is composed of a series of parallel descriptions of the summary morphology of each species, with all characters considered measured and provided. Floras usually have shorter, less exhaustive descriptions than do monographic works (compare, e.g., the treatment of Lavandula in Flora Europaea [Guinea 1972] with that in the monograph by Upson and Andrews [2004], or the treatment of Argyranthemum by Press [1994] with that of Humphries [1976]). The creation of parallel descriptions, in which each has all characters, has its roots in the search for the “true” natural classification; in the eighteenth century, Michel Adanson considered the totality of compared descriptions critical for determining the “natural order” (Winsor 2004). This, of course, depends on descriptions being completely comparable. Characters are only of use in either phylogeny or identification if they are compared (Rieppel 2004), thus making the parallel nature of descriptions essential for their subsequent use in any new analysis. Ultimately it is the objects themselves that possess characters, and if all specimens were accurately databased with all features measured (perhaps a reality in the not so distant future, see Wheeler 2008), then we would be able to generate synthetic descriptions from a set of specimens ad hoc (see Pullan et al. 2005). The online databases, specimen images, and character measurements represent the primary data from floristics and monography, and they are the raw materials for the descriptive element, but they currently do not replace it completely.

WHY DESCRIPTIVE TAXONOMY MATTERS

Hypotheses generated from taxonomy are critical to many other fields in biology (Godfray 2002; Gotelli 2004; Mace 2004). Phylogenetic trees are often taken as the most important product needed for other biologists, but a tree not well rooted in the organisms is alone not really the basis for future exploration of the evolutionary process. Keys are critical

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for identification; Gotelli (2004) cites them as the single most useful taxonomic product for macroecologists, more important even than robust phylogenetic hypotheses. Keys alone, however, often only use a few of the many characters—those useful for identification—and can sometimes serve to confuse or mislead if a more complete word picture (description) of the organism is not provided as a backup (see Alcock 2009). Both keys and phylogenetic trees (via the terminals used and their previous identification) stand on the foundation of a good morphological characterization of taxa; a synthetic description is a check, but as a summary of the variation within a given taxon, it can also be revisited and reevaluated. Descriptions can be used to generate data sets for cladistic analysis (Funk 1993), but their real value lies in their actual preparation. By preparing a morphological description via examining specimens, a botanist is forced to examine the organism carefully and compare it with relevant taxa previously described. Wortley and Scotland (2006) have shown that morphological character sets are often of equal utility (measured as number of parsimony–informative character–state changes) as much larger molecular data sets, and they suggest that molecular data sets alone are not necessarily the most useful for reconstructing robust trees. A morphological data set, while smaller, can often have more utility than the number of characters might suggest. Choice of characters is important, and morphological data sets are smaller in general due to this choice. Choosing the morphological characters to include is the equivalent of a priori character weighting (see Wägele 2004), and the production of parallel descriptions allows others to test the hypotheses of homology that these characters represent through reciprocal illumination. Homology is the way in which to understand organisms, not just name them, and leads to further hypotheses about relationships, function and process. Descriptive taxonomy should be seen as the foundation for new ideas and views on how the world works (Winsor 2009). Charles Darwin, at the same time as beginning his species notebooks and articulating his ideas about evolution by natural selection, began an in-depth taxonomic study of barnacles (Darwin 1851, 1854) in order to better understand characters and how they were distributed. His time spent on barnacles (1846–1854) allowed him to see in detail how characters relate to one another (homology), and these data certainly influenced his conception of life as interconnected through branching evolution (Winsor 2009). His descriptions of the whole organism—the phenotype—in the barnacle monographs allowed others to assess his ideas of character identification

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and relationships; this information, including his keys, is still in use today. Descriptive taxonomy is far from being a sterile production of lists of names and species, but it should instead be seen as the crucible in which new ideas about taxa and their relationships are generated using the Hennigian principle of reciprocal illumination.

Acknowledgments

Our ideas in this contribution come from discussions over many years not only with Chris but also with other colleagues at the Natural History Museum, London, and elsewhere. A Planetary Biodiversity Inventory award from the National Science Foundation (DEB-0316614, “Solanum: A Worldwide Treatment”) supports S.K.’s monographic work, and J.R.P. is supported by KeyToNature (eContentplus program of the European Commission, ECP-2006-EDU-41001).

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Systematics Agenda 2000. 1994. Systematics Agenda 2000: Charting the biosphere. Technical Report. Society of Systematic Biologists, American Society of Plant Taxonomists, Willi Hennig Society, Association of Systematics Collections, New York. Upson T., Andrews S. 2004. The genus Lavandula. Richmond, U.K.: Royal Botanic Gardens, Kew. Wägele, J.-W. 2004. Hennig’s phylogenetics systematics brought up to date. In: Williams D.M., Forey P.L., editors. Milestones in systematics. Systematics Association Special Volume 67. Boca Raton, FL: CRC Press pp. 101–125. Wheeler, Q. 2004. Taxonomic triage and the poverty of phylogeny. Philos. Trans. R. Soc. Lond., B 359: 571–583. Wheeler Q. 2008. Introductory. In: Wheeler Q., editor. The new taxonomy Systematics Association Special Volume 76. Boca Raton: CRC Press pp. 1–18. Winsor M.P. 2004. Setting up milestones: Sneath on Adanson and Mayr on Darwin. In: Williams D.M., Forey P.L., editors. Milestones in systematics. Systematics Association Special Volume 67. Boca Raton, FL: CRC Press pp. 1–17. Winsor M.P. 2006. The creation of the essentialism story: An exercise in metahistory. Hist. Philosoph. Life Sci. 28: 149–174. Winsor M.P. 2009. Taxonomy was the foundation of Darwin’s evolution. Taxon 58: 1–7. Wortley A.H., Scotland R.W. 2006. Determining the potential utility of datasets for phylogeny reconstruction. Taxon 55: 431–442.

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PA R T T W O

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SIX

David Bramwell

ISLAND HOT SPOTS The Challenge of Climate Change

Biodiversity hot spots hold especially high numbers of endemic species, yet their combined area of remaining habitat covers only 2.3 percent of the Earth’s land surface. Each hot spot faces extreme threats and has already lost at least 70 percent of its original natural vegetation. Over 50 percent of the world’s plant species and 42 percent of all terrestrial vertebrate species are endemic to the thirty-four biodiversity hot spots (Conservation International Web site 2008). Islands are of particular importance in a biodiversity conservation context as they cover about 5 percent of the Earth’s land surface but have more than 35 percent of the world’s vascular plants including about fifty thousand endemics. At the same time, about 15 percent of the world’s mammals, amphibians, and birds are exclusively insular in distribution, and 35 percent of all threatened birds are island endemics In fact, of the thirty-four biodiversity hot spots defined by Myers et al. (2000) and refined by Conservation International in 2005, fourteen are islands or island archipelagos or have an important insular component, and six others include offshore islands within their limits. These include such hot spots as New Zealand, Polynesia/Micronesia, Madagascar and the Indian Ocean islands, the Caribbean Islands, the Philippines (with over seven thousand islands), the Mediterranean Basin including Macaronesia (the hot spot was recently expanded to include the Azores Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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and Cape Verde Islands), the Valdivian forests of Chile now including the Juan Fernández Islands, and the Galápagos Islands included in the Tumbes/Chocó continental hot spot, among others. It seems, however, to make little sense to subordinate these last three archipelagos to mere appendices of continental hot spots especially as their high endemicity means that they generally have little in common with the adjacent continents in terms of their unique biodiversity. Island organisms have always been especially vulnerable to human activities, from the extinction of flightless birds such as the dodo through overhunting, the destruction of natural vegetation for agricultural exploitation (e.g., the sugar cane industries in the Canaries and Mauritius), urban development especially for tourism, or the more subtle threat of competition from invasive, introduced alien species. Since human arrival on islands, the native species have always been up against it. And now, because of human-induced climate change they face further threatening challenges including a rise in sea level of, according to recent estimates, between 2 and 15 meters in the next 100 years (Geo-Arizona Web site 2007). Although generally the lowest islands are not rich in endemic biodiversity, it is still a pity to lose them! Apart, however, from being covered by water, we have to ask the question, What makes insular organisms and, in the context of this chapter, insular plants so vulnerable?

CARLQUIST’S ISLAND SYNDROME

Over 35 years ago, Sherwin Carlquist, in his book Island Biology (Carlquist 1974) defined a series of characteristics common to many organisms from islands throughout the world as the island syndrome. This syndrome includes such phenomena as woodiness and longevity in generally herbaceous groups of plants and gigantism in animals, reduction of dispersal capacity through enlarged seeds, diminished efficiency of dispersal mechanisms such as a depauperate pappus in plants of the Asteraceae, and the loss of flight capacity in birds and insects. The obvious tendency for island plants to be poor competitors in the face of invasive species is also considered to be one of the syndrome’s characteristics. The island syndrome includes adaptation to narrow, specific ecological niches through what Carlquist considered to be an irreversible specialization leading to a major ecological shift from the original colonizer, including the need to adapt to new pollinators especially as many islands

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do not have rich pollinating insect faunas. Spencer Barratt, in an important review of reproductive biology of island plants, cites as examples the depauperate insect fauna of the Hawaii archipelago with only six moth species, two butterflies, and two bumblebees, and the Galápagos Islands with only one pollinating bee (Barratt 1998). The strong trend to obligate outcrossing through dioicy and gynodioicy, the so-called escape from homozygosity, also seems to qualify as part of the island syndrome. As long ago as 1955, Herbert Baker pointed out the advantages of being hermaphrodite and self-compatible for the colonization of islands remote from continental sources, (Baker’s law or Baker’s rule; see Baker 1955). As Barratt (1998) suggests, Baker’s rule seems to be supported in general by the evidence, from various sources, that the endemic floras of New Zealand, Hawaii, and the Galápagos Islands have a much lower incidence of homomorphic and heteromorphic incompatibility systems than continental floras. The postcolonization, insular evolution of outcrossing is demonstrated by the endemic flora of Hawaii where Sakai and her collaborators have shown that of about 290 original colonists, only about 10 percent were dimorphic; but that in the endemic flora, almost 15 percent of species are dioecious and 21 percent are sexually dimorphic, apparently the highest proportions known from any flora (Sakai et al. 1995a, 1995b). As an example of the development of outcrossing mechanisms, the situation in Hawaiian Bidens species is significant: 50 percent of the endemic species are gynodioecious, but this mechanism to avoid inbreeding is not found in any of the two hundred or so Bidens species and their relatives occurring outside the Hawaiian archipelago. At the same time the development of wind pollination in some insular endemics can also be seen as an escape from dependence on specific pollinators. A recent paper by Crawford and collaborators on Canarian Tolpis species (Crawford et al. 2008) indicates that the endemic species are incompletely self-incompatible or as the authors term it “pseudo-self compatible”; but the only nonendemic species examined, the Mediterranean Tolpis barbata, which also occurs in the Canaries, is described as highly autogamous, so here again there is probably a trend toward the development of some form of postcolonization outcrossing mechanism in the endemic species. Despite the evolution of outbreeding capacity, there is still considerable evidence of genetic depauperation in island plants generally as a result of passing through postcolonization bottlenecks. Barratt (1998) cites the evidence of reduced variation in allozyme loci in isolated populations of several insular taxa when compared to their continental counterparts.

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A further contributor to the island syndrome, according to Carlquist (1974) and apart from the adaptive shift mentioned earlier, is the phenomenon of adaptive radiation, a speciation process with a marked tendency to enhance floristic richness and lead to the evolution of specialized niche-specific species with narrow ecological and geographic ranges, weak intrinsic isolating mechanisms, and poor dispersal capacity. Generally, selection in this process is for immediate fitness, but, as Givnish (1998) has pointed out, in changing situations such as new competition or unstable environmental conditions, the specialized characteristics arising from adaptive radiation can make the resulting species particularly prone to extinction.

THE ISLAND SYNDROME, CLIMATE CHANGE, AND CONSERVATION

From a conservation point of view, it is informative to consider some of the island syndrome characteristics in the context of climate change. It is frequently stated that the isolated position of islands has made them living laboratories for understanding the adaptation and evolution of species. Islands house unique biodiversity in terms of both ecosystems and species. Isolation, however, has also made them extremely susceptible to invasive species and other stresses, resulting in some of the highest extinction rates of all (Pimm et al. 2006). They can also be highly climate sensitive. For example, coral bleaching associated with El Niño events and the long-term warming of surface waters has become widespread in both the Pacific and Caribbean islands since the 1990s (McWilliams et al. 2005). Other possible climate change concerns include increased extinction rates of high-elevation species that have limited opportunities for migration. Changes in coastal ecosystems such as mangroves, dunes, and halophyte communities and declines in forest cover due to floods, droughts, or increased incidence of pests, pathogens, or fire will affect island endemics. In addition, it is probable that disturbance to natural ecosystems caused by increases in the frequency or intensity of hurricanes and other major climatic incidents would generally favor the intrusion of invasive species, for example, in the Caribbean islands (Maunder et al. 2008). In addition, the unique cloud forests located on many islands of higher altitude occupy a narrow geographic and climatological niche, and a relatively small change in temperature or

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precipitation patterns could possibly cause forest zones to shift upward enough to be eliminated altogether (Loope and Giambelluca 1998). Certainly there is no doubt islands are very vulnerable, and the synergy between climate change itself and the ongoing destruction of habitat due to human activities will, in the future, cause a massive increase in the numbers of threatened island plants and will lead to the extinction of many of them. So, how can island plants and ecosystems respond to climate change? Only by adapting to changing conditions or by migration or extinction. In order to consider how plants might respond or adapt to climate change, the fact that ecosystems are made up of whole series of interacting individual species of many types of different organisms, not just plants, has to be taken into account, especially as each of these species has its own particular climate envelope. Modeling of the climate envelope can be useful in predicting changes in distribution under climate change (Hijmans and Graham 2006). Generally, however, as a result of climate change, each organism including plants will have basically three options: to migrate, to adapt individual climatic envelopes to changing local conditions, or to become extinct.

MIGRATION

Plant response to climate change in the past, at least from what the palaeobotanical evidence tells us, is one of changing their geographic centers of distribution; that is, the response has been to migrate to areas of a more suitable climate. This seems to have been, for example, the principal response in recent interglacial periods (Cheddadi et al. 2005). Obviously, therefore, migration is an issue to take into account for future response to climate change, but (and there is a very large but) species will migrate at different rates depending on a number of independent factors such as generation times, dispersal mechanisms, and available and suitable migration routes. Especially in the case of islands, finding suitable climatic, edaphic, topographical conditions within a migration distance, overcoming genetic bottlenecks and achieving optimum rates of population growth and capacity to establish genetically viable populations are major requirements for survival. The availability of specific niches, competition with broad climate envelope species such as invasive weeds, encountering potentially new pathogens and predators, will also affect the capacity of plants to reestablish after migration. Finding the

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right habitat is not just a question of finding a suitable temperature and water regime; it is obviously a much more complicated issue. Recent studies also tend to suggest that migration will not be able to keep pace with the rate of climate change (Dyer 2007).

ADAPTATION

As for the alternative of adaptation, natural adaptation is not generally a rapid process; even our accelerated, artificial plant breeding processes for annual crop species need various generations to produce genetically stable cultivars. Climate change presents a major challenge for adapting organisms, principally because of the diversity of factors that may be modified in the local environment by changing climatic conditions. Species will, in many cases, be pushed outside their natural climate envelope and have to adapt physiologically to higher temperatures and modified water regimes as well as increasing competition from invasive species. Temperature changes will also affect flowering and fruiting periods, and due to the loss of synchronous relationships with specialist pollinators and seed dispersers, they can disrupt dispersal and pollination efficiency. At the same time, many plant species depend, for passing periods of adversity, on the availability of seed reserves in the soil seed bank to rebuild populations; in turn, the survival of seeds in the soil depends on factors such as humidity and microbial activity. Therefore, we must ask what will happen to microbial activity as the soil warms up? The evidence points to an initial increase in activity until the individual species get to their climate envelope limits. This will affect both the beneficial, mycorrhizal type of organisms and also the microbial seed-infecting pathogens. Changes in both temperature and moisture in the soil may also have an adverse effect on seed dormancy, thus further diminishing the soil seed bank’s capacity for regeneration. Thus, if plants are to stay where they are and adapt to changing local conditions, they may be faced with having to respond to the simultaneous selection pressures for widely differing new traits, not just to the pressure of adaptation to a single factor. Can plants adapt, or will climate change simply outpace individual plant species ability to do so? Bradshaw and McNeilly (1991, p.5), as a result of their own intensive research on plant adaptation, make the following comment: “Although some evolution in relation to climatic change may take place, we must

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not therefore presume that its power will be unlimited in relation to future climatic change. As a result, and because the natural migration of species is now very restricted, we should expect considerable numbers of extinctions.”

CONCLUSION

The characteristics of Carlquist’s island syndrome do not seem to help either adaptation or migration. Insular woodiness and the tendency toward longevity, implying longer generation times, is not contusive to rapid adaptation to changing climatic and ecological conditions. In fact, Carlquist (1974) argues that a moderate, rather humid, stable climate with relatively long growing seasons is what has favored the development of insular woodiness. If climate change, as predicted by many models, implies rapidly increasing temperature and aridity and intensification of extreme conditions, the elements required for survival of woody insular endemics will be disrupted, leading to a new wave of extinctions. Obviously on isolated islands, any migration can only be local, and whole climatic zones with their endemic flora may disappear as the possibility to migrate becomes exhausted by long generation times, ecological limitations, or lack of physical space. A second characteristic of the island syndrome, loss of dispersability, also limits the possibilities of migration. Several authors—Carlquist (1974) and Ehrendorfer (1979), for example—have reviewed this subject, and the latter author concludes that as closed island ecosystems develop, easily and widely dispersed propagules are at a selective disadvantage. He considers that as colonizers radiate from coastal to lowland communities and to humid, upland forest habitats, fewer but larger seeds with more reserves evolve adapted to local reproduction in more stable conditions. Carlquist (1974) calls this change in dispersibility “precinctiveness.” The changes in breeding systems suggested by Carlquist (1974) as a feature of the island syndrome also have a restricting effect on migration and adaptation. Ehrendorfer (1979) suggests that the “genetically more simple way to dioecy” rather than the development of self-incompatibility has been the principal, but not the only, route to overcoming homozygosity. Dioecy, however, has major disadvantages for migration (Baker’s rule) and for adaptation to climate change when the symbiosis with pollinators can be critically affected by changes in pollinator distribution.

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In general terms, therefore, it can be said that the island syndrome creates a critical balance between insular endemics and their environment that can easily be disrupted by climate change and does not help the prospects for their in situ conservation in the face of rapidly changing conditions. Even though we are dealing with relatively manageable numbers of endemics in many cases, we are still, in these circumstances, faced with what Vane-Wright et al. (1991) described as the “agony of choice.” It seems obvious that up to now we have not been very good at the sustainable management and conservation of the world’s islands and their ecosystems even in stable climatic conditions (Rodrigues et al. 2004). How, therefore, are we going to cope with in situ conservation in very delicate and precarious climate change situations on islands where limited resources for human survival may well lead to the further sacrifice of sustainability and conservation. A reading of Jared Diamond’s chapter on Easter Island in his book Collapse (Diamond 2005) creates a feeling of despair for many of the world’s islands, such as Madagascar. This is the real agony of choice: Where to use limited conservation resources available and how to manage them effectively. In these special circumstances where some 15 percent of the world’s natural plant resources are under threat, we cannot wait to see if climate change can be managed in situ, especially considering that for most islands even the most sophisticated climate change models are not good at predictions. In stable conditions, the ideal system is a combination of in situ conservation with an “insurance policy” backup of seed banks and ex situ collections. However, in view of the problems that in situ conservation faces through the impacts of climate change, can major reserves and protected areas be moved to compensate for climate change? Or in how many of them will the future find that what they were set up to protect originally is simply no longer there? The World Wide Fund for Nature report (WWF 2003) shows the extent to which protected areas may be disrupted by climate change and suggests that a major reevaluation of conservation in protected areas is needed. The reliance on in situ conservation alone in the wake of climate change may lead to numerous extinctions. In the case of biodiversity-rich islands, the ex situ insurance policy should be put into effect before it is too late to rescue the wonderful, natural, and scientific resource provided by insular organisms that, apart from everything else, are needed to help interpret evolution and phylogeny on a global scale.

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REFERENCES Baker H.G. 1955. Self-compatibility and establishment after “long distance” dispersal. Evolution 9: 347–349. Barratt S. 1998. The reproductive biology and genetics of island plants. In: Grant P.R., editor. Evolution on islands. Oxford: Oxford University Press pp. 18–34. Bradshaw A.D., McNeilly T. 1991. Evolutionary response to global climatic change. Ann. Bot. (Oxford) 67: 14. Carlquist S.J. 1974. Island biology. New York: Columbia University Press. Cheddadi R., de Beaulieu J.-L., Jouzel J., Adrieu-Ponel V., Laurent J.-M., Reille M., Raynaud D., Bar-Hen A. 2005. Similarity of vegetation dynamics during interglacial periods. Proc. Nat. Acad. Sci. USA 102, 13939–13943. Conservation International. 2008. www.biodiversityhotspots.org/ Crawford D.J., Archibald J.K., Stroermer, D., Mort, M.E., Kelly, J.K., SantosGuerra, A., 2008. A test of Baker’s law: breeding systems and the radiation of Tolpis (Asteraceae) in the Canary Islands. Int. J. Plant Sci. 169: 782–791. Diamond J.M. 2005. Collapse: How societies choose to fail or succeed. New York: Viking Press. Dyer J.M. 2007. Implications of habitat fragmentation on climate changeinduced forest migration. Profess. Geographer 46: 449–459. Ehrendorfer F. 1979. Reproductive biology in island plants. In: Bramwell D. editor. Plants and islands. London: Academic Press pp. 293–306. Geo-Arizona Web Site 2008. http://www.geo.arizona.edu/dgesl/research/other/ climate_change_and_sea_level/sea_level_rise/sea_level_rise.htm. Givnish T.J. 1998. Adaptive plant evolution on islands: Classic patterns, molecular data, new insights. In: Grant P.R., editor. Evolution on islands. Oxford: Oxford University Press pp. 281–304. Hijmans R.J., Graham C.H. 2006. The ability of climate envelope models to predict the effect of climate change on species distributions. Global Change Biol. 12: 2272–2281. Loope L.L., Giambelluca T.W. 1998. Vulnerability of island tropical montane cloud forests to climate change with special reference to east Maui, Hawaii. Clim. Change 39: 503–517. Maunder M., Leiva A., Santiago-Valentin E., Stevenson D.W., Acevedo-Rodriguez P., Meerow A. W., Mejía M., Clubbe C., Francisco-Ortega J. 2008. Plant conservation in the Caribbean Island biodiversity hotspot. Bot. Rev. (Lancaster) 74: 197–207. McWilliams J.P., Cote I.M., Gill J. A., Sutherland W. J., Watkinson A.R. 2005. Accelerating impacts of temperature-induced coral bleaching in the Caribbean. Ecology 86: 2055–2060. Myers N., Mittermeier R.A., Mittermeier C.G., da Fonseca G.A.B., Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–858. Pimm S., Raven P., Peterson A., Sekercioglu C.H., Erlich P.R., 2006. Human impacts on rates of recent, present and future bird extinctions. Proc. Nat. Acad. Sci. USA 103: 10941–10946. Rodrigues A.S.L., Reset Akcakaya H., Andelman S.J., Bakarr M.I., Boitani L., Brooks T.M., Chanson J.S., Fishpool L.D.C., da Fonseca G.A.B., Gaston K.J., Hoffmann M., Marquet P.A., Pilgrim J.D., Pressey R.L., Schipper J., Sechrest

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W., Stuart S.N., Underhill S.G., Waller R.W., Watts M.J.E., Xie Yan. 2004. Global Gap Analysis: Priority regions for expanding the global protected-area network. BioScience 54: 1092–1100. Sakai A., Wagner, W.L., Ferguson D.M., Herbst, D.R. 1995a. Biogeographical and ecological correlates of dioecy in the Hawaiian flora. Ecology 76: 2530–2543. Sakai A., Wagner, W.L., Ferguson D.M., Herbst, D.R. 1995b. Origins of dioecy in the Hawaiian flora. Ecology 76: 2517–2529. Vane-Wright R., Humphries C.J., Williams P.H. 1991.What to protect? Systematics and the agony of choice. Biol. Conservation 55: 235–254. WWF. 2003. No Place to Hide: Effects of Climate Change on protected Areas. World Wide Fund for Nature 12pp.

SEVEN

Mark A. Carine, Arnoldo Santos-Guerra, I. Rosana Guma, and J. Alfredo Reyes-Betancor t

ENDEMISM AND EVOLUTION OF THE MACARONESIAN FLORA

The Macaronesian region (Fig. 7.1) comprises the volcanic oceanic archipelagos of the Azores, Madeira, Salvages, Canary Islands, and Cape Verdes located in the North Atlantic Ocean. The flora of the region demonstrate many characteristics typical of oceanic archipelago floras, notably a high degree of endemism, several spectacular examples of evolutionary radiations, and a distinctive growth form spectrum in the endemic flora with a much higher proportion of woody and succulent taxa than in the near-continent flora (e.g., Shmida and Werger 1992). Argyranthemum (Compositae), the subject of Chris Humphries’s doctoral research (see Humphries 1973, 1975, 1976a, 1976b) provides an excellent example of island evolution in region. Endemic to Macaronesia, Argyranthemum comprises twenty-four species of woody perennials. Molecular data support the monophyly and radiation of the genus in the region (Francisco-Ortega et al. 1997) and indicate that its closest relatives are herbaceous and distributed in North Africa. These findings are consistent with a scenario in which both woodiness evolved in response to insularity and the group radiated in Macaronesia following colonization from the near-continent. Other examples of groups showing similar Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

101

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500km Azores (8.12) Cabo Espichel

Madeira (15) Salvages (24–27) Canary Islands (20.5)

Cape Verdes (10.3)

FIGURE 7.1 Location of the Macaronesian archipelagos of the Azores, Madeira, Salvages, Canary Islands, and Cape Verdes. Cabo Espichel in Portugal is also indicated as the flora of this headland includes endemic species of Euphorbia and Convolvulus considered to have evolved through back-colonization from the Macaronesian islands. The maximum age of each archipelago is given in parentheses.

characteristics include the Aeonium alliance (seventy-five species; Mort et al. 2002), Echium (29 species; Böhle et al. 1996) and Sonchus (twentynine species; Lee et al. 2005). In 1979, Chris Humphries published a paper entitled “Endemism and Evolution in Macaronesia” that reviewed patterns of floristic diversity in the Macaronesian region and discussed the evolution of the region’s endemic flora. The paper also introduced cladistic concepts into the study of the endemic flora for the first time. While no explicit cladistic analyses were presented, the paper highlighted the need for cladistic principles to guide investigations of Macaronesian diversity. Since the publication of Humphries (1979), cladistic methodology has been widely applied to the study of Macaronesian endemic groups. Carine et al. (2004) reviewed sixty-four molecular cladistic analyses of Macaronesian endemic plant lineages that collectively accounted for approximately 32 percent of the endemic flora. The intervening 5 years have seen a further

ENDEMISM OF MACARONESIAN FLORA / 103

substantial increase in the number of published cladistic analyses such that the relationships of more than ninety Macaronesian endemic lineages have now been analyzed within a cladistic framework. These collectively represent over 50 percent of the endemic flora (Table 7.1). While variable both in terms of sampling of taxa and characters and in terms of the degree to which relationships are resolved, they nevertheless provide a rich resource for the study of Macaronesian diversity. In this chapter, we consider the impact of cladistic analyses on our understanding of the Macaronesian flora, focusing specifically on three aspects. First, we consider the biogeographic relationships of Macaronesian plant groups, building on the analyses of Carine et al. (2004) and Andrus et al. (2004) and incorporating more recent results. Second, we consider the impact of cladistic analyses, together with other analyses of regional diversity patterns, on our understanding of patterns of intraregional radiations. Finally, we consider the distinctive growth form spectrum of Macaronesian endemic plants (Shmida and Werger 1992) and present a preliminary evaluation of the extent to which woodiness in Macaronesia may be associated with insularity and linked to intraregional diversification.

THE RELATIONSHIPS OF MACARONESIAN ENDEMIC PLANT GROUPS

Table 7.1 presents data on the relationships of seventy-three genera and alliances with endemic taxa represented in the Macaronesian islands derived from published molecular phylogenetic analyses. Groups such as Euphorbia, Limonium, and Lotus, have not been included because published studies of these groups are extremely limited in sampling of either island or continental taxa (Molero et al. 2002; Lledó et al. 2005; Allan et al. 2004, respectively). In total, the seventy-three genera included in Table 7.1 correspond to eighty-six endemic lineages. Of these, 25 percent are represented in Macaronesia by a single endemic taxon, while 56 percent comprise two or more taxa that are resolved as a monophyletic group. Paraphyly within Macaronesian groups is extremely rare (Table 7.1). To date, it has been documented in the Aeonium alliance (Mort et al. 2002) and is consistent with the pattern observed in Tolpis (Moore et al. 2002). In the case of the Aeonium alliance, more than 70 taxa are endemic to Macaronesia and these form a group that is well supported but is paraphyletic with respect to three taxa that are

TABLE 7.1. molecular phylogenetic studies of macaronesian endemic plant groups In Boldface Are Groups Within Which the Predominant Habit in the Macaronesian Endemic Group Differs from That of the Continental Sister Group

Groupa Adenocarpus Aeonium alliance Androcymbium Andryala Angelica Arbutus Argyranthemum Artemisia Asteriscus 1 Asteriscus 2 (A. graveolens subsp. stenophyllus) Autonoe Avena Azorina Bellis Bencomia alliance Bupleurum Bystropogon Camptoloma Ceballosia Cheirolophus Cicer Cistus

Number of Endemics

Sister Group Distribution

Habit of Macaronesian Lineage

Habit of Sister Group

Reference

3 75 (paraphyletic) 2 5 1 1 24 3 4 1

Mediterranean Mediterranean North Africa Inadequate sampling Eurosiberia+Asia Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean

W W/H G WH WH W W W W W

W H G H H W H WH WH WH

Percy and Cronk, 2002 Mort et al., 2002 Caujape-Castells et al., 1999 Ferher et al., 2007 Spalik et al., 2004 Hileman et al., 2001 Francisco-Ortega et al., 1997 Torrell et al., 1999 Goertzen et al., 2002 Goertzen et al., 2002

4 1 1 1 8 2 7 1 1 17 1 7

Mediterranean Mediterranean Conflicting placement Mediterranean Mediterranean Mediterranean Conflicting placement East Africa Inadequately resolved Mediterranean Inadequate sampling Mediterranean

G H W H W W W WH W W H (per) W

G H H H H/W W H H W W H (ann) W

Wetschnig and Pfosser, 2003 Alicchio et al., 1995 Roquet et al., 2008 Fiz et al., 2002 Helfgott et al., 2000 Neves and Watson, 2004 Trusty et al., 2004 Kornhall et al., 2001 Diane et al., 2002 Susanna et al., 1999 Iruela et al., 2002 Guzman and Vargas, 2005

Convolvulus 1 Convolvulus 2 Crambe Cryptotaenia Cytisus 1 [= Chamaecytisus] Cytisus 2 [= Spartocytisus] Descurainia Echium Erucastrum Euphrasia

8 (paraphyletic) 3 14 1 1 2 7 29 2 2

Genista Gonospermum alliance Hedera 1 (H. azorica) Hedera 2 (H. canariensis) Hedera 3 (H. maderensis subsp. maderensis) Hypochaeris Ilex 1 (I. canariensis) Ilex 2 (I. perodo s.l.)

2 8 1 1 1 1 1 1

Isoplexis Ixanthus Kleinia Kunkeliella Lavatera 1 (L. phoenica) Lavatera 2 (L. acerifolia) Lolium Micromeria Monizia+Melanoselinum

4 1 1 4 1 1 4 17 2

Mediterranean Mediterranean Conflicting placement Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean Widespread: Nearctic and Palearctic Mediterranean Mediterranean Inadequately resolved Inadequately resolved Inadequately resolved Mediterranean Sister to rest of genus East Asia (but I. aquifolium not included) Mediterranean Mediterranean Limited sampling South Africa Limited sampling Conflicting placement Mediterranean Mediterranean Mediterranean

W W W H W W W W (reversal to H) H H (per)

H W H H W W H H H H (ann)

Carine et al., 2004 Carine et al., 2004 Francisco-Ortega et al., 1999 Spalik and Downie 2007 Cubas et al., 2002 Cubas et al., 2002 Goodson et al., 2006 Böhle et al., 1996 Warwick and Black, 1993 Gussarova et al., 2008

W W/WH W W W

W H/WH W W W

Percy and Cronk., 2002 Francisco-Ortega et al., 2001a Válcarel et al., 2003 Válcarel et al., 2003 Válcarel et al., 2003

W W W

H W W

Cerbah et al., 1998 Manen et al., 2002 Manen et al., 2002

W W W W W W H W WH

H H W WH/H W/H — H W H

Bräuchler et al., 2004 Thiv et al., 1999 Pelser et al., 2007 Der and Nickrent, 2008 Fuertes-Aguilar et al., 2002 Fuertes-Aguilar et al., 2002 Inda et al., 2008 Braüchler et al., 2005 Spalik and Downie, 2007 (Continued)

TABLE 7.1. ( CONTINUED ) Sister Group Distribution

Habit of Macaronesian Lineage

Habit of Sister Group

Reference

1 1

South Africa S.W. Morocco

W W

W W

Chanderbali et al., 2001 Besnard et al., 2007

1

Mediterranean

W

W

Besnard et al., 2007

2 15

Conflicting placement Conflicting placement

H W (reversal to H)

H H

Phoenix Phyllis Pinus

2 2 1

Conflicting placement South Africa Conflicting placement

W W W

W W W

Plantago 1 Plantago 2 (P. leiopetala) Plantago 3 (P. subspathulata) Plocama Pulicaria canariensis Pulicaria diffusa Ranunculus Reichardia Reseda crystallina Reseda scoparia

3 1 1

Mediterranean Widespread Mediterranean/ European Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean/Asian

W WH WH

W H WH/H

Hohmann et al., 2006 Panero et al., 1999; Swenson and Manns, 2003 Barrow, 1998 Anderson et al., 1997 Krupkin et al., 1996; Liston et al., 1999; Geada-López et al., 2002 Rønsted et al., 2002 Rønsted et al., 2002 Rønsted et al., 2002

W WH WH H WH H W

W WH WH H H H W

Backlund et al., 2007 Francisco-Ortega et al., 2001b Francisco-Ortega et al., 2001b Paun et al., 2005 Kim et al., 2007 Martín-Bravo et al., 2007 Martín-Bravo et al., 2007

Groupa Ocotea Olea 1 (O. europaea subsp. guanchica) Olea 2 (O. europaea subsp. cerasiformis) Patellifolia Pericallis

Number of Endemics

1 1 1 1 3 1 1

Ruta Sambucus Saxifraga Schizogyne Sedum Sideritis Sideroxylon

3 2 3 2 5 27 3

Silene Sinapidendron Solanum I (Normania) Solanum II Sonchus alliance Teline 1 (linifolia group) Teline 2 (monspessulana group) Tinguarra Todaroa Tolpis

7 5 2 2 29 5 7

Tornabenea Vaccinium Vierea

1 2 10 (poss. paraphyletic) 6 2 1

Mediterranean Mediterranean Eurosiberia Mediterranean New World Mediterranean East Africa/Pacific/ Indian Ocean (Limited sampling) Eurosiberia Mediterranean Mediterranean East Africa Limited sampling Mediterranean Mediterranean

W W H W WH W W

WH W H W WH H W

Salvo et al., 2008 Eriksson and Donoghue,1997 Vargas et al., 1999 Andrus et al. 2004 Van Ham and ’t Hart, 1998 Barber et al., 2002, 2007 Smedmark et al., 2006

W/WH W/H H W W W W

WH H H WH H W W

Clement et al., 1997 Warwick and Black, 1993 Bohs and Olmstead, 2001 Bohs and Olmstead, 2001 Lee et al., 2005 Percy and Cronk, 2002 Percy and Cronk, 2002

Mediterranean Mediterranean Mediterranean

H H WH/H

H H H

Spalik et al., 2001 Spalik et al., 2001 Moore et al., 2001

Mediterranean Unresolved Mediterranean

H W W

H W W

Spalik and Downie, 2007 Kron et al., 2002 Francisco-Ortega et al., 2001b

note: The number of endemic taxa, distribution of sister group (where sampling/resolution of relationship permits this to be determined), and habit of the endemic lineage and sister group are given for each group. Paraphyletic or putatively paraphyletic groups are indicated as such in the column “Number of Endemics.” The following codes are used to describe habit: W, woody; WH, herb woody at the base; H, herb; G, geophyte; (per), perennial; (ann), annual. 1Euphorbia (Molero et al., 2002) and Lotus (Allan et al., 2004) are not included because of inadequate sampling of continental taxa in these groups that show complex patterns of island–continent relationships; Limonium was excluded for similar reasons, with only limited sampling of Macaronesian taxa in this complex genus in the study of Lledó et al. (2005); Festuca was excluded because the resolution available does not allow the number of island groups to be resolved with confidence in the analysis of Inda et al. (2008).

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distributed on the continent. The most plausible explanation for such a pattern of Macaronesian paraphyly is back-dispersal from the islands to the continent, suggesting that islands in the Macaronesian region may not always be the “evolutionary end of the road” (Bellemain and Ricklefs 2008). In total, genera with single endemics (25 percent), monophyletic clades (56 percent), and paraphyletic island grades (3 percent), all of which are consistent with a single introduction into Macaronesia, account for 84 percent of groups considered to date. Of the remaining genera considered, almost all (15 percent) are di- or triphyletic. For example, in the case of Lavatera, there are two species endemic to the Canary Islands. One taxon (L. phoenica) is sister to the entire Lavatera–Malva complex (and is consequently often treated as the monotypic genus Navaea), while the other (L. acerifolia) is resolved in a late-branching position within that clade, and the two are therefore distantly related within the complex (Fuertes-Aguilar et al. 2002). A different sort of pattern of diphyly is suggested by the work of Besnard et al. (2007) on the Olea europaea complex. Relationships in this group are particularly complex. Sequence data suggest that the island lineages are closely related, and both are subspecies of O. europaea, but the endemic subspecies of Olea europea in Madeira (subsp. cerasiformis) is most closely related to the European O. europaea subsp. europaea, while the Canarian subspecies guanchica is most closely related to the southwest Moroccan subsp. maroccana. The remaining genus among our seventy-three study genera is Convolvulus, and this exhibits an even more complex pattern of relationship between island and continent (Carine et al. 2004). Eleven species are endemic to Macaronesia, and these form two distinct clades: one that comprises shrubs endemic to Canary Islands, and a second that comprises woody climbers (Fig. 7.2). The genus is therefore diphyletic in Macaronesia. However, within the climber clade, the Macaronesian species are paraphyletic with respect to the woody continental species C. fernandesii (Fig. 7.2) that is a pinpoint endemic found only at Cabo Espichel in Portugal (Fig. 7.1). As with Aeonium, these data are consistent with back-colonization from the islands to continent (in this case, to Cabo Espichel). Molecular data support a similarly complex pattern in Euphorbia although this group was not included in Table 7.1 because of limited continental sampling. It is notable, however, that Euphorbia pedroi is also endemic to Cabo Espichel and is likely also to be the result of a back colonization from the islands to the continent. The co-occurrence

9 6 9 3

9 9

10 0

6 5 7 9

8 4

9 0

9 0

9 1 10 0

5 4 8 3

9 6

8 10 4 0 10 0

9 8

9 8

10 0 9 5 9 9

9 7

7 7 10 0 9 8 8 4

7 9 5 4 5 7

10 0

7 1

10 0 10 0

5 2

8 9

6 7 9 9 6 6 10 0

9 9 10 0 7 7 0 6

C. gharbensis C. siculus C. supinus C. sabatius C. canariensis1 C. canariensis2 C. fernandesii C. fruticulosus C. lopezsocasii II C. massonii1 C. massonii2 C. glandulosus1 C. glandulosus2 C. volubilis C. tricolor C. humilis C. glomeratus C. arvensis Calystegia sepium Calystegia sylvatica Calystegia soldanella C. althaeoides1 C. althaeoides2 C. leucochnous1 C. leucochnous2 C. leiocalycinus C. caput-medusae C. scoparius I C. floridus C. cneorum C. lanuginosus C. doryanium C. acanthocladus C. lineatus1 C. lineatus2 C. mazicum C. compactus C. boisierri C. holosericeus C. cantabrica1 C. cantabrica2 C. oleifolius C. argyrothamnos C. desertii C. prostratus C. trabutianus1 C. trabutianus2 C. ulicinus C. cephalopodus C. oxyphyllus1 C. oxyphyllus2 lpomoea polymorpha lpomoea tricolor Lepistemon owarensis Turbina corymbosa Ipomoea arborescens Merremia tuberosa C. nodiflorus Jacquemontia mexicana

FIGURE 7.2 Strict consensus tree from analysis of ITS data (after Carine et al. 2004) showing relationships of the Macaronesian endemic species of Convolvulus. Clades I and II correspond to the two Macaronesian endemic groups. Clade I comprises three species of shrubs, all of which are endemic to the Canary Islands. Clade II comprises shrubby climbing and trailing plants. Most are distributed in the Canary Islands, but C. massonii is endemic to Madeira, and C. fernandesii is endemic to Cabo Espichel in mainland Portugal. Bootstrap percentages and Bremer support values are shown above and below branches, respectively.

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of these two endemics of Macaronesian affinity at Cabo Espichel suggests a particularly intriguing relationship between this small area of the Portuguese mainland and the Macaronesian islands. In terms of the biogeographic relationships of island endemics, cladistic studies support the view that the endemic flora of Macaronesia is, for the most part, closely related to the Mediterranean flora, with more than 60 percent of groups documented in Table 7.1 having a sister clade exclusively or largely Mediterranean in distribution. Given that the sister group relationships of a further 20 percent of groups included in Table 7.1 have yet to be satisfactorily resolved (due to inadequate sampling of continental taxa, unresolved relationships or conflicting relationships), the proportion of Macaronesian endemic groups with clearly established sister group relationships outside the Mediterranean basin is extremely limited. Many Macaronesian endemic groups appear to have good dispersal ability, as evidenced by distributions within the region that span several archipelagos. For example, Argyranthemum occurs on the Canaries, Salvages and Madeira, a distribution spanning over 400 kilometers (see Fig. 7.1); Echium occurs on Madeira, the Canaries, and Cape Verdes, the latter two separated by about 1,300 kilometers (see Fig. 7.1). Both distributions suggest dispersal over large distances within the region. In contrast to remote oceanic island archipelagos such as the Hawaiian Islands, located approximately 3,500 kilometers from the nearest continental landmass, the Macaronesian islands and particularly the Canaries are relatively close to continental landmasses. Indeed, the easternmost Canary Islands are presently only 95 kilometers from the coast of North Africa and at periods during the last 20 million years have probably been as close as 65 kilometers (García-Talavera 1997, 1999), with the Mediterranean vegetation zone also extending farther south at times during the Pliocene-Pleistocene (Quézel 1978). The close relationship between the Macaronesian endemic flora and the Mediterranean flora implied by cladistic analyses is therefore somewhat at odds with the limited connection between the island and continental floras suggested by the low frequency of island paraphyly and polyphyly, particularly when the apparent dispersal ability of island endemic lineages is taken into account. Carlquist (1974) noted that establishment following initial dispersal of propagules may be a more significant factor than dispersal in limiting the number of successful colonizations onto oceanic islands; and, more recently, several papers have discussed “niche pre-emption” in the context of the patterns of sister group relationships observed for

ENDEMISM OF MACARONESIAN FLORA / 111

Macaronesian endemic taxa (Silvertown 2004; Silvertown et al. 2005; but see Herben et al. 2005; Saunders and Gibson 2005). Such explanations may offer a more plausible explanation than dispersal barriers to explain the patterns of continental sister-group relationships of continental sister group relationships of Macaronesian endemic lineages revealed by cladistic analyses.

INTRAREGIONAL RADIATION PROCESSES

Reyes-Betancort et al. (2008) investigated the distribution of endemic diversity in the Canary Island archipelago using WORLDMAP. From their analysis of the patterns of endemic taxon richness, it is apparent that diversity is not evenly distributed (Fig. 7.3). Thus, in Tenerife for example, two areas of particularly high diversity can be identified, and these correspond to the Teno and Anaga massifs, respectively, areas that are highly eroded and relatively ancient massifs. Reyes-Betancort et al. (2008) also investigated patterns of range size rarity, a diversity measure that simulates endemicity, and phylogenetic diversity sensu Vane-Wright et al. (1991) that utilizes information on the cladistic relationships of taxa to derive a measure of diversity. They found a close correspondence between range size rarity and phylogenetic diversity. This suggests that the centers of endemism observed in the archipelago are not the result of the localized radiation of lineages. Rather, they are the result of the accumulation of endemics from many different lineages, indicating that geographic speciation has played an important role in generating the patterns of endemic diversity observed in the Canary Islands flora. Cladistic analyses of Macaronesian endemic plant groups also support this conclusion. In a review of molecular phylogenies of island lineages, Baldwin et al. (1999) concluded that adaptive radiation (i.e., adaptation to different habitats) is prevalent in plants of the Hawaiian, Juan Fernández, and Madeiran archipelagos, whereas in the Canary Islands, geographic speciation through isolation on different islands but in similar habitats has been more common. Baldwin et al. (1999) considered only three Macaronesian groups (Argyranthemum, Francisco-Ortega et al. 1996; Sonchus, Kim et al. 1996; the Aeonium alliance, Mes and ‘t Hart 1996). However, molecular phylogenies of other Canary Island endemic groups suggest a similar dominant island isolation pattern (e.g., Gonosperminae, Francisco-Ortega et al. 2001a; Crambe section Dendrocrambe, Francisco-Ortega et al. 2002; Lotus, Allan et al. 2004; Bystropogon, Trusty et al. 2004); while in other Canarian radiations, both

FIGURE 7.3 The distribution of endemic plant diversity in the Canary Islands archipelago at a 10 × 10-kilometer grid scale. Numbers in each cell indicate the total number of endemic species present.

ENDEMISM OF MACARONESIAN FLORA / 113

adaptive radiation and island isolation appear to have contributed to the diversity observed (e.g., Sideritis, Barber et al. 2002, 2007; the Sonchus alliance, Lee et al. 2005; Pericallis, Swenson and Manns 2003). It is not yet clear why geographic isolation should be such an important mechanism in the Canary Islands flora. One possible explanation was put forward by Carine and Schaefer (2010), who drew on palaeoclimatic inferences to suggest that it may be related to the highly variable Pleistocene climatic regime in the islands. Ortiz et al. (2006) presented palaeosol data from the Eastern Canary Islands that suggested frequent and abrupt transitions between humid and arid conditions with an approximate cyclicity of every 7,000 years during the late Pleistocene and Holocene. Carine and Schaefer suggested that this could have served as a driver of the recent and rapid diversification of the flora (consistent with the pattern observed in molecular phylogenetic analyses of many groups), with climatically induced population contractions and expansions leading to genetic bottlenecks and driving the differentiation of lineages isolated on different islands.

GROWTH FORM SPECTRUM

In the case of oceanic island systems such as Hawaii, the predominance of woodiness in the endemic flora has been attributed to the evolution of woodiness in situ and in response to insularity—so-called insular woodiness (Carlquist 1974). In Macaronesia, however, the situation has been more complex. One of the habitats unique to Macaronesia is the laurisilva, a temperate rain forest dominated by Lauraceae taxa. Previously such forests may have been more widespread across the continent as evidenced by fossils of Lauraceae and other laurisilva taxa found in deposits in southern Europe. It has been hypothesized that the impact of glaciations in Europe and the aridification of North Africa led to the eradication of continental laurel forests, with their survival only in Macaronesia (Axelrod 1975) and in small refugial areas (Barbero et al. 1981; Arroyo-García et al. 2001; Rodríguez-Sánchez and Arroyo 2008). The Macaronesian flora has therefore been viewed, for the most part, as a relict of a formerly widespread vegetation type, with woodiness in the flora a primitive trait. Insights from cladistic analyses suggest that this is certainly not the case in all groups, and in several examined to date—for example, Argyranthemum (Francisco-Ortega et al. 1997) and Echium (Böhle et al.

1 1 4 / B O TA N Y

1996)—woodiness appears to be a derived trait associated with insularity, in a manner comparable to the situation observed in the Hawaiian flora. The situation, however, is complicated. In Convolvulus, for example, both island groups are woody. However, one clade (Fig. 7.3, clade I) has a woody continental sister clade, and woodiness is therefore plesiomorphic for this group; whereas the other endemic Macaronesian clade, clade II, also woody, is nested within a herbaceous clade, and woodiness is therefore a derived island condition for this group. As a preliminary analysis of the extent to which a robust, woody habit in Macaronesian endemic lineages is associated with insularity, we compared the growth form of island groups and their closest continental relative inferred in the eighty-six cladistic analyses presented in Table 7.1. We used dominant growth form to reflect the fact that in some island endemic groups, most species exhibit a particular growth form distinct from the closest continental relative while a subset may not. For example, in Echium, most island endemic taxa are woody, in contrast to the herbaceous habit of the continental sister group. However, some Macaronesian endemic Echium species show a reversal to a herbaceous habit (Böhle et al. 1996). For several groups in which the sister group relationships of the island clade remain imprecisely resolved, we were able to assess the habit of the island clade in relation to continental taxa because either (1) there is little variation in habit across the genus (e.g., Ceballosia) or (2) the Macaronesian clade is markedly more robust than any closely related taxa (e.g., Azorina, Pericallis). In most groups documented in Table 7.1 (69 percent of groups; Table 7.2), the habit of the island group is the same as that on the continent with herbaceous Macaronesian endemics possessing herbaceous

summary of the habit of island endemics and their continental sister taxa

TABLE 7.2.

For Groups in Table 7.1 Habit of Island and Continental Taxa Similar habit in both continental and island sister taxa Habit of island taxon more robust than that of continental sister taxon Habit of continental taxon more robust than that of island sister taxon

Proportion of Groups in Table 7.1 (%) 69 31 0

ENDEMISM OF MACARONESIAN FLORA / 115

continental sister taxa and woody island endemics possessing woody continental sister taxa. The remainder (31 percent) show a more robust, woody growth form in the island clade in comparison with their closest continental relative. There are no examples of lineages that show a less robust form in the island clade (Table 7.2). It is interesting to note that the unidirectional transition contrasts with the situation observed in animal groups wherein some groups show island dwarfism (e.g., ungulates, small carnivores), while others show island gigantism (e.g., murid rodents; Meiri et al. 2008). The results of our survey indicate that the predominance of woodiness observed in the Macaronesian flora reflects both (1) woodiness that is shared with continental sister taxa and therefore plesiomorphic for the island group, and (2) a significant proportion of taxa within which a robust woody habit is present in the insular clade but not the continental sister clade. We have not explicitly sought to optimize characters on to cladograms, so no indication of polarity is conveyed in these analyses. However, as we have already noted, in several studies where a transition has been documented, it has occurred from herbaceous to woody in association with insularity. If this is generally true for the sister taxon comparisons we present (as we expect to be the case), then there is a substantial proportion of taxa for which woodiness in Macaronesia is a derived island trait, a finding consistent with the views of Carlquist (1995). Many of the groups within which woodiness is associated with insularity have also radiated extensively in the region, such as Argyranthemum (twenty-four species), Echium (twenty-nine species), and Sideritis (twenty-seven species; Table 7.1). However, this is not always the case. For example, Azorina, which is much more woody and robust in habit than its close continental relatives within Campanula, comprises a single Macaronesian endemic taxon. Figure 7.4 illustrates the patterns of taxon richness for the eighty-six endemic groups considered in Table 7.1. Overall, most endemic lineages have a single representative (Fig. 7.4; 35 taxa) and the number of endemic taxa per lineage follows a classic hollow curve such that very few lineages have many endemics. However, comparison of groups that (1) exhibit the same habit on the islands and continent (Fig. 7.4; white bars) and (2) those that are more woody on the island than on the continent (Fig. 7.4; shaded bars) indicates that the largest endemic groups all exhibit a different habit to their continent sister group. Indeed, endemic lineages that show greater woodiness than their continental sister taxon appear to be disproportionately represented to the right of the curve (Fig. 7.4). A Mann-Whitney test

1 1 6 / B O TA N Y

FIGURE 7.4 Graph summarizing the number of species per group for lineages in Table 7.1. White bars indicate groups in which the island endemic lineage has a habit similar to that of its closest continental relatives; solid bars indicate groups in which the habit of the island endemic lineage is more robust and woody than that of its closest continental relatives.

further suggests that the number of species per lineage in those groups with different habits on island and continent differ significantly in their endemic taxon diversity from those with the same habit (p = 0.0006). Why should such a pattern be observed? Assuming that sister group comparisons are an effective surrogate for character optimizations, it is possible that the evolution of a more robust habit on islands may represent a key innovation freeing lineages from evolutionary and ecological constraints and thereby facilitating their radiation. This analysis is, of course, preliminary and rather speculative based, as it is, only on sister group comparisons. Further work is therefore necessary to robustly test the pattern observed but the analysis we present does illustrate the potential power of cladistics to shed new light on patterns of island diversity.

CONCLUSION

Our aim in this chapter was to give an overview of the contribution of cladistics to our knowledge of the Macaronesian flora since Chris Humphries first sought to apply cladistic concepts to the study of the Macaronesian flora in his 1979 paper “Endemism and Evolution in the Macaronesian Flora.” Cladistics has provided many new insights into the endemic diversity of the Macaronesian region. In some instances,

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cladistic analyses have supported earlier hypotheses—for example, in revealing a close relationship between the Macaronesian endemic flora and the Mediterranean flora. In other cases, established hypotheses have been challenged—notably, in the origin of the robust, often woody habit that is predominant in the endemic flora and that now appears to be plesiomorphic in some endemic lineages but apomorphic in many others. Cladistic analyses have helped to highlight unique features of the region’s diversity—for example, differences in the relative contribution of island vicariance and adaptive radiation in generating endemic diversity in the Canaries and in other oceanic island floras—and have provided a framework for investigating other aspects of Canarian diversity, such as the relationship between the evolution of novel growth forms and diversity that requires explicit knowledge of relationships. There has recently been a renewed interest in the use of oceanic volcanic archipelagos such as those of the Macaronesian region as model systems for the study of evolutionary processes (e.g., Emerson and Kolm 2005; Whittaker et al. 2007, 2008). Knowledge of the relationships of endemic lineage derived from cladistic analyses are fundamental to efforts to understand the historical processes responsible for generating the unique diversity of such regions.

Acknowledgments

We gratefully acknowledge the assistance of Marta Bermejo Jambrina in the compilation of Table 7.1. We also thank the organizers of the symposium for the opportunity to present this work. Finally, we acknowledge Chris Humphries for his support, encouragement, and collaboration with our research on the Macaronesian flora.

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EIGHT

J av i e r Fr a n c i s c o - O r t e g a , A r n o l d o S a n t o s - G u e r r a , Charlie E. Jar vis, Mark A. Carine, Miguel Menezes de Sequeira, and Mike Maunder

E A R LY B R I T I S H C O L L E C T O R S A N D OBSERVERS OF THE MACARONESIAN FLORA From Sloane to Darwin

MACARONESIA: AN EXOTIC INSULAR FLORA CLOSE TO MAINLAND EUROPE

Although the four northern Macaronesian archipelagos of the Azores, Canaries, Salvages, and Madeira are located relatively close to the European mainland, they have many endemic species that are morphologically very different from those found on the mainland. These islands were therefore an early place of interaction between European botanists and a spectacular flora characterized by high levels of endemism. European botanists found in these islands an “exotic” flora that was convenient to visit as part of larger scale Atlantic explorations and one that could be studied directly without major logistical investments. It is, therefore, not surprising that the unique flora of Macaronesia has attracted the attention of herbalists and botanists since the islands were colonized by European settlers in the fifteenth and sixteenth centuries. As early as 1494, a specimen of the dragon-tree, (Dracaena draco L. L. [Dracaenaceae]), a species then known only from the Macaronesian islands, was cultivated in the monastery of the Holy Trinity in Lisbon (Paz-Sánchez 2004), with another one reported in the grounds of the Convent of Our Lady of Grace, in the same city (Clusius 1576). During the fifteenth and sixteenth centuries, this species was depicted Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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in several religious paintings as one of the notable elements of the Garden of Eden (reviewed by Sánchez-Pinto 2001; Mason 2006). Likewise, we also know that between 1558 and 1603, during Elizabeth I’s reign, plants from the Canaries were brought to the Royal Gardens at Hampton Court; interestingly, the same gardens sent at least one expedition to collect plants from these islands in the late seventeenth century during the reign of William III (Sands 1950). The Macaronesian archipelagos were important stopping points for several of the most important European expeditions to study the natural resources found in the New and Old World colonies, and extensive reports on the natural history of the islands are found in most of the published travel logs of these scientific trips (Herrera Piqué 2006a). It is also well known that during this period there were active and strong trade links between Macaronesia and England (Morales Lezcano 1970; Andrews 1984; Sousa 1994), and it has been suggested that these commercial connections might have facilitated an early knowledge of the peculiarities of the insular flora among European herbalists (FranciscoOrtega et al. 1994; Francisco-Ortega and Santos-Guerra 1999). In 1992 we started a project to investigate to what extent the flora of Macaronesia was known among pre-Linnaean botanists from Britain (see Santos-Guerra 1993; Francisco-Ortega et al. 1994, 2008, 2009; Francisco-Ortega and Santos-Guerra 1999). Our work has been based on a study of documents and herbarium specimens located in the Sloane Manuscript Collection of the British Library, the Linnean Society of London, and the Natural History Museum in London (with a special emphasis on Sloane’s Horti Sicci collection). In this chapter, we present a review of our major findings. The first part of our paper provides an overview of three plant hunting expeditions that took place between 1678 and 1797 (Fig. 8.1), followed by an evaluation of what was known of the Macaronesian flora by seventeenth-century British botanists and horticulturists. Finally, we give an account of a plant-hunting trip to Macaronesia that took place between 1776 and 1779, which established the initiation of modern plant taxonomic studies for this region (Fig. 8.1). The main conclusion of our research is that these collections represent some of the most important milestones in the history of natural history of Macaronesia, and also that they enhance the extraordinary historical importance of public and private gardens in the advancement of botanical research in Europe. We argue that these early studies helped to establish the Macaronesian islands as a resource for British horticultural collectors and as a scientific arena that ultimately, via the activities of

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FIGURE 8.1 Plant hunting expeditions from Britain to Macaronesia undertaken by James Cuninghame, Francis Masson, Sir Hans Sloane, and Thomas Simmons in the late seventeenth and eighteenth centuries.

authorities such as Alexander Von Humboldt (1769–1859) and Charles Darwin (1809–1882), created a pivotal role for islands in studies of biogeography and evolution, and subsequently in the development of conservation as a quantitative science. This chapter pays homage to our esteemed colleague Dr. Chris Humphries and is a celebration of the great tradition of synergy among horticulture, systematics, and field botany that has so characterized the study of the Macaronesian flora.

1687: SIR HANS SLOANE’S VISIT TO MADEIRA

Sir Hans Sloane (1660–1753) was one of the most important patrons of science during the first half of the eighteenth century (MacGregor 1994). Trained as a physician, he was interested in all branches of natural history, but particularly in plants, and he amassed a huge collection

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of all manner of material: animal, vegetable, and mineral (Brooks 1954). While he personally collected many specimens when he was young, the enormous size of his mature collection (which formed the core of the British Museum’s collections at its inception in 1753) was mainly the result of the acquisition of collections made by others (Caygill 1994). Sloane founded a botany club at the Temple Coffee House, an informal gathering of plantsmen now recognized as the earliest natural history society in Britain (Riley 2006). On September 12, 1687, as a young man, he left for Jamaica as physician to the new governor of the island, and Sloane’s subsequent published accounts of the natural history of Jamaica are well-known (Sloane 1696, 1707, 1725). However, what is perhaps less well-known is that on the route out, Sloane’s ship (the Assistance) stopped in Madeira for three days (October 21–23, 1687), giving him the opportunity to collect plant specimens, over forty of which are still preserved in Sloane’s Horti Sicci at the Natural History Museum in London (Menezes de Sequeira et al. 2010). Images of these specimens can be seen at www.nhm. ac.uk/research-curation/research/projects/sloane-herbarium/index.htm. Although it seems clear that others collected specimens in Macaronesia before 1687 (this is an area where further research is needed), as far as we are aware, Sloane’s material appears to be the earliest documented herbarium collection for Macaronesia. A concise catalogue of the plants Sloane found during his time abroad, including those found in Madeira, using polynomial Latin diagnoses, was published in his Catalogus plantarum (Sloane 1696), but a far more detailed account of Sloane’s travels, with additional English descriptions and illustrations of many of the plants, appeared in 1707 (a second volume followed in 1725) with his Voyage to the Islands Madera, Barbados, Nieves, S. Christophers and Jamaica (Sloane 1707, 1725). In all, over sixty Madeiran plants are described, with several of them also illustrated (Sloane 1707; Menezes de Sequeira et al. 2010).

1692: PLANT HUNTING FOR THE CHELSEA PHYSIC GARDEN—MACARONESIAN PLANTS IN EARLY HORTICULTURE

A second early reference for plant exploration, this time concerning the flora of the Canary Islands, is also linked to Sloane. The Sloane Manuscript Collection at the British Library contains a three-page manuscript,

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listing both seeds (two pages) and trees (apparently as living plants; one page) collected in the Canary Islands in 1694 (Francisco-Ortega and Santos-Guerra 1999). The material was collected by Tho [Thomas] Simmons, whom we believe to have been a British merchant who worked in the Canaries during the late seventeenth century (Francisco-Ortega and Santos-Guerra 1999). On the verso of one of the folios, it is indicated that the material was sent to Samuel Doody (1656–1706), an apothecary who was by then the curator of the Chelsea Physic Garden. We have not found any herbarium collections associated with this manuscript, but we believe that this manuscript list represents the earliest known account of plant material being shipped from the Canaries to enrich the living collections of a botanic garden. Comparison of the seed and plant lists shows that the former has forty-six entries and the latter has twenty-two. The total number of different species across both lists is forty-seven. Thirtyeight Spanish vernacular names appear in the lists, and many of them are also found in Plukenet’s accounts (which we discuss later). Many of the common names refer to endemic species such as Bosea yervamora L. (Amaranthaceae) (“Yerva mora”) and Bystropogon canariensis (L.) L’Hér. (Lamiaceae) (“Poleo mons”), and we are certain that, by then, several of these species were commonly grown in the gardens of London. There was considerable interest in Macaronesian plants in European living plant collections at the time. Enthusiasts included Gaspar Fagel (1634–1688), Magdalena Poulle (1632–1699), the Commelins in the Netherlands (Wijnands 1983; Hartog and Teune 2002; Zwaan 2002), and notably the Duchess of Beaufort in the United Kingdom, a member of Sloane’s circle who maintained a large, exotic plant collection including Macaronesian species. Apart from the family’s estate at Badminton, the Duchess also owned a property adjacent to the Chelsea Physic Garden, and Doody gave her “roots and plants” from the Chelsea collection (McClain 2001). Aiton (1789) lists over twelve Macaronesian endemics being grown in the gardens of the Duchess of Beaufort, and more than thirteen endemics from the islands were cultivated in the Hortus Medicus of Amsterdam by the Commelins between 1697 and 1706 (Wijnands 1983). Likewise, the Royal Gardens of Hampton Court also boasted several Macaronesian plants, and Aiton (1789) mentions four species from the region cultivated in these gardens, with the Canarian endemic Justicia hyssopifolia L. (Acanthaceae) being grown as early as 1690. By the early eighteenth century, at least nine Canary Island species were also cultivated at the Chelsea Physic Garden (FranciscoOrtega et al. 1999).

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We also think that the famous gardens established by John Tradescant (ca. 1570–1638) and his son, also called John (1608–1662), between the late 1620s and late 1670s in Lambeth, near London, contained plants from Macaronesia. These gardens, together with a cabinet of curiosities, were known as “The Ark” that formed Britain’s first public museum (Allan 1964; Potter 2006). Although no Macaronesian plants appear to be listed in the garden catalogue published by Tradescant the younger (1656), we know that by 1646 he was involved in trading between England and the Canaries (Potter 2006). Although it is not certain what trade was being conducted, it would be surprising (given his interests) if at least some exotic plants from these islands did not reach The Ark via these commercial activities.

1697–1698: JAMES CUNINGHAME’S HERBARIUM COLLECTION FROM THE CANARY ISLANDS

Chronologically, the third contributor of Macaronesian specimens, James Cuninghame (ca. 1667–1709), a native of Scotland who had trained as a physician, was another of Sloane’s numerous correspondents. Little is known of Cuninghame’s early life, but he is well-known for his travels in China. He was the first Western plant hunter whose Chinese herbarium collections reached Europe (Bretschneider 1881; Cox 1945). Cuninghame collected specimens of nearly six hundred Chinese species, as well as many more wherever he made landfall on his journeys to and from that country. Much of his material he sent to James Petiver (1665–1718), a London-based apothecary who amassed a huge collection of natural history objects and who refers to Cuninghame as an outstanding botanist and “a most industrious promoter of Natural Philosophy” (Petiver 1695– 1703). After Petiver’s death, Sloane purchased the collection, the plant portion of which now comprises 106 volumes (out of 265) of Sloane’s Horti Sicci. Unfortunately, no portrait of Cuninghame is known. Cuninghame left England for his first trip to China, to the island of Chusan, in 1697 aboard HMS Nassau, a sixty-four-gun ship-of-the-line recently converted to a troop ship. However, there was a mutiny on board and, at the island of La Palma in the Canary Islands in December 1697, some of the men deserted (Dandy 1958). In trying to recapture them, the captain incurred the wrath of the Spanish authorities, resulting in the ship being seized and the crew imprisoned. Cuninghame, too, was imprisoned, but during his stay in this island he developed friendships with Fathers Juan

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B. Poggio (1632–1707) and Isidoro Arteaga de La Guerra, two prominent priests of the parish of San Salvador in Santa Cruz de La Palma. We believe that these two clergymen arranged for him to collect plants on the island. After his departure from La Palma, Cuninghame exchanged several letters with Fathers Poggio and Arteaga. These letters can also be found in the Sloane Manuscript Collection of the British Library, but they mostly deal with theological topics (Santos-Guerra 1993). Cuninghame created the first known documented collection of herbarium specimens from the Canary Islands, running to over 188 specimens which are now in Sloane’s Horti Sicci. Among the material collected by Cuninghame there is a specimen of Argyranthemum haouarytheum Humphries & Bramwell (Asteraceae) (Fig. 8.2), a species endemic to La Palma that was only described and named for the first time in Chris Humphries’s monograph of the Macaronesian genus Argyranthemum (Humphries 1976). Scattered between three different volumes (HS 189, 241, 267), the specimens reached Sloane through Petiver’s collections (Dandy 1958). Although the identification of a few specimens remains uncertain, we have so far identified over 111 different species (including lichens, mosses, and ferns, as well as seed plants) from among the collected specimens. The collection is surprising in its breadth as it includes plants from all the main ecosystems of La Palma with the exception of the high-elevation areas (Fig. 8.2). For example, it includes Pinus canariensis C. Sm. (Pinaceae), evidently collected in the lowland pine forest; Apollonias barbujana (Cav.) Bornm. (Lauraceae), Gesnouinia arborea (L.f.) Gaudich. (Urticaceae), Myrica faya Aiton (Myricaceae), Phyllis nobla L. (Rubiaceae), Picconia excelsa (Aiton) DC. (Oleaceae), Semele androgyna (L.) Kunth (Liliaceae), and Teline stenopetala Webb & Berthel. (Fabaceae) from the laurel forest; Dracaena draco, Maytenus canariensis (Loes.) G. Kunkel & Sunding (Celastraceae), Micromeria herpyllomorpha Webb & Berthel. (Lamiaceae), and Visnea mocanera L.f. (Ternstroemiaceae) from the lowland scrub; and Rumex lunaria L., Polygonum maritimum L. (both Polygonaceae), and Asteriscus aquaticus (L.) Less. (Asteraceae) from the coastal belt. As well as bringing back plant specimens, Cuninghame also prepared a five-folio catalogue, with sixty-nine entries, that apparently accompanied some of the herbarium material sent to Petiver, now in the Sloane Manuscript Collection of the British Library (Fig. 8.3). Cuninghame was evidently thoroughly abreast of the botany of his time; his Chinese specimens, for instance, often carry labels with full

A

B

D

E

G

H

C

F

FIGURE 8.2 Selection of herbarium specimens collected by James Cuninghame in La Palma between December 1697 and January 1698. Location of specimens in Sloane’s Horti Sicci herbarium is indicated. A, Phyllis nobla L. (Rubiaceae), Vol. 267: 40; B, Micromeria herpyllomorpha Webb & Berthel. (Lamiaceae), Vol. 189: 23; C, Semele androgyna (L.) Kunth (Ruscaceae), Vol. 189: 25; D, Argyranthemum haouarytheum Humphries & Bramwell (Asteraceae), Vol. 189: 16; E, Myrica faya Aiton (Myricaceae), Vol. 189: 31; F, Pinus canariensis C. Sm. (Pinaceae), Vol. 189: 31; G, Visnea mocanera L.f. (Ternstroemiaceae), Vol. 189: 37; H, Teline stenopetala Webb & Berthel. (Fabaceae), Vol. 189: 36. Used by permission of the Natural History Museum, London.

FIGURE 8.3 Reproduction of first page of a manuscript listing plants recorded by James Cuninghame during his plant hunting expedition to La Palma (Canary Islands). Copyright © British Library Board. All rights reserved. Folio 5 (recto), volume 2376 from the Sloane Manuscript Collection (The British Library).

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descriptions of the plants, with information as to their localities, uses, and local names (Dandy 1958). Although this is not generally true of his Canary Island specimens, each of the La Palma plants in this list has an apparently novel Latin diagnosis provided by him.

1691–1705: HOW WELL WAS THE MACARONESIAN FLORA KNOWN IN BRITAIN?

The fourth historical milestone is supplied by Leonard Plukenet (1642– 1706), a well-to-do London botanist who also appears to have practised as a physician (though no record is known of his having either trained or registered as one). During his lifetime, he amassed a large herbarium of some eight thousand specimens, most of them acquired from correspondents abroad. He had his own small botanic garden in Westminster and was appointed superintendent of the Royal Gardens at Hampton Court after the accession of William and Mary in 1689 (Allen 2004). However, Plukenet is probably best known for the many descriptions and illustrations of new species that he published between 1691 and 1705 that appeared in four main works (Plukenet 1691–1694, 1696, 1700, 1705). With over 2,000 drawings arranged over 327 copper plates (illustrated by John Collins, ca. 1691–1705), his Phytographia is one of the most remarkable pieces of botanical illustration ever published, and Linnaeus had a high opinion of his work. After Plukenet’s death in 1706, his herbarium was purchased by Sir Hans Sloane in whose own herbarium Plukenet’s specimens now occupy twenty-three bound volumes. A study has shown that there are numerous descriptions and illustrations of Macaronesian plants in Plukenet’s published works, and they can often be associated with corresponding specimens in his herbarium (Francisco-Ortega et al. 1994). A total of 97 species descriptions and 54 drawings of Macaronesian taxa have been found in Plukenet’s writings, the vast majority of them from the Canary Islands but also with a few from Madeira. We also found 131 herbarium specimens, representing 87 species, associated with these descriptions and drawings, together with a further 33 herbarium specimens of taxa not reported in his published works. A total of 91 different species from Macaronesia are found in Plukenet’s works or herbarium collections. Plukenet was aware of the collections made in Madeira by Sloane (1696), for in his accounts of the Macaronesian species Asplenium

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hemionitis L. (Aspleniaceae) and Euphorbia piscatoria Aiton (Euphorbiaceae), Plukenet refers to the corresponding descriptions provided by Sloane (1696) for Madeiran plants. It is likely that Plukenet also knew about the collections made in the Canaries by Simmons (and sent to Doody) and by Cuninghame. Although Plukenet’s Macaronesian plant descriptions do not make any direct mention of these two herbalists, references to Doody are common in Plukenet’s works (Dandy 1958), and twenty-three of the Spanish common names found in Simmons’s lists of Canary Island plants can be found in Plukenet’s descriptions of Macaronesian plants (Francisco-Ortega and Santos-Guerra 1999).

1724: LOUIS FEUILLÉE IN THE CANARY ISLANDS

Another naturalist who made a major botanical contribution was the French naturalist Rev. Louis Feuillée (1660–1732) who visited the islands of La Gomera, El Hierro, and Tenerife between June 23 and October 10, 1724 (Puig-Samper and Pelayo 1997). Feuillée not only collected herbarium specimens but also made drawings of thirty-one species of plants, most of which were accompanied by botanical descriptions in French. His extraordinary account of this visit resulted in a 306-page manuscript entitled Voyage aux Isles Canaries ou journal des observations physiques, mathematiques, botaniques e historiques faites par ordre du sa Majesté. Unfortunately, this study was not published at the time, and the undoubted scientific impact it would have made was lost. It has, however, recently been published (with a Spanish translation and a facsimile of the original handwritten document) by Herrera Piqué (2006b).

1776–1779: FRANCIS MASSON AND THE FIRST MODERN STUDIES OF THE MACARONESIAN FLORA

In this section, we jump forward nearly three-quarters of a century to focus on the contribution Francis Masson (1741–1805) made to the knowledge of the Macaronesian flora. This Scottish plant collector is a very significant figure in the botanical history of the region, and his contributions as a plant hunter marked the beginnings of modern studies of Macaronesian plants (Francisco-Ortega et al. 2008, 2009). Masson was the first official collector of Kew Gardens. He collected extensively in South and North Africa, the Iberian Peninsula, the West

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FIGURE 8.4 Itinerary of Francis Masson during his first trip to the Macaronesian Islands.

Indies, and Macaronesia (Bradlow 1994; Saltmarsh 2003). His collections contributed to the remarkable growth of Kew gardens’s living collections during this period (Desmond 1994). Masson made two trips to Macaronesia. The first one took place between 1776 and 1779, during which he visited three of the archipelagos (Madeira, Azores, and Canaries), using Madeira as the hub for his expeditions in the region (Fig. 8.4). In 1779, he departed to the Lesser Antilles in search of further plants for Kew, though this collecting trip was less successful. His second Macaronesian trip, to Madeira, was brief and took place in 1784 when Masson was collecting in Spain and Portugal. However, it appears that only limited material was shipped home from this visit. Indeed, Aiton (1789) reports only six species—Clethra arborea Aiton (Clethraceae), Euphorbia mellifera Aiton (Myrsinaceae), Heberdenia excelsa (Aiton) Banks ex DC. Picconia excelsa, Rhamnus glandulosa Aiton (Rhamnaceae), and Rubia fruticosa Jacq. (Rubiaceae)—having been sent by Masson in 1784.

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During his first Macaronesian expedition, we are aware of Masson sending sixteen letters to Sir Joseph Banks (1743–1820), one to Carl Linnaeus (1707–1778), one to Linnaeus the younger (1741–1783) and one to William Aiton (1731–1793), who by then was curator at Kew Gardens. The letter sent to Aiton was accompanied by a manuscript on the Natural History of the Island of St. Miguel that was published in the Philosophical Transactions of the Royal Society of London in 1778 (Fig. 8.5; Masson 1778). This was the only article that Masson published on Macaronesia.

FIGURE 8.5 Title page of paper on the natural history of St. Miguel (Azores Islands) published by Francis Masson (1778).

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As with his other expeditions, Masson’s trip was arranged under the patronage of Sir Joseph Banks to whom the bulk of the material that Masson collected (359 accessions in four shipments) was sent. However, through his correspondence and other sources, we know that he also sent material to Linnaeus the elder, Linnaeus the younger, and Nicolaus Jacquin (1727–1817). It is likely that he also sent material to one of Linnaeus’s students, Carl Peter Thunberg (1743–1828), with whom Masson had collected in South Africa in 1773. Our research on Masson’s contribution to the knowledge of the Macaronesian flora has focused on the material sent to Linnaeus and his son. It has, therefore, concentrated on manuscripts and herbarium specimens found in the collections of the Linnean Society of London and of the Swedish Museum of Natural History in Stockholm. The letters sent by Masson to Linnaeus and his son are held at the Linnean Society, and two of them include lists of herbarium material and seeds that were being shipped with the letters. We also examined specimens collected by Masson housed at the Natural History Museum; this institution has the bulk of the material he collected during his expeditions. There are two letters in existence that were sent to Linnaeus from Masson. The first is dated December 28, 1775, and was sent from London (see transcription in Smith 1821). Masson introduced himself and explained that he was forwarding an enclosed package of seeds that had been collected by Linnaeus’s student Anders Sparrman (1748– 1820), which Masson had picked up in South Africa. However, the second letter, dated August 6, 1776 (see Smith 1821), was sent to Linnaeus from Madeira along with a list of twenty-one herbarium specimens that accompanied it. This list has three columns. The first has Masson’s identification (and sometimes a vernacular name); the second has Masson’s habitat and locality information; the third has annotations in the hand of Linnaeus filius (rather than his father). It seems, therefore, that Linnaeus did not study these specimens himself, doubtless because his health was by this time very poor (he was to die a year later); but the specimens were studied by his son, and several of the new species he described were based on this material. In contrast to the material sent to his father, Linnaeus filius received from Masson a more extensive collection that included both seeds (fiftythree accessions) and herbarium specimens (sixty-one accessions). Based on this shipment and the material send to his father, Linnaeus filius described thirty-seven new species for the Macaronesian Islands, which

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were published in Supplementum plantarum (Linnaeus filius 1782). Both the list of seeds and that of herbarium specimens included vernacular names for a few entries. In the seed list, for example, there are references to “Balo” (Plocama pendula Aiton [Rubiaceae]) and “Mocanera” (Visnea mocanera L.f.). The list of herbarium specimens has additional information, and for most of the accessions there are details concerning the collection locality. Several of the entries in the herbarium list were annotated by Linnaeus filius. Masson’s manuscript species names and habitat descriptions evidently had a strong influence on the binomial names subsequently published by Linnaeus filius. Seventeen (46 percent) of the specific epithets given by Linnaeus filius to the new species described by him are those provided by Masson, and the habitat descriptions of 26 (70 percent) of the new species match Masson’s information. A number of other authors also made significant use of Masson’s specimens, contributing a further seventy-one names. Primary amongst these authors are William Aiton, who described sixty-two new Macaronesian taxa in his Hortus Kewensis (Aiton 1789); Charles-Louis L’Héritier (1746–1800) with nineteen new species published between 1788 and 1791; Nicolaus J. Jacquin, with seven new taxa published between 1782 and 1787; and Johann Link (1767–1851), with one new species described in 1819 (Francisco-Ortega et al. 2008). Twenty-seven of the thirty-seven species described by Linnaeus filius for the Macaronesian islands are basionyms for Macaronesian endemics, and six of them have been transferred to genera that are endemic to Macaronesia, demonstrating the taxonomic value of the material collected by Masson.

CONCLUSION: 1832—EUROPEAN EXPLORERS AND CHARLES DARWIN

We argue that the early “Enlightenment” explorers of the Macaronesian region set the scene for Western botany and horticulture’s continued fascination with Macaronesia, and later with the flora of oceanic islands in general. Subsequent to Masson’s trip to Macaronesia, a number of wellknown European naturalists visited the islands in the eighteenth and nineteenth centuries inspired by the accounts of these early visitors (Herrera Piqué 2006a), most notably Alexander Von Humboldt who stopped in Tenerife (June 19–25, 1799) during his famous trip to the New World.

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Humboldt’s writings in his Personal Narrative (Humboldt and Bonpland 1907) had a major impact on Charles Darwin. In his autobiography, Darwin indicated that few other books had influenced him as much as this one (Darwin 1929). Indeed, Darwin states, “I copied out from Humboldt long passages about Teneriffe, and read them aloud.” We also know that Humboldt was familiar with the accounts on the natural history of these islands provided by explorers such as Christian Leopold Von Buch (1774–1853), Jean Charle Borda (1733–1799), Pierre Louis Antoine Cordier (1777–1861), and Auguste Broussonet (1761–1807) (Hernández González 1995). Most of these visitors (e.g., Bory de Saint-Vincent 1803; Buch 1819, 1825) linked their accounts to those provided by other naturalists such as Masson, Feuillée, Daniel Solander (1733–1782), or Joseph Banks who had traveled to the islands much earlier. Such was Darwin’s interest in visiting and learning about the Canaries that, together with some of his Cambridge friends, he planned to sail from England to the islands in June 1832 (Porter 1985). Darwin started learning Spanish and contacted a merchant in London to inquire about ships (Darwin 1929). He wrote, “I never will be easy till I see the peak of Teneriffe and the great Dragon tree. . . . I have written myself into a Tropical glow” (April 28, 1831, letter to Caroline Darwin in Burkhardt and Smith 1985). However, the trip was canceled because Marmaduke Ramsay (1795–1831), one of the potential participants in this expedition, died unexpectedly in Scotland on July 31, 1831. Shortly after this tragic loss, Darwin received, on August 29, 1831, the invitation to join the Beagle expedition (Desmond and Moore 1991). Darwin was familiar with some of the remarkable plants of the Canary Islands from studying with Rev. John S. Henslow (1796–1861) at the University of Cambridge Botanical Garden. Henslow, who was fascinated by island floras, never visited any islands. Through his teachings, however, he introduced Darwin to the influential phytogeographic work of De Candolle (J. Parker, pers. comm.). The plants that Henslow and Darwin studied may have been the direct descendants of collections made by Masson or Simmons. Interestingly, it is believed that Henslow also encouraged Rev. Richard Lowe (1802–1874), author of the first comprehensive flora of Madeira (Lowe 1857–1872), to make his first trip to this island in 1826, where he eventually settled between 1827 and 1871 (Nash 1990). It also appears that Henslow recommended Lowe to receive the scholarship from Cambridge University that supported his first visit to Macaronesia (Nash 1990). Lowe sent two letters to Darwin in 1854 and 1856 (Burkhardt and Smith 1990, 1991). However, Darwin

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joined the “magic circle” of Henslow at Cambridge after Lowe had left Britain (Nash 1990). Clearly, important European naturalists were influenced by the accounts of the natural history of Macaronesia provided by the many visitors who traveled to the region from the seventeenth century onward. Unfortunately, Charles Darwin could not land on Tenerife when he passed near the island on January 6, 1832. The Beagle was prohibited from entering the port of Santa Cruz without a period of quarantine for several days because of a cholera outbreak in England. In a letter sent to his father from Bahia (Brazil) dated February 8–March 1, 1832, Darwin writes, “We were becalmed for a day between Teneriffe & the grand Canary & here I first experienced any enjoyment: the view was glorious. The peak of Teneriffe—was seen amongst the clouds like another world.—Our only drawback was the extreme wish of visiting this glorious island” (Burkhardt and Smith 1985). Oceanic islands continue to fascinate us. As scientists we walk in the footsteps of those great historical collectors who first documented these extraordinary places. Today our responsibility is to advance that historical heritage by studying and conserving the unique biota of islands.

Acknowledgments

This study has been funded by the Royal Society, ICIA, Fairchild Tropical Botanic Garden, the Ministry of Science and Education of Spain, and the Natural History Museum, London. We have also received considerable logistical support from staff and colleagues at the British Library, the libraries of the Botany Department of the Natural History Museum (London) and of the Linnean Society of London, Uppsala University, and the Swedish Museum of Natural History in Stockholm. During the summer of 2008, Javier Francisco-Ortega received grant support from the Louis J. Skinner Foundation to conduct biodiversity studies of island plants. This grant was awarded to Fairchild Tropical Botanic Garden through the support and effort of Ronald Herzog, José R. Garrigó, and Mike Maunder. A grant from the North America Incoming Short Visits Program of the Royal Society (International Short Visits—North America—2006/R1) to Charlie E. Jarvis provided funds for Javier Francisco-Ortega to visit the Natural History Museum, London. John Parker provided biographical information on Charles Darwin. This is contribution number 103 from the Tropical Biology Program of Florida International University.

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REFERENCES Aiton W. 1789. Hortus kewensis or, a catalogue of the plants cultivated in the Royal Botanic Garden at Kew. 3 volumes. London: George Nicol. Allan M. 1964. The Tradescants. Their plants, gardens and museums 1570–1662. London: Michael Joseph. Allen D.E. 2004. “Plukenet, Leonard (bap. 1642, d. 1706)” Oxford Dictionary of National Biography. Oxford: Oxford University Press. Andrews K.R. 1984. Trade, plunder and settlement. Maritime enterprise and the genesis of the British Empire, 1480–1630. Cambridge: Cambridge University Press. Bory de Saint-Vincent J.B.G.M. 1803. Essais sur les îles Fortunées et l’Antique Atlantide ou Précis de l’histoire de l’Archipel des Canaries. Paris: Author. Bradlow F.R. 1994. Francis Masson’s account of three journeys at the Cape of Good Hope 1772–1775. Cape Town: Tablecloth Press. Bretschneider E. 1881. Early European researches into the flora of China. J.N. China Branch Roy. Asiat. Soc. 16: 1–194. Brooks E. St. J. 1954. Sir Hans Sloane: The great collector and his circle. London: Batchworth Press. Buch L. von. 1819. Allgemeine Uebersicht der Flora auf de Canarischen Inseln. Abhandl. Königlichen Akad. Wissensch. Berlin 1816–1817: 337–384. Buch L. von. 1825. Physicalische Beschreibung der Canarischen Inseln. Berlin: Druckerei der Koeniglichen Akademie. Burkhardt F., Smith S. 1985. The correspondence of Charles Darwin: Vol. 1. 1821–1836. Cambridge: Cambridge University Press. Burkhardt F., Smith S. 1990. The correspondence of Charles Darwin: Vol. 5: 1851–1855. Cambridge: Cambridge University Press. Burkhardt F., Smith S. 1991. The correspondence of Charles Darwin: Vol. 6: 1856–1857. Cambridge: Cambridge University Press. Caygill M. 1994. Sloane’s will and the establishment of the British Museum. In: MacGregor A., editor. Sir Hans Sloane: Collector, scientist, antiquary—founding father of the British Museum. London: British Museum Press pp. 45–68. Clusius C. 1576. Rariorum aliquot stirpium per Hispanias observatarum historiae. Antwerp: Plantin. Cox E.H.M. 1945. Plant-hunting in China. A history of botanical exploration in China and the Tibetan marches. London: Collins. Dandy J.E. 1958. The Sloane Herbarium. London: Trustees of the British Museum. Darwin F. 1929. Autobiography of Charles Darwin. London: Watts. Desmond A., Moore J. 1991. Darwin: The life of a tormented evolutionist. New York: Warner Books. Desmond R. 1994. The transformation of the Royal Gardens at Kew. In: Banks R.E.R., Elliot B., Hawkes J.G., King-Hele D., Lucas G.L., editors. Sir Joseph Banks: a global perspective. Richmond: Royal Botanic Gardens, Kew pp. 105–212. Francisco-Ortega J., Santos-Guerra A. 1999. Early evidence of plant hunting in the Canary Islands from 1694. Arch. Nat. Hist. 26: 239–267. Francisco-Ortega, J., Santos-Guerra A., Carine M.A., Jarvis C.E. 2008. Plant hunting in Macaronesia by Francis Masson: the plants sent to Linnaeus and Linnaeus filius. Bot. J. Linn. Soc. 157: 393–428.

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Francisco-Ortega J., Santos-Guerra A., Carine M.A., Jarvis C.E. 2009. Francis Masson y los primeros estudios taxonómicos modernos de la flora Macaronésica. El Indiferente. 20: 2–11. Francisco-Ortega J., Santos-Guerra A., Jarvis C.E. 1994. Pre-Linnaean references for the Macaronesian flora found in Leonard Plukenet’s works and collections. Bull. Nat. Hist. Mus. London, Bot. 24: 1–34. Hartog E. D., Teune C. 2002. Gaspar Fagel (1633–88): His garden and plant collection at Leeuwenhorst. Gard. Hist. 30: 191–205. Hernández González M. 1995. Estudio preliminar. In: Hernández González M., editor. Alejandro Humboldt: Viajes a las Islas Canarias. La Laguna, Canary Islands, Spain: Francisco Lemus pp. 9–28. Herrera Piqué A. 2006a. Pasión y aventura en la ciencia de las luces. Vol. 1. Introducción a la exploración científica de las Hespérides 1700–1850. Las Palmas de Gran Canaria, Spain: Cabildo de Gran Canaria. Herrera Piqué A. 2006b. Pasión y aventura en la ciencia de las luces. Vol. 2. Observaciones científicas realizadas por el astrónomo y naturalista Louis Feuillée en las Islas Canarias, año 1724. Las Palmas de Gran Canaria, Spain: Cabildo de Gran Canaria. Humboldt, A. von, Bonpland A. 1907. Personal narrative of travels to the equinoctial regions of America during the years 1799–1804. Vol. 1 (Translated and edited by T. Ross, original French version). London: George Bell & Sons. Humphries C.J. 1976. A revision of the Macaronesian genus Argyranthemum Webb ex Schultz Bip. (Compositae–Anthemideae). Bull. Brit. Mus. (Nat. Hist.), Bot. 5: 145–140. Linnaeus filius C. 1782. Supplementum plantarum systematis vegetabilium. Braunschweig, Germany: Impesis Orphanotrophei. Lowe R.T. 1857–1872. A manual flora of Madeira and the adjacent islands of Porto Santo and the Desertas. Two Volumes. London: John van Voorst. MacGregor A. 1994. The life, character and career of Sir Hans Sloane. In: MacGregor A., editor. Sir Hans Sloane: Collector, scientist, antiquary—founding father of the British Museum. London: British Museum Press pp. 11–35. Mason P. 2006. A dragon tree in the Garden of Eden. J. Hist. Collect. 18: 169–185. Masson F. 1778. An account of the island of St. Miguel. Philos. Trans. R. Soc. Lond. 68: 602–610. McClain M. 2001. Beaufort: The Duke and his Duchess, 1657–1715. New Haven, CT: Yale University Press. Menezes de Sequeira M., Santos-Guerra A., Jarvis C.E., Oberli A., Carine M.A., Maunder, M., Francisco-Ortega J. 2010. The Madeiran plants collected by Sir Hans Sloane in 1687, and his descriptions. Taxon. 59: 598–612. Morales Lezcano V. 1970. Relaciones mercantiles entre Inglaterra y los archipiélagos del Atlántico Ibérico. Su estructura y su historia (1503–1783). La Laguna, Canary Islands, Spain: Instituto de Estudios Canarios, Universidad de La Laguna. Nash R. 1990. Scandal in Madeira: The story of Richard Thomas Lowe. Sussex: Book Guild. Paz-Sánchez M. de. 2004. Un drago en El Jardín de las Delicias. In: Paz-Sánchez M. de, editor. Flandes y Canarias. Nuestros orígenes nórdicos, Vol. I. Santa Cruz de Tenerife, Spain: Centro de la Cultura Popular Canaria pp. 13–109.

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Petiver J. 1695–1703. Musei Petiveriani centuria prima [- decima]: Rariora Naturæ continens: Viz. Animalia, Fossilia, Plantas, ex variis mundi plagis advecta, ordine digesta, et nominibus propriis signata. London: S. Smith and B. Walford. Plukenet L. 1691–1694. Phytographia sive illustriorum. Pars prior—Pars quarta. London: Author. Plukenet, L. 1696. Almagestum botanicum sive phytographiae Pluc’netianae. London: Author. Plukenet, L. 1700. Almagesti botanici mantissa. London: Author. Plukenet, L. 1705. Amaltheum botanicum. London: Author. Porter D.M. 1985. The Beagle collector and his collectors. In: Kohn D., editor. The Darwinian heritage. Princeton, NJ: Princeton University Press pp. 973– 1019. Potter J. 2006. Strange blooms: The curious lives and adventures of the John Tradescants. London: Atlantic Books. Puig-Samper, M.A., F. Pelayo. 1997. El viaje del astrónomo y naturalista Louis Feuillée a las Islas Canarias (1724). La Laguna, Canary Islands, Spain: Centro de la Cultura Popular Canaria, Ayuntamiento de La Laguna. Riley M. 2006. The club at the Temple House revisited. Arch. Nat. Hist. 33: 90–100. Sánchez-Pinto L. 2001. El gigante de Arautava. El Indiferente 12: 17–21. Santos-Guerra A. 1993. La botánica canaria y los prelinneanos (segunda mitad del siglo XVII y primera del XVIII). In: Anonymous, editor. I encuentro de geografía, historia y arte de la ciudad de Santa Cruz de La Palma. Santa Cruz de La Palma, Spain: Cabildo Insular de La Palma pp. 205–212. Saltmarsh A.C. 2003. Francis Masson: Collecting plants for king and country. Curtis’s Bot. Mag. 20: 225–244. Sands M. 1950. The gardens of Hampton Court: Four centuries of English history and gardening. London: Evans Brothers. Sloane H. 1696. Catalogus plantarum quae in insula Jamaica sponte proveniunt. London: D. Brown. Sloane H. 1707. A voyage to the islands Madera, Barbados, Nieves, S. Christopher and Jamaica. Vol. 1. London: Author. Sloane H. 1725. A voyage to the islands Madera, Barbados, Nieves, S. Christopher and Jamaica. Vol. 2. London: Author. Smith J.E. 1821. A selection of the correspondence of Linnaeus and other naturalists from the original manuscript. Vol. 2. London: Longman. Sousa J.J. de 1994. História rural da Madeira: A colónia. Funchal Madeira, Portugal: Direcção Regional dos Assuntos Culturais. Tradescant J. the younger. 1656. Musaeum Trandescantianum or, a collection of rarities preserved at South Lambeth, neer London. London: John Grismond. Wijnands D.O. 1983. The Botany of the Commelins. Rotterdam: A.A. Balkema. Zwaan M.S.-D. 2002. Magdalena Poulle (1632–99): A Dutch lady in a circle of botanical collectors. Gard. Hist. 30: 206–220.

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NINE

Olivier Rieppel

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The school of biological systematics known as cladistics is notorious for drawing a distinction between pattern and process (Nelson and Platnick 1981; Beatty 1982). The pattern is one of relative degrees of relationships, the process is one of species lineages splitting and splitting again. A cladogram potentially has two interpretations (Platnick 1977). If the nodes in the cladogram are taken to be speciation events, and the internodes to be stem species, then the cladogram is isomorphic with a phylogenetic tree. If the cladogram is taken to represent a hierarchy of relative degrees of relationships that can also be represented in a Venn diagram (i.e., as a system of sets within sets), then the cladogram can be taken as a basis for classification, Linnaean or otherwise. Hull (1988: 101) argued that a branching diagram and a corresponding classification could indicate common ancestry or phylogenetic relationship, but not both. Phylogenetic relationships are expressed as a phylogenetic tree, which is a system of species lineages splitting and splitting again. The result is a “division hierarchy” that does not specify relations of inclusiveness. Relative recency of common ancestry is indicated by an inclusive hierarchy of groups within groups, the more inclusive groups sharing a more distant ancestry than the included, less inclusive groups.

Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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In 1992, P. A. Williams “suggested that some major problems found in cladism stem from a confusion inherent in its philosophy.” Specifically, she (Williams 1992: 151) claims to “have demonstrated that the divisional ‘hierarchy’ and the Linnaean hierarchy are different types of ‘hierarchy,’” that “Hennig conflated the two types of ‘hierarchy’ and, in so doing, made the school of biological taxonomy known as ‘cladism’ philosophically confused.” Cladists naturally responded that the confusion is located in philosophy, not in cladism (D. M. Williams et al. 1996: 134): “there is little excuse for philosophers, when it is their job to enlighten their readers rather than to obfuscate the issues. At the very least, philosophers should attempt to understand the arguments of cladists rather than depend on the views of their critics.” One of the authors whom cladists (D. M. Williams et al. 1996) found to be critical of their program is Hull (1988), who in turn was acknowledged by P. A. Williams (1992: 152) for having clarified some of the issues she was dealing with when writing her paper. Indeed, Hull (1988: 101) stated, “Although diagrams representing phylogenetic trees and the arrangements of taxonomic names in classifications might appear to be related to each other in a systematic and straightforward way, this appearance is extremely deceptive.” The question thus arises whether P. A. Williams’s (1992: 151) claim that “the only way to eliminate the confusion and problems from cladism is to eliminate cladism as a school of biological taxonomy” is based on a mere misunderstanding, or whether some deeper issue is at stake in this debate.

THE TWO HIERARCHIES

P. A. Williams (1992) located the confusion in cladistics in Hennig’s (1966) allegedly mistaken interpretation of Gregg’s (1954) analysis of the Linnaean hierarchy in the light of Woodger’s (1952) work. Indeed, referring to Woodger’s (1952) and Gregg’s (1954) analysis of the nature of a hierarchy, Hennig (1966: 16–17) asserted, “We consider the investigations of Woodger and Gregg extraordinarily important because they clarify, with methods that exclude all confusion and contradiction, the peculiarities of the hierarchic system.” From the lasting success of a hierarchical representation of biodiversity, Hennig (1966: 20) concluded to some “deeper significance”—namely, that “the phylogenetic system, which corresponds exactly to this hierarchic type, is . . . indeed the general reference system of biology that we have been seeking.” Hennig here

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invokes a “hierarchic type,” which presumably implies that there are different types of hierarchies, of which one type is best suited to represent genealogy. In his 1950 book, at a time before he was acquainted with the work of Woodger (1952) and Gregg (1954; see Hennig 1957), Hennig (1950: 20) raised the question whether “the fact that similarity relations which exist between two discrete [numerically different] natural things . . . are best represented by a hierarchical system of groups, is in itself enough already to prove the historical development of those things, i.e., whether in this case the conclusion ‘hierarchy of similarity relations = division hierarchy’ (Woodger see Bertalanffy 1931 [sic], I, p. 265ff) is justified” (my translation). In other words, Hennig (1950) raised the question of whether it is justified to identify the hierarchy of similarity relations with the “division hierarchy” (Teilungshierarchie) that was formulated by Woodger (1930a, 1930b, 1931) and discussed by Bertalanffy (1932), the latter being the source for Hennig’s (1950) discussion. P. A. Williams (1992) located Hennig’s (1966) confusion in his attempt to equate the division hierarchy with the Linnaean hierarchy. She interpreted the Linnaean hierarchy, one that can be represented by nested boxes (P. A. Williams 1992, fig. 1), as an atemporal inclusive hierarchy of groups within groups. As was discussed by Hull (1988: 397–401), such a hierarchy can be treated as a part-to-whole as well as a class-inclusion hierarchy, depending on what metaphysics one accepts for biological (historical) entities (taxa). The division hierarchy, in contrast, cannot be represented by nested boxes, as it “nowhere expresses inclusion relationships” (P. A. Williams 1992: 140). Instead, “the divisional ‘hierarchy’ in biology is a linear, temporal, phylogenetic tree” (P. A. Williams 1992: 145). Yet, it was Woodger’s (1952: 11) stated intention to “reach a purely abstract definition of hierarchy” that would capture a system of squares divided into squares, a zygote dividing and the resulting cells dividing again, as well as the Linnaean system. A zygote dividing and the resulting cells dividing again certainly yields a “division hierarchy,” but whereas for P. A. Williams (1992) the Linnaean hierarchy is a different one, Woodger (1952) intended his definition of “hierarchy” to apply to both of them. Woodger (1952) interpreted as a mereological sum the “division hierarchy” that obtains from the repeated subdivision of a square: “draw a square on a piece of paper, bisect each side, and join the middle points of opposite sides to produce four smaller squares. If ‘X’ names each of these smaller squares, then ‘3’ names that larger square of which they are parts” (Wooder 1952: 11). Hennig (1950), who took his clues from

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M R M m

W M

m M m R m FIGURE 9.1 The graphical expression on a division hierarchy, as it results from subdividing a square into four parts, and subdividing these parts again. See text for further discussion.

Bertalanffy (1932: 264f), found there the following interpretation of this abstract hierarchy: call the singular square “W,” and the smaller squares (i.e., its parts) “M”; then M stands to W in the relation “R = to be a quarter of”; M itself has parts “m” that stand in the same relation R to M. A graphical expression of Woodger’s (1952) example (Fig. 9.1) would be four one-directional relation arrows running from W to each of the four M’s, and four one-directional relation arrows running from M to the four m’s, etc. (see Gregg 1954: fig. 2.5; Hennig 1957: fig. 1; 1966: fig. 2). Bertalanffy (1932: 265ff.) found this type of hierarchy to be often realized in biology. The first is the division hierarchy exemplified by the zygote dividing and the resulting cells dividing again. In this case, the relation R is named “to be an immediate cellular descendant of.” The second case is the “spatial hierarchy,” which is the organism represented by the totality of its cells at any specific point in time. The relation R in which its organs stand to the whole organism is called “organic relation.” The third hierarchy is the “genetic hierarchy,” which starts from the zygote and proceeds to the F1, F2, etc., generations: here, the relation R is called “to be an immediate descendant of.” The problem is, however, that the zygote comes into being by the fusion of two gametes. Hence, in the case of bisexually reproducing organisms, the genetic hierarchy is really only part of a reticulated system.

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The relation “to be an immediate descendant of” is evidently the one that Hennig (1950, 1966) found most relevant, but he extrapolated it from the (onto-)genetic to the phylogenetic hierarchy (Günther 1956). On Gregg’s (1954) interpretation of Woodger’s (1952) hierarchy, a onedirectional relation arrow r connecting two discrete entities, A and B, symbolizes an ordered pair r(A, B). Following Woodger (1952) and Gregg (1954), Hennig (1957, 1966) defined monophyly as a relational concept. For a stem species A, and its two descendant species B and C, the relation r (“to be an immediate descendant of”) marks out the monophyletic taxon Tax in terms of a set that includes two ordered pairs: Tax = r {(A, B) (A, C)} (for a more detailed discussion, see Rieppel 2007). Limiting speciation to a dichotomous splitting of the ancestral lineage, as was done by Hennig (1950, 1966), the monophyletic taxon Tax thus includes the ancestor and all, and only, its descendants. The hierarchy of monophyletic taxa is therefore an inclusive one, yet it is based not on intrinsic properties of taxa (as the traditional Linnaean hierarchy is) but on relational properties instead. On Gregg’s (1954) interpretation of Woodger’s (1952) definition of hierarchy, the division hierarchy can thus be represented by an inclusive system of groups within groups. The classical Linnaean system is, indeed, a class inclusion hierarchy (or was interpreted as such: Buck and Hull 1966), but Hennig (1966) reinterpreted it as a part-to-whole hierarchy, a metaphysical move that was licensed by Gregg (1954: 70). A system of sets (of ordered pairs) within sets (of ordered pairs) “is converted to a part/whole hierarchy. . . . Although the change is metaphysically quite drastic, it does not alter any traditional inferences” (Hull 1988: 399). The confusion identified by P. A. Williams (1992) seems not to be Hennig’s interpretation of the Linnaean hierarchy, who was in fact ready to replace it with a ranking system based on indentation (Hennig 1965: 98). But there certainly is a difference between an inclusive system of natural groups and an exclusive “hierarchy” of splitting lineages: Amniota includes Mammalia—every mammal is also an amniote. But whereas the ancestral (stem) species is included in the monophyletic taxon that is constituted by it and all and only its descendants, a descendant species is not included in the ancestral species. It is this asymmetry between descent (of one species from another) versus ancestry (of a monophyletic taxon) that P. A. Williams (1992) found confusing. “Descent” connotes a process (of lineage splitting); “ancestry” connotes a pattern (a hierarchy of monophyletic taxa). The confusion, it seems, stems from the application of the concept of monophyly as defined earlier to evolving species.

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P. A. Williams (1992) worked out the contrast between the inclusive Linnaean hierarchy and the division hierarchy at the interface between the species level and supraspecific levels of biological organization. On the Linnaean scheme, species group into genera, those into families, these into orders, and so forth. In contrast, the divisional scheme “is a historical representation of species dividing producing more species” (P. A. Williams 1992: 141). Bertalanffy (1932) recognized that the divisional genetic hierarchy of bisexually reproducing organisms really forms part of a network because the zygote forms by the fusion of two gametes. Hennig (1966: fig. 4) similarly distinguished phylogenetic relationships at supraspecific levels from reticulating tokogenetic relationships at the species or population levels. In a tokogenetic system, any individual organism can be related to any other by more than one relation-arrow (Hennig 1966: fig. 4): the relation is many-many. In contrast, a division hierarchy such as the phylogenetic system has a “beginner” (Gregg 1954), which Hennig (1966) took to be the ancestral (stem) species: several relationship arrows (Hennig allowed for only two) can originate from the beginner, but none can point toward the beginner: the relation is one-many (see Hennig 1966: fig. 2, taken from Gregg 1954: fig. 2.5). The web of relationships that ties together populations of sexually reproducing organisms cannot be represented by a phylogenetic system; the concept of monophyly as defined here cannot be applied to species (of bisexually reproducing organisms). Following Woodger (1952), and Gregg (1954), the hierarchy of monophyletic taxa requires a unique “beginner”—that is, a unique ancestor (stem species)—such that “sexually reproducing organisms [cannot] fulfill Woodger’s criteria” (Wheeler and Platnick 2000a: 141). The crucial transition is where tokogenetic relationships are disrupted and phylogenetic relationships become established. “Without a boundary to the reticulating networks, there can be no nested hierarchy and no monophyly” (Goldstein and DeSalle 2000: 370). On this account, monophyly is strictly a phylogenetic concept that cannot be applied to tokogenetic systems, such as species (Willmann 1983, 1985). Goldstein et al. (2000: 127) noted that the methods used in cladistic analysis will always retrieve a hierarchical pattern, such that “phylogenetic interpretations of cladistic analysis depend fundamentally on the presence of an underlying hierarchy to begin with”1 (see also Nixon and Wheeler 1990; Davis and Nixon 1992; Wheeler and Platnick 2000b). Relationships such as those among parents, children, and cousins in sexual populations cannot be depicted unambiguously as a nested hierarchy (Luckow 1995). The conclusion must be that the concept of monophyly as defined here cannot

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be applied to species or subspecific levels of biological organization. This reveals a fundamental asymmetry in Hennig’s (1950, 1966) phylogenetic system, with species on the one side and supraspecific taxa on the other (Goldstein and DeSalle 2000). HOW CLADISTS LOST THE SPECIES CATEGORY

The unification of Hennig’s (1950, 1966) system is certainly an ideal for many cladists. If species are taxa, and taxa are monophyletic, then species must be monophyletic (Rosen 1979). Add to this the lure of the pattern. Many cladists, but also comparative (“systematist”: Naef 1919) morphologists, have argued that pattern analysis (reconstruction) has epistemological, as well a logical, precedence over process explanation (for a review, see Rieppel 2004, 2006): “No patterns, nothing to explain by invoking one or another concept of process. In short, a process is that which is the cause of a pattern. No more, no less” (Nelson and Platnick 1981: 35). In his 1981 Hennig Society lecture, Colin Patterson praised the fact that “pattern cladism” severs all connections with evolutionary biology, “where nothing seems accessible to investigation and test. Instead fantasy is free to wander” (Patterson, unpublished manuscript). As I understand it, cladistics is theoretically neutral so far as evolution is concerned—it has nothing to say about evolution, and no knowledge of evolution or belief in it is necessary to do cladistic analysis. All cladistics demands is that groups have characters and that groups are non-overlapping, (Patterson, unpublished manuscript; but see my note 1)

A scientific realist attitude toward species and evolutionary theory takes species to be historical entities causally grounded (in terms of replicators and interactors) in the evolutionary process (Hull 1989). Divorcing pattern analysis from the evolutionary process renders species simply “the smallest detected samples of self perpetuating organisms that have unique sets of characters” (Nelson and Platnick 1981: 12). This position naturally engenders instrumentalism about species. Among the earliest proposals to remove the asymmetry between tokogenetic systems (species) and phylogenetic systems (a hierarchy of monophyletic taxa) ranks that of Hill and Crane (1982: 308), who asserted that “a species is recognized and distinguished from others by autapomorphy. . . . For convenience of discussion such a cladistic species can be termed a ‘cladistically resolved unit’ (CU) . . . there is no necessary congruence between such a CU and real species.” “Real species” are presumably the tokogenetic systems of reproductive communities

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that exist in nature, as opposed to the CUs, which are operational units convenient for classificatory purposes (Hill and Crane 1982: 309). Some continued to pursue the project to seek a biologically relevant conception of species as the basic unit of evolution, but one that can also be accommodated by cladistic analysis. For Nixon and Wheeler (1990: 218; see also Wheeler and Platnick 2000b: 58; Wheeler 2004), such a phylogenetic species concept defines species as “the smallest aggregation of populations (sexual) or lineages (asexual) diagnosable by a unique combination of character states in comparable individuals (semaphoronts).” Others have brushed the species category away because “for a consistent, general reference classification system, all taxa must be of the same type [i.e., monophyletic]; species should be regarded as simply the leastinclusive taxon in the system” (Mishler 1999: 307; see also Mishler and Donoghue 1982). The view of species as simply the least inclusive (monophyletic) taxon has received particular support from some of the architects of the PhyloCode (Cantino and de Queiroz 2007). The problems created by the species category for this program are notorious: “A discussion of species nomenclature is conspicuous in its absence from the current draft of the PhyloCode . . . there is disagreement on whether or not species should be considered ‘biological entities’ distinct from clades, and several authors have suggested that the status of species as a special biological ‘entity’ be abandoned” (Dayrat et al. 2004: 485; but see the most recent discussion of this topic by Dayrat et al. 2008). Pleijel (1999: 756) has been particularly supportive of the abandonment of the species category: “species should not be recognized as taxa.” Pleijel (1999: 759) acknowledged the asymmetry between tokogenetic species and monophyletic taxa, which is precisely what motivated his rejection of species: “I here advocate that species entities should be disregarded, and not used in taxonomy. . . . Taxon names are . . . restricted to monophyletic groups and the word species loses its meaning: In the presence of synapomorphies we describe taxa, in the absence of apomorphies, we don’t” (Pleijel 1999: 759). Referring back to Mishler’s (1999) conception of “species,” Pleijel and Rouse (2000a) formally introduced the “least-inclusive taxonomic unit” (LITU) as the basal unit based on synapomorphy that is to be recognized by the PhyloCode. We . . . suggest that taxa should always constitute the same kind of entities; named monophyletic groups which are identified by unique shared similarities (apomorphies). . . . This . . . will lead away from . . . the view as species being some kind of basic comparable units in biodiversity and evolution. (Pleijel and Rouse 2000a: 629)

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De Queiroz and Donoghue (1988: 331) already discussed which kinds of “groups” (historical entities) might be conceptualized as “the smallest (least inclusive) monophyletic groups,” but Pleijel and Rouse (2000b: 165) recommend a more instrumentalist perspective: “When labeling a taxon as a LITU it should be emphasized that this is a statement, not about group inclusiveness or lack of internal nested structure, but about our current state of knowledge.” The identification of LITUs thus serves nothing but the identification of taxa that on the basis of current knowledge contain no other taxa (Pleijel and Rouse 2003: 169). The species category has thus succumbed to ignorance, or, more technically, the species category has been discarded because of “lack of consensus [and] lack of empirical connotations” (Pleijel 1999: 759).

DNA AS AN INSTRUMENT FOR SPECIES RECOGNITION

That there can be causally integrated systems in nature (populations, demes, species) that lack autapomorphies (synapomorphies) is wellknown (Nixon and Wheeler 1990). These nonmonophyletic entities are the “metaspecies” of Donoghue (1985; see also de Queiroz and Donoghue 1988; Baum 1992; Baum and Shaw 1995), the “plesiospecies” of Olmstead (1995), or the “ferrespecies” of Graybeal (1995). The concept of recognizing nonmonophyletic yet causally integrated (through replication and interaction) entities is consistent with the fact that species cannot be both monophyletic and ancestral (e.g., Sober 1992). But how, then, are we to recognize, identify, and reidentify these entities in the absence of autapomorphy (synapomorphy)? The instrumentalist turn in systematics that is reflected in the loss of the species category in cladistics has carried over into biodiversity research that tries to recover biologically relevant taxonomic units on the basis of DNA sequence data. The currency of instrumentalist phylogeography and conservation biology is no longer the realist species concept (a causally integrated system stretching through space and time: Hull 1989): “A contrasting view . . . is a recognition of more or less distinct clusters of organisms at varying biological scales, without assuming some fundamental and universal level of clustering that has evolutionary significance out of proportion to all other levels of clustering” (Hendry et al. 2000). Such a “cluster of organisms” has been called an “evolutionary significant unit” (ESU; Waples 1991), or a “molecular operational taxonomic unit” (Blaxter et al. 2005).

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One way to identify such “sequence clusters” is through DNA barcoding: while superficially appealing, the term should not imply that each species has a fixed and invariant genetic code similar to a barcode on a supermarket product (Moritz and Cicero 2004). But then, species are not necessarily the issue: “We are agnostic as to whether the taxa we can define using these barcode sequences (which we call ‘molecular operational taxonomic units’ or MOTU) are ‘species’ or not” (Blaxter et al. 2005: 1936). The concept of an evolutionary significant unit is more ambitious. Broadly defined, ESUs are “entities that are on largely independent evolutionary trajectories” (Hey et al. 2003: 600). Operationally, ESUs “should be reciprocally monophyletic2 for mtDNA alleles and show significant divergence of allele frequencies at nuclear loci” (Moritz 1994: 373). This operational definition renders ESUs complementary to species, rather than replacing them (Moritz 1994: 372). DNA barcoding is a relatively uncontroversial method for rapid species identification. “In its strictest sense, DNA barcoding addresses only a limited aspect of the taxonomic process, by matching DNA sequences to ‘known’ species, the latter being delimited with traditional (e.g., morphological) methods. In this context, the role of barcodes is to provide a tool to assign unidentified specimens to already characterized species” (Savolainen et al. 2005: 1807). But ambitions quickly grew, as Savolainen et al. (2005: 1807) continue: “it is a widely accepted fact that species, however defined, are variable for most DNA markers. . . . Therefore, an obvious contribution that barcoding is making to taxonomy is helping to discover cryptic species.” Moritz and Cicero (2004) advocate the use of barcoding to assign unknown individuals to species, and to enhance the discovery of new species. Hebert et al. (2003: 314) find “barcodes sensitive enough not only to identify species, but also ‘phylogeographic groups’ within species,” such as ESUs. But how, then, can such “phylogeographic groups” be distinguished from genuine species on the basis of barcodes? “The success of the barcoding approach depends either on the strength of the claim that interspecific variation exceeds intraspecific variation by an order of magnitude, thus establishing a ‘barcoding gap,’ or on the reciprocal monophyly of species . . . our data show the lack of a barcoding gap” (Wiemers and Fiedler 2007). Indeed, “with the increasing resolution of molecular techniques, significant differentiation can be found at very small scales, even down to the individual” (Crandall et al. 2000: 290). Brower (2006: 131) emphasized: Funk & Omland (2003) found that some 23% of animal species . . . are polyphyletic as implied by their mtDNA. If this is a general pattern, it

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means that even under the best of circumstances, a circumscription of terminal clusters as species based on DNA barcoding will be ambiguous or wrong in about a quarter of the time (Meyer & Paulay 2005).

Whether or not a barcoding gap exists in any given case study is a purely empirical matter. Whether a barcoding gap—if it exists in any given case study—separates species, cryptic species, or reciprocally monophyletic phylogeographic groups is a theoretical (conceptual) matter. Wheeler (2004: 576) concluded that “DNA barcoding is an extremely exciting and potent tool for making species identifications but it is a poor approach to species discovery and description,” because it is based on a “theoretically vacuous technology.”

HOW TO GET THE SPECIES BACK

When discussing species realism in the light of the barcoding initiative, a distinction must be drawn between epistemic and metaphysical issues. The barcoding initiative views the DNA barcode as a useful tool for species identification and discovery, a tool whose use, furthermore, can be embedded within an array of other tools (morphology, ecology, behavior) in an effort to let reciprocal illumination guide the process of species identification and discovery (Smith et al. 2008). Whether to use DNA barcodes for species identification and discovery is an epistemological issue. Whether the “species” so discovered are considered to constitute real entities in nature (the realist claim, as argued, for example, by Hull 1989), or whether they are considered to merely be groupings that most adequately reflect current knowledge (the instrumentalist claim, as argued, for example, by Wiens et al. 2008) is a metaphysical issue. The controversy over these latter positions is well reflected in the current debate about a possible “inflation of species” in contemporary conservation biology, a debate that highlights the role of species concepts in the discovery and description of species (e.g., Isaac et al. 2004; Harris and Froufe 2005; Knapp et al. 2005; Köhler et al. 2005). The tools of species recognition and discovery to one side, it is this conceptual issue that will be addressed in greater detail here. In the philosophy of biology, the term species is a theoretical term (Hull 1989; Ereshefsky 2007), which means a term that refers to unobservables. In contrast, an observation term refers to observables such as the average-sized items of everyday life stocked in the store around the corner. Apple is an observational term; electron is a theoretical term.

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Scientific realism is a position in the philosophy of science, which claims that theoretical terms make an ontological commitment: the claim is that the entities referred to by theoretical terms “really exist.” If we can successfully build an electron microscope, it is because electrons really exist (Hacking 1983). Instrumentalism denies the necessity of an ontological commitment for theoretical terms. For an instrumentalist, scientific theories are instruments that organize contemporary scientific knowledge in a useful way allowing successful predictions (Rosenberg 1994). For a scientific realist, science tracks the truth about the world we live in without being able to take possession of it (Psillos 1999); for an instrumentalist, scientific theories must be empirically adequate in terms of their predictive power (van Fraassen 1980). Species is a theoretical term in the philosophy of biology because we cannot see a species; we can only see possible spatiotemporal parts of species. Nevertheless, most biologists would adopt a realist perspective of species. Evolutionary theory says that species multiply and interact. Speciation makes two (or more) species out of one; an invasive species can drive a native species toward extinction. Replication and interaction (Hull 1989; Sterelny and Griffiths 1999) are causal processes, and causal relations are existence implying: it is hard to imagine nonexistents to enter into causal relations. The claim that species is a theoretical term because we can only see spatiotemporal parts of species thus implies that species are historical entities that stretch through space and time—in short, that species have histories or, indeed, make history (Løvtrup 1977, 1979). The temporal parts of the species that biologists can see are captured by Mayr’s (1963: 17) nondimensional species concept: it is “the species concept of the local naturalist.” The appreciation that species have histories has led to the formulation of a variety of phylogenetic species concepts, starting with Simpson (1961; see also Wheeler and Meier 2000). As was discussed, Hennig’s (1950, 1966) concept of monophyly is not applicable to sexually reproducing species, because these are reticulated, not hierarchically structured systems (Goldstein and DeSalle 2000; Goldstein et al. 2000). Because the cladistic approach misfires at the population level, the barcoding approach might appear more suitable as it is a simple phenetic clustering approach. The goal is to assess variation in ubiquitous genes across different populations, assess that variation quantitatively, and define a certain threshold of dissimilarity that would justify the recognition of different species. Suppose that barcoding technology allows separation of two contemporaneous populations

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by a distinct barcoding gap. Let’s call the populations separated by such a barcoding gap two different “gene species.” This would mean that separate clusters of DNA characters sampled from contemporary populations are used to differentiate two separate species. In such a case, “the DNA sample and its sequence readout would act simultaneously as a key part of the type specimen . . . and as a kind of label for the taxon to which the specimen is deemed to belong” (Mallet and Willmott 2003: 57). This is an interesting quote that deserves careful unpacking. The DNA sample is first invoked as a key part of the type specimen, then as a kind of label for the species represented by the type specimen. The “type specimen method” is a taxonomic convention that requires every description of a new species to designate a type specimen for that species. Perhaps the most important function of the designated type specimen is to ground the meaning of the associated species name (Hull 1988: 497): whatever species a designated type specimen belongs to, this species will always be the referent for the species name that was coined in association with the designation of that type specimen (this holds whether or not the newly coined species name eventually turns out to be synonymous with a previously introduced name). The species name attaches to the species like a tag; the type specimen is the string that attaches the name tag to the species. But for this name to designate a species, the species must be assumed to really exist as a spatiotemporally located, causally integrated entity. Or else there would be nothing to tie the name tag to. According to Mallet and Willmott (2003: 57), the DNA barcode can be thought of as both, part of the type specimen as well as an identifying tag that attaches to the species represented by the type specimen: “In principle, a single DNA sequence is no different from a single unique name for every taxon.” This is the juncture at which “barcoding life” runs into conceptual problems. Contemporary discussions of phylogenetic species concepts (e.g., Wheeler and Meier 2000) take a species to come into existence through its origin in a speciation event and to go extinct when it itself undergoes speciation (or terminal extinction). The lineage that stretches from one speciation event to the next is the species stretching through space and time (de Queiroz 1999). In spite of the fact that such an evolutionary species lineage may undergo anagenetic change, the species name does not change but remains the same. The species name continues to designate this unique evolutionary lineage, individuated by two speciation events that mark its beginning and its end in time. If, in contrast, it is claimed that “a single DNA sequence is no different from a single unique

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name for every taxon” (Mallet and Willmott 2003: 57), then a species so designated cannot extend through time and anagenetic change; or, if it does, its DNA barcode must remain the same throughout such change. This is a conceptual issue that originates from the presentist approach to biodiversity as is inherent in barcoding: it looks at population structures in the present time slice only. Such clusters could at best correspond to Mayr’s (1963) nondimensional species appreciated by the local naturalist. They are not compatible with an evolutionary species concept. DNA and its sequence characteristics are what philosophers call an intrinsic property of the organism. An instrinsic property is one that is specific for a certain object and is independent from other objects. “Tom is 6 feet tall” specifies an intrinsic property of Tom; “Tom is taller than his cousin Frank” specifies an extrinsic (relational) property of Tom. If a species is a causally integrated system (a complex whole) that is located in space and time, then the intrinsic properties of its constituents collectively constitute the intrinsic property of the species. The sequence of the DNA barcode is an intrinsic property of the species that must be maintained throughout its history if that barcode is to “tag” the species though space and time. On this account, barcoding espouses an essentialistic species concept. The barcode sequence becomes an intrinsic essential property of the species, which “contrasts with current evolutionary thinking that incorporates the complex, dynamic relationships seen between organisms and lineages in nature into our species concept” (Rubinoff et al. 2006: 2). To pursue the barcoding initiative as pragmatically useful and empirically successful, while denying its essentialist implications, requires an instrumentalist approach to species. A realist approach to species, which takes species to be spatiotemporally extended, causally integrated systems, will denounce barcoding as a theoretically vacuous technology (Wheeler 2004; Hamilton and Wheeler 2008). Evolving species cannot have intrinsic essences (Hull 1989, 1999; Ghiselin, 1997). DNA barcodes may be useful as contingent (rather than essential) markers for biodiversity assessments in the current time slice (Herbert and Gregory 2005), but they have no explanatory force (Hacking 2007: 234).

CONCLUSION

Systematists as well as conservation biologists work in the present time. Only the present time is epistemically and empirically accessible. If that is accepted, and if it is also accepted that species have histories, then

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the term species is a theoretical term. The meaning of the term species must then be given through the scientific theory in which this term is deployed. But a theory that gives the meaning of a theoretical term such as species must not do so simply by a definition, for definitions are (or can be) largely arbitrary; at the very least, they are conventional. Instead, a theory gives relevant meaning to a theoretical term by conveying substantial (and revisable) empirical knowledge about the causal relations in which the entities to which the term refers take part. The theory that tells us about which causal roles species engage in is evolutionary theory. This calls for an evolutionary species concept. Taking a strictly presentist approach to biodiversity, the barcoding initiative instead adopts species instrumentalism. Species and their constituents cannot have essential intrinsic properties, at least not on the basis of current evolutionary theory (e.g., Hull 1989, 1999; Griffiths 1999; Okasha 2002; Rieppel 2007). A taxonomy that takes the historical dimension of species seriously must be a theory-driven research program, the relevant theory being evolutionary theory (Hamilton and Wheeler 2008). Evolutionary theory tells us that species not only have a history, extant species indeed make history (Løvtrup 1977, 1979). As the history of species plays out through space and time, the “divisional hierarchy” of P. A. Williams (1992) unfolds. The divisional hierarchy is an exclusive one: the ancestral species excludes its descendants, just as the descendants also exclude each other. Looking back on the history species once made, one notes that the relative degrees of their relationships become apparent in a system of monophyletic taxa—at least for bisexually reproducing organisms, and for species that did originate through lineage splitting and not through hybridization. Monophyletic taxa do not make history. Instead, monophyletic taxa form an inclusive hierarchy: species cannot be monophyletic taxa; species are included in monophyletic taxa. For Hennig (1950, 1966), monophyletic taxa are systems of higher complexity that include species, themselves systems of lower complexity. Species, as well as monophyletic taxa, were taken by Hennig (1950, 1966) to be individuals (spatiotemporally located and causally integrated systems); but whereas ancestral species do not include descendant species, the ancestral species and all, and only, its descendants are included in a monophyletic taxon. Inclusion is here understood as an enkapsis, an encapsulation of parts within wholes (Günther 1956: 41; Zimmermann 1953: 9). For Hennig (1950, 1966), species are the fundamental building blocks of the phylogenetic system, characterized by their potential to subdivide into two daughter species. From a genealogical (as opposed to

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an ecological) perspective, the encapsulated entities (i.e., the species) are independent individuals that travel through time on their own separate evolutionary trajectories and that replicate through lineage splitting. The inclusive monophyletic taxon is a complex whole that is constituted by the system of splitting species lineages it encapsulates. This is how the two hierarchies identified by P. A. Williams (1992) come together (Hennig 1957, 1966). Let a cell divide and the resulting cells divide again: c1 gives rise to c2 and c3; c3 gives rise to c4 and c5; c4 gives rise to c6 and c7; c5 gives rise to c8 and c9, and so forth, another cell lineage taking its origin from c2. The result is a dichotomous hierarchy of cell lineages. Bertalanffy (1932: fig. 2) called a cell lineage such as the one comprising c3 through c9 (metaphorically speaking: a monophyletic clade of cell lineages) a “cell-cone” (Zellkonus) within the whole cellular system. In analogy, a monophyletic taxon corresponds to a “species cone” in the Tree of Life, a system of species lineages splitting and splitting again that goes back to a “beginner,” the ancestral stem species of that taxon.

Acknowledgments

I thank David Williams and Sandra Knapp, who invited me to contribute to this Festschrift for Chris Humphries. David Williams shared the unpublished manuscript of Colin Patterson’s lecture delivered at the 1981 Willi Hennig Society meeting in Ann Arbor. An anonymous referee offered helpful comments on an earlier version of this chapter.

NOTES 1. This is the so-called pasta problem: take twenty-five different types of pasta, declare one (e.g., the thin spaghetti) as plesiomorphic, and do a cladistic analysis on them. The same can be done to taxa. What is the difference between applying cladistics to pasta or to taxa? As it cannot be the method, it must be the underlying ontology. 2. “Reciprocal monophyly” (Avise 2000) is based on a different definition of monophyly than the one adopted here. Monophyly in this chapter refers to a taxon that includes the ancestor and all, and only, its descendants. Reciprocal monophyly implies a concept of monophyly that applies to “an entity in which no included unit is more closely related to a unit that is not part of the entity than to any unit that is part of it” (de Queiroz and Donoghue 1990: 70). This latter concept of monophyly, rejected by Hennig (1966: 73), was named “exclusivity” by Graybeal (1995).

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Williams D.M., Scotland R.W., Humphries C.J., Siebert D.J. 1996. Confusion in philosophy: A comment on Williams (1992). Synthese 108: 127–136. Williams P.A. 1992. Confusion in cladism. Synthese 91: 135–152. Willmann R. 1983. Biospezies und Phylogenetische Systematik. Z. Zool. Syst. Evolutionsforsch. 21: 241–249. Willmann R. 1985. Die Art in Raum und Zeit. Das Artkonzept in the Biologie und Paläontologie. Hamburg: Paul Parey. Woodger J.H. 1930a. The “Concept of Organism” and the relation between embryology and genetics. Part I. Quart. Rev. Biol. 5: 1–22. Woodger J.H. 1930b. The “Concept of Organism” and the relation between embryology and genetics. Part II. Quart. Rev. Biol. 5. 438–463. Woodger J.H. 1931. The “Concept of Organism” and the relation between embryology and genetics. Part III. Quart. Rev. Biol. 6: 178–207. Woodger J.H. 1952. From biology to mathematics. Brit. J. Philos. Sci. 3: 1–21. Zimmermannn, W. 1953. Evolution: Die Geschichte ihrer Probleme und Erkenntnisse. Munich: Karl Albert Freiburg.

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TEN

David M. Williams, Malte C. Ebach, a n d Q u e n t i n D. W h e e l e r

B E YO N D B E L I E F The Steady Resurrection of Phenetics Those who cannot accept the heady mixture of operationalism and objectivity should divert their attention to other things, such as the collation of published information advocated by Waters (1961). (Barker 1996: 670)

I have waited a long time for this. . . . I shall build a new race of Daleks. They will be even more deadly and I, Davros, shall be their leader! This time we shall triumph. My Daleks shall once more become the supreme beings! (Doctor Who: “Resurrection of the Daleks,” BBC 1984)

Nowadays phenetics per se is rarely taught in systematics courses, its heyday during the 1960s supposedly having come and gone. For example, botanist Richard Jensen, reviewing the Twenty-fifth Numerical Taxonomy Conference held at the University of Pittsburgh sixteen years ago, made the following comments: This anniversary meeting allowed reflection on the impact that numerical taxonomy has had on systematics and comparative biology. Although few would agree with Herbert Ross’s opinion that “numerical taxonomy is an Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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excursion in futility,” it is clear that its role in systematics has not evolved as proponents projected: The methods are rarely used as the foundations for classifications. (Jensen 1993: 599)

Cladistics, on the other hand, remains if not a persistent (and menacing) presence (Brummitt 2006), then, as it was at first perceived, a shadowy specter (Campbell 1975: 86), dominating biological classification. Yet recently Mishler posed the following question: “Why is it that . . . virtually all systematists (at least the younger generations) are now Hennigian phylogenetic systematists?” (Mishler 2009: 63). Odd, too, that in his account of the history of numerical taxonomy, based on a presentation at the same Numerical Taxonomy Conference Jensen summarized, Sneath offered the following, a view that contrasts in an absolute sense to Mishler’s: “Hennigian cladistics, however, is a side issue that has not proven its value. Numerical taxonomy in the broadest sense is the greatest advance in systematics since Darwin or perhaps since Linnaeus” (Sneath 1995: 281, from abstract). Leaving aside the view that numerical taxonomy is “the greatest advance in systematics since Darwin or perhaps since Linnaeus,” Sneath’s general claim rests on his assessment of numerical taxonomy’s influence, having “stimulated several new areas of growth, including numerical phylogenetics, molecular taxonomy, morphometrics, and numerical identification” (Sneath 1995: 281, from abstract). Mishler’s claim stems from the answer he provides to his own question: “. . . divergent evolution is the single most powerful and general process underlying biological diversity” (Mishler 2009: 63). Mishler’s claim for success is a process, but his meaning implies its representation as a tree. That is, the tree as reality rather than metaphor, originating from Charles Darwin’s work which helped Ernst Haeckel turn the old metaphorical tree—the hierarchical relationships expressed in a classification—into “a condensation of real events, rather than a metaphor” (Beer 1983: 38) coupled with, some years later, Willi Hennig recognizing the profit to be gained from monophyletic classification, a direct and accurate representation of that tree (Hennig 1966). The contrast is Sneath views the issue from the point of view of methodology, Mishler from a cause and its representation. Such a contrast has been noted before, with respect to cladistics: Cladistics is a term with two distinct meanings. In one, it implies acceptance of a cladistic position on classification, the view that groups in the

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classification system should be monophyletic. In its other meaning, it signifies an interest in reconstructing phylogenies, without regard to how the classification system is set up. . . . The question of how to construct classifications and how to reconstruct phylogenies are logically separable, so that it would be better to avoid the word cladistics altogether. (Felsenstein 1984: 169; Felsenstein 1983a: 315 and Felsenstein 2004: 145–146)

Avoiding the word is a possibility, but others have considered the whole matter superfluous, such as Hughes, who nearly a dozen years ago, wrote: The conflict between pheneticists and cladists properly belongs to the era of morphological systematics—an era that is now effectively at an end. The availability of molecular data has revolutionized the field and made many old controversies obsolete. (Hughes, 1999: 34, see also Kim 2001)

Regardless of any truth in any or all of those statements, phenetics and cladistics might very well be viewed as contrasting methodologies, situated within the larger phenomenon of numerical taxonomy—this might even be the accepted interpretation (de Queiroz and Good 1997; Kitching et al. 1998). For example, Felsenstein has suggested, “In fact, both methods [cladistics and phenetics] can be considered to be statistical methods, making their estimates in slightly different ways” (Felsenstein 2004: 146). Thus, a contemporary solution might be to ignore the words cladistics and phenetics, and to assume they represent just alternative methodologies (among many), to be judged by certain parameters and applied to DNA as the sole source of data. That approach might oversimplify matters, but it does appear to be the prevailing rationale in certain quarters. Alternatively, it is possible to view both phenetics and cladistics as philosophies, ways to think about things, rather than particular methodologies. We attempt to examine both from that perspective.

DEFINITIONS AND COMPARISONS

To begin we offer some rudimentary comments on definitions. Phenetics was first used 50 years ago by Cain and Harrison: “we shall refer to the arrangement by overall similarity, based on all available characters without any weighting as phenetic, since it employs all observable characters (including, of course, genetic data when available)” (Cain and Harrison 1960: 3).

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100

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FIGURE 10.1 After Sokal and Sneath, 1963, Fig. 9-1, pp. 252–253; slightly redrawn in Sneath and Sokal, 1973, Fig. 5-33, pp. 295–296. “Drawing a horizontal line across the dendrogram [phenogram Sneath and Sokal 1973] at a similarity value of 75% creates four 75-phenons, 1, 2, 5, 9; 3, 6, 7, 10; 4; and 8. . . . A second phenon line at 65% forms three 65-phenons.”

That definition includes a number of items: “overall similarity,” “all available characters,” “all observable characters,” and, of course, “genetic data.”1 The last three items all refer to data, the visible (“all observable characters”) and the invisible (“genetic data”) in its totality (“all available characters”). It might be worth noting that the last item of the definition—“all available characters”—surfaced in the cladistic literature under the concept of “total evidence” (Kluge 1989, critiqued by, among others, Rieppel 2005, Fitzhugh 2006) and in the molecular literature under the concept of “concatenation” (e.g., see Gadagkar et al. 2005; the concept of concatenation has been critiqued by, among others, Edwards 2009). Given that it is possible to find a parameter that successfully measures “overall similarity” from “all available characters,” Sokal and Sneath illustrated how those results might be presented in a tree diagram displaying various levels of “overall similarity” (or just plain “similarity”) (Fig. 10.1). They described part of their tree thus:

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Drawing a horizontal line across the dendrogram [phenogram; Sneath and Sokal 1973] at a similarity value of 75% creates four 75-phenons, 1, 2, 5, 9; 3, 6, 7, 10; 4; and 8. . . . A second phenon line at 65% forms three 65-phenons. (after Sokal and Sneath 1963: 252–253, Fig. 9-1; slightly redrawn in Sneath and Sokal 1973: 295–296, Fig. 5-33)

The levels can be used to form a classification and an internested series of groups. For example, referring to Figure 10.1, if the 65 percent level is chosen, three groups result: {1, 2, 5, 9} = A; {3, 6, 7, 10} = B; {4, 8} = C; which relate in the following way: A(BC). Sneath and Sokal created the word phenon to mean “groups produced by any form of cluster analysis from any form of similarity coefficients . . . groups which approach natural taxa more or less closely, and like the term taxon, they can be used at any rank” (Sneath and Sokal 1962: 860; Sokal and Sneath 1963: 251; Sneath and Sokal 1973: 294). Sneath and Sokal suggested that such groups could be equated with genera, tribes, or families but “as those terms have evolutionary, nomenclatural and other connotations, we prefer to use new expressions,” hence phenons (Sneath and Sokal 1962: 860; Sokal and Sneath 1963: 251; Sneath and Sokal 1973: 294; but not the phenon of Camp and Gilly 1943: 335 or that of Mayr 1969). Thus, the concept phenon relates to the process of classification, derived from the grouping method itself, understood as an “arrangement” rather than a “classification” (McNeill 1979; Jensen 2009). Significantly, Sneath and Sokal suggest that such groups “approach natural taxa” (Sneath and Sokal 1962: 860). Methodology to one side, the central issue is the concept of natural groups and how they relate to the idea of natural classification. At first Sokal and Sneath (1963: 252) referred to their tree as a dendrogram, a term introduced into biology some years earlier by Mayr et al.: “Such a diagrammatic illustration of degree of relationship based on degree of similarity (morphological or otherwise) may be called a dendrogram” (Mayr et al. 1953: 58; see Fig. 10.2 for the diagram in Mayr et al. 1953: Fig. 8; “I had long used this term [dendrogram], in lectures and in manuscript, for any branching, tree-like diagram serving to indicate degrees of relationship” (Mayr 1978: 85). In his definition, Mayr equates “degree of relationship” with “degree of similarity.” In their second numerical taxonomy book, Sneath and Sokal use the term phenogram instead (Sneath and Sokal 1973: 295), which is, according to Mayr, “a diagram (usually a dendrogram) representing degree of

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37

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FIGURE 10.2 After Mayr et al. 1953: Fig. 8; “I had long used this term [dendrogram], in lectures and in manuscript, for any branching, tree-like diagram serving to indicate degrees of relationship” (Mayr 1978: 85).

overall similarity (usually unweighted similarity)” (Mayr 1978: 85–86, its origin credited to both Mayr 1965 and Camin and Sokal 1965). Again, it is worth noting that, for Mayr, an “orthodox phyletic diagram” was the “true dendrogram,” a diagram that would combine details of both cladogenesis and anagenesis, branching and branch lengths (Mayr 1965: 82; his figure is reproduced here as Fig. 10.3). Defining cladistics might appear even more problematic than phenetics, given the various interpretations available. Once it would have been directly equated with Willi Hennig’s phylogenetic systematics, renamed cladistics (Mayr 1965: 81; Camin and Sokal 1965). Gradually it became equated more or less directly with parsimony, the computer algorithm (Farris et al. 1970). Once again avoiding methodologies, we present a diagram from Hennig (Fig. 10.4, from Hennig 1957: 66, Abt. 9, modified in Hennig 1966: 91, Fig. 22 and reproduced many times; see Williams and Ebach 2007: 143, footnote 5). Hennig’s diagram is like that of Sokal and Sneath’s; but rather than “percentage similarities” uniting terminals, Hennig used characters—and rather than taxonomic characters, as understood in the usual sense (as simple similarities), he placed them on the tree to express relationships. Thus, the tree in Figure 10.4, character 1 unites terminals B, C, and D relative to A, character 3 unites terminals

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A

B

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D

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F

T3 T2 Time

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FIGURE 10.3 After Mayr 1965: 82. For Mayr, an “orthodox phyletic diagram” was the “true dendrogram,” a diagram that would combine details of both “cladogenesis” and “anagenesis,” branching and branch lengths (Mayr 1965: 82).

FIGURE 10.4 After Hennig 1957: 66, Abt. 9, modified in Hennig 1966: 91, Fig. 22 and reproduced many times; see Williams and Ebach 2007: 143, footnote 5.

B relative to C and D, when combined offer A(B(CD)) as the expression of relationships among the four terminals A–D (characters 2 and 4 have their derived state in only A and B, respectively; characters 5 and 6 have their derived state in only C and D, respectively). That expression can be turned directly into a classification reflecting the internested series of monophyletic groups. The characters on Hennig’s tree are homologies. That is, they express relationships that are the natural taxa of Hennig.

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Thus comparing phenetics with cladistics can be rendered simple, relating to a concept of “naturalness”: phenetics discovers taxa (classification) via the parameter “overall similarity” derived from an assessment of “similarities,” cladistics discovers taxa (classification) via the parameter “relationship,” expressed in its simplest form as A(BC), derived from an assessment of particular homologies. PHENETICS AND AN INTELLECTUAL LINEAGE

A significant event in the development of numerical taxonomy was the publication of Felsenstein’s book Inferring Phylogenies (Felsenstein 2004). Enthusiastically reviewed, Steel noted, “Few books in molecular systematics have been awaited with such anticipation. Rumors had been circulating for many months, even years, that Joe Felsenstein’s long-promised Inferring Phylogenies was about to be published. Now that it has finally appeared, has it been worth the wait?” (Steel 2004: 173). According to Steel, indeed it has: “An Epic Worth the Wait” (Steel 2004: 173). It is “the book we’ve been waiting for” because “occasionally a book is a classic by the time it is published and this is it” (Penny 2004: 669)— “[a]n instant classic,” no less (Drummond 2004). Thus, a classic before it was printed, an epic before it was read, influential before it was written. Among the thirty-five chapters in Inferring Phylogenies is one entitled “A Digression on History and Philosophy” (Felsenstein 2004: Chap. 10). Felsenstein begins by acknowledging Principles of Numerical Taxonomy (Sokal and Sneath, 1963), the first book to summarize phenetics, to be the beginning, if not the foundation, of numerical phylogenetic methods (Felsenstein 2004: 121). Sokal and Sneath (1963) was also enthusiastically reviewed, enthusiasm being either positive or negative. A positive review ended: I am convinced that numerical taxonomy will ultimately find its proper place in the methodology of systematics and that the Sokal and Sneath book will play a most important role in bringing this about. (James 1964)

A negative review ended: After reading this book carefully, it is my considered opinion that numerical taxonomy is an excursion in futility. (Ross 1964: 108, as cited by Jensen above; for more on Ross see Nelson and Ladiges 2009; Sokal got his own back by reviewing Ross’s 1974 book: Sokal 1975)

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Ten years later, the second numerical taxonomy book appeared, with a simpler title—Numerical Taxonomy—and reversed authorship (Sneath and Sokal 1973: 295). It, too, was reviewed enthusiastically. For phenetics, the next two decades came and went with no major summary (there were a few introductory texts and proceedings of symposia—e.g., Felsenstein 1983b). Instead, there were a few books on cladistics (Eldredge and Cracraft 1981; Nelson and Platnick 1981; Wiley 1981). It was during the late 1970s—the period in which David Hull suggested cladistics to have won the “systematics battle” (Hull 1988)—phenetics appeared to have died. But from its ashes a new phylogenetics was born, students of phenetics busy inventing algorithms to analyze similarity, invoking a plethora of models to represent aspects of the evolutionary process— models are, after all, simply various forms of character weighting—and arguing for the necessity of a statistical viewpoint (Felsenstein 2001). Following Felsenstein, then, one might derive an intellectual transformation series, or lineage, having its beginnings in the Principles of Numerical Taxonomy (Sokal and Sneath 1963) via Numerical Taxonomy (Sneath and Sokal 1973) to Inferring Phylogenies (Felsenstein 2004), from 1964 to 2004—Felsenstein’s 40 years (“Phylogenies . . . have been around for over 140 years, but statistical, computational, and algorithmic work on them is barely 40 years old” (Felsenstein 2004: xix)—phenetics (equal weighted similarity) resurrected as phylogenetics (weighted similarity), Jensen’s dead subject becoming the epic we were all waiting for, an epic now being endlessly rewritten and replayed, numerically revised and honed (Gascuel 2005; Sakhar 2006; Salemi and Vandamme 2003; Semple and Steel 2003). As histories go, Felsenstein’s is unique. One might contrast it with other histories (Vernon 1988, 1993, 2001; Hagen 2001, 2003; Williams and Ebach 2007; Hamilton and Wheeler 2008). CLASSIFICATION AND HOMOLOGY IN THE PHENETIC LINEAGE

Felsenstein’s numerical taxonomy lineage represented as a transformation series might not be the best approach. An alternative would be to evaluate the three books—Principles of Numerical Taxonomy (Sokal and Sneath 1963), Numerical Taxonomy (Sneath and Sokal 1973), Inferring Phylogenies (Felsenstein 2004)—from the perspective of classification and homology, the two central principles of systematics. Principles of Numerical Taxonomy (Sokal and Sneath, 1963) devotes roughly a third of its pages to techniques—that is, explanations of

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particular methods to determine degrees of similarity, how to construct graphs, charts, and trees. Inspection of the index reveals twenty-seven entries for classification including a reference to Chapter 8, “Phylogenetic Considerations” (Sokal and Sneath 1963: 347), and thirteen entries for homology including the section on “Operational Homology” in Chapter 5, “Taxonomic Evidence: Characters and Taxa” (Sokal and Sneath 1963: 351). After a brief introduction there is a chapter entitled “A Critique of Current Taxonomy” (Sokal and Sneath 1963: 5), where the natural system is discussed (Sokal and Sneath 1963: 11). Their conclusions can be summarized by two factors: (1) many characters are required; (2) a measure of degree of similarity is required. Phenons—“groups produced by any form of cluster analysis from any form of similarity coefficients . . . groups which approach natural taxa more or less closely, and like the term taxon, they can be used at any rank”—are equated with natural taxa. Numerical Taxonomy (Sneath and Sokal 1973) is a revised version of the earlier book; although set out differently, the topics are much the same, including the discussion and conclusions concerning the natural system (discussed later). Still, inspection of its index reveals twenty-six entries for classification including references to a section of Chapter 2, “Choice of a Basis for Classification” and Chapter 5, “Optimality Criteria and the Comparison of Classifications” (Sneath and Sokal 1973: 560) and forty entries for homology including a whole section of Chapter 3 devoted to the subject (sixteen pages) (Sneath and Sokal 1973: 564).

ANCESTRAL PHENETICS AND THE NATURAL SYSTEM

Historian Polly Winsor has tackled many of the claims first promoted in the philosophical works of zoologist Arthur Cain (1921–1999; Clarke 2008) and botanist J. S. L. Gilmour (1906–1986; Waters 1989) (Gilmore 1937, 1940, 1951, 1961; Cain 1958, 1962) as well as others associated with the mid–twentieth century New Systematics (Winsor 2000, 2001, 2003, 2004, 2006a, 2006b; for histories, see Dean 1979; Hagen 1983, 1984, 1986). Winsor has vigorously tackled what has become know as the “essentialism story” (Winsor 2001, 2003, 2006a, 2006b; see also Amundson 2005; Müller-Wille 2007; Wilkins 2009), an analysis of the philosophy of past taxonomic practice forged by Cain, assisted by Ernst Mayr and David Hull (1965), a story that Winsor is “convinced it is little more than myth,” and “in its broad sweep across the history of

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systematics, this story is not merely inaccurate in particulars, it is wrong and harmful in its basic message” (Winsor 2006a: 3). Furthermore, it is a “miserable history of depreciatory comment without a particle of truth” (Nelson 2004b; Reid 2009 offers a different view). The essence of that story (myth) is that taxonomists were typologists-essentialists and were engaged in the search for the essences of species, their defining characters—a story that seems to have no substance when the activities of taxonomists themselves are examined. Sneath and Sokal’s discussion of the natural system relies heavily on interpretations found in the philosophical works of Cain and Gilmour. Even before the first numerical taxonomy textbook was published, Sneath used a historical claim to justify his view on the nature of natural groups (Winsor 2004). His view was derived from a reading of Michel Adanson and Georges Cuvier via Francis Bather’s essay (Bather 1927). Sneath discovered reference to Bather’s essay in Gilmour’s “Taxonomy and Philosophy” paper (Gilmour 1940), a contribution to Huxley’s New Systematics book (Winsor 2004). To derive the groups found in Adanson’s Familles des plantes (1763– 1764), Bather suggested Adanson had tabulated “all possible characters, basing a classification on each. Then, setting his 65 classifications side by side, he found certain groupings to occur more frequently, and those he took as his families” (Bather 1927, after Winsor 2004: 2). To Sneath, this was an early version of phenetics: classifications “based on giving every feature equal weight . . . may be conveniently called ‘Adansonian’” (Sneath 1957: 196); but Bather’s interpretation was derived from Cuvier’s Éloge historique de Michel Adanson (Cuvier 1807), who was naturally critical of Adanson’s “raw empiricism” as it contrasted with his (Cuvier’s) own more functional way of deriving affinities, and was inaccurate (Winsor 2004: 2; as Winsor points out, Michel Guédès discovered the error in 1967—see Guédès 1967). For numerical taxonomy, then, regardless of whether one might find a reliable parameter to measure “overall similarity” accurately, the basis of their argument rests in faulty history and philosophy.

DERIVED PHENETICS AND THE NATURAL SYSTEM

Inferring Phylogenies differs from Sneath and Sokal’s books. Inspection of its index reveals no entries at all for homology (Felsenstein 2004: 652, where one will find a remarkable six entries for homoplasy;

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synapomorphy is mentioned three times [p. 661], two of which are embedded in quotes). Classification is different. The index reveals nine entries, all but two form part of “digression on history and philosophy” chapter (Felsenstein 2004). Classification is different because Felsenstein creates, or claims to create, “The It-Doesn’t-Matter-Very-Much school,” its outline covered in a section entitled “The Irrelevance of Classification” (Felsenstein 2004: 145), “a bizarre thumb in the eye to systematists” (Sanderson 2005: 2057). The spirit has been expressed before in a variety of slogans: “The focus of systematics has shifted massively away from classification: it is the phylogenies that are central, and it is nearly irrelevant how they are then used in taxonomy” (Felsenstein 2001); “Systematists get so worked up declaiming the centrality of classification in systematics that I have argued the opposite” (Felsenstein in Franz 2005); and from a different source, “Many phylogeneticists now see nomenclature and classification as largely irrelevant to phylogenetics” (Hillis 2007). The point being made is that it is only the tree that is required. Names are of little significance. Felsenstein’s forty intervening years—the “statistical, computational, and algorithmic work” (Felsenstein 2004: xix)—amounts to the dismissal of classification and homology, reinventing and remodeling phenetics and christening it bioinformatics (Hagen 2000), thereby reducing the subject of systematics to a set of methodologies, a mere technique. One of Willi Hennig’s collaborators, Dieter Schlee (Hennig and Schlee 1978; Schlee 1971, 1978), reviewed the Numerical Taxonomy book (Schlee 1975). He closed his review with the following: “The author’s warning that ‘the systematist who ignores numerical taxonomic methods in his own work does so at his own loss’ will, I hope, be tolerated with composure” (Schlee 1975: 268). It is worth recalling here that Arthur Cain had unfavorably reviewed Hennig’s 1966 book Phylogenetic Systematics (Cain 1967), later concluding that it is “difficult to tell which are shared ancestral characters and which are convergent,” and thus cladistics was a “ridiculous scheme” (Cain 1981: 16; Cain 1982). Rather oddly, he later wrote that “Hennigism has achieved its popularity for a reason that does no credit to science; computers are the latest and most fashionable technique, and Hennig’s procedures can be easily computerized” (Cain 1988: 192), commentary that might seem puzzling in the light of Felsenstein’s “Principles of Numerical Taxonomy—Numerical Taxonomy—Inferring Phylogenies” lineage. A previous reaction of ours was to suggest the systematics community is “Drowning by Numbers” (Williams and Ebach 2005). On reflection,

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the general effort of these most derived numerical taxonomists—to ignore classification, ignore homology, thereby embracing phenetics— reminds us more of Huxley’s New Systematics, a movement that also ignored classification to focus solely on species and the processes they imagined brought them into being (Wheeler 1995). It seems fitting, then, that Julian Huxley, a prominent British biologist responsible for ushering in the New Systematics era to the United Kingdom via the newly formed Systematics Association (Winsor 19952), should have his name on a lecture series, of which the third was given by Felsenstein in 2008, aptly squaring that particular circle.

ANOTHER NATURAL SYSTEM AND INTELLECTUAL LINEAGE: 1778 AND ALL THAT . . . As far as I can see, Linnaeus was the first to draw a clear terminological distinction between artificial and natural systems, and this was praised as one of his main achievements by later naturalists and philosophers (Jussieu 1789: xxvi; Candolle 1819: 52; Whewell 1857, Vol. 3: 268). (Müller-Wille 2007: 544)

“Unknown to most, the year 1778 looms large in the annals of botanical thought,” wrote Leon Croizat in 1945 (Croizat 1945: 64): Linnaeus died on January 10 of that year; less than a month after, on February 4, Augustin Pyramus de Candolle was born in Geneva; Lamarck’s Flore française was printed in 1778 (the first edition was named Flore françoise but was not available until 1779: “all three volumes after 21 March 1779”; Stafleu and Cowan 1976: 731). Flore française went through three editions. While the second edition was “an almost word by word reprint’’ of the first (Stafleu and Cowan 1976: 732), the third, published in 1805, was handed over to Candolle, who wrote almost all of it (for histories of this book see Ebach and Goujet 2006 and Scharf 2009). The third edition was a remarkable book indeed: it contained the first ever biogeographic map (Ebach and Goujet 2006), the first ever dichotomous key, and Candolle’s novel introductory text Principes élémentaires de botanique (Lamarck and Candolle 1805). After he left Paris for Montpellier, Candolle developed his Principes chapter into a book length treatment, Théorie élémentaire de la botanique (Candolle 1813), which, according to Croizat, was “the first work in which the soul of the natural and artificial method had been laid

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bare” (Croizat 1945: 64). An English translation was published in 1821 (Candolle and Sprengel 1821) derived from an earlier German translation (Candolle and Sprengel 1820); Candolle was unhappy with both (see later discussion). Candolle began his discourse by praising Linnaeus, as “the first to distinguish carefully between the artificial method and the natural method . . . he was the first to give examples of one and the other” (Candolle 1813: 453). Some 170 years later the same sentiment was expressed by Gareth Nelson and Norm Platnick in their Systematics and Biogeography: “Linnaeus may be viewed as having placed the study of systematic botany on a new and modern basis. The central problem, for him and later workers as well, is the meaning and significance of artificial and natural systems” (Nelson and Platnick 1981: 88). One might briefly consider Candolle’s view. He first distinguished between systems and methods, where a system is a key or classification based on a particular part of an organism, while a method is a key or classification based on all of the parts of an organism. Here, it is worth recalling Sneath and Sokal’s discourse on the natural system, with their conclusion that one requires many characters and some measure of similarity. It is here the phenetic enterprise stops, as if merely using all characters and having a measure of similarity is enough. And it is irrelevant if there is but one measure of similarity, or a thousand, whether one is barcoding species or sequencing genomes. Candolle went further by suggesting that methods can be subdivided into artificial and natural depending on their purpose, such that artificial classifications are for identifying plants, natural classifications are for expressing “real relationships.” We noted earlier that Candolle was unhappy with both the German and English translations of Théorie élémentaire de la botanique (in his memoirs, Candolle referred to both the English and German translations thus: “Ouvrage entièrement rédigé par M. Sprengel, d’après ses propres idées, et auquel je suis étranger” [“a work written entirely by Mr Sprengel, after his own ideas, to which I was entirely foreign”], Candolle 1862 [2004]: 511, from Nelson 1978: 279; see also Stevens 1984a: 205, comment in bibliography). William Whewell (1894–1866), an English philosopher, was influenced by many of Candolle’s ideas (Stevens 1984b) and summarized the issues relating to classification in his The Philosophy of the Inductive Sciences (1840). Rather than explore Whewell’s and Candolle’s notions in depth, a few items are of immediate significance. In a summary of natural systems, Whewell wrote:

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And the maxim by which all Systems professing to be natural must be tested is this: that the arrangement obtained from one set of characters coincides with the arrangement of another set. (Whewell 1840: 521 and 1847: 539)

The statement became Aphorism 100 (C) in the second edition of The Philosophy of the Inductive Sciences: The basis of all Natural Systems of Classification is the Idea of Natural Affinity. The Principle which this Idea involves is this:—Natural arrangements, obtained from different sets of characters, must coincide with each other. (Whewell 1847, II: 463)

The basis is derived from Candolle, in a relevant passage from Théorie élémentaire de la botanique, whom Whewell cites in translation: Thus, the natural classes founded on one of the great functions of the vegetable are necessarily the same as those which are founded upon the other function; and I find here a useful criterion to ascertain whether a class is natural: namely, in order to announce that it is so, it must be arrived at by the two roads which the vegetable organization presents. (Whewell 1840, I: 520 and 1847, I: 539, italics in original, passage translated from Candolle 1813: 83–84,4 see also Candolle 18295)

There are two parts to Candolle’s equation: 1. “Natural arrangements, obtained from different sets of characters, must coincide with each other”—which is an expression of the notion that rather than mere similarities, it is the coincidence (congruence) of characters that determines the naturalness of the arrangement 2. “The Idea of Natural Affinity”—a notion expressed through the concept of homology In effect, Candolle captures both the phenetic and the cladistic enterprise and distinguishes between them—or at least expands on the latter. After discussing the various approaches to classification, for natural methods Candolle notes, “There are those persons who want to study plants, either in themselves, or in their real relations among themselves” (translated from Candolle 1813: 276). One might ask, What are “real relations”? Today, “real relations” are usually understood as being related to common ancestry, and common

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ancestry relates to phylogeny. One might then ask, What is phylogeny? Charles Darwin wrote on the Natural System: But many naturalists think that something more is meant by the Natural System; they believe that it reveals the plan of the Creator; but unless it be specified whether order in time or space, or what else is meant by the plan of the Creator, it seems to me that nothing is thus added to our knowledge. Such expressions as that famous one of Linnaeus, and which we often meet with in a more or less concealed form, that the characters do not make the genus, but that the genus gives the characters, seem to imply that something more is included in our classification, than mere resemblance. I believe that something more is included; and that propinquity of descent,—the only known cause of the similarity of organic beings,—is the bond, hidden as it is by various degrees of modification, which is partially revealed to us by our classifications. (Darwin 1859: 413–414)

In this passage Darwin does not write of phylogenies, such things being unknown in 1859 (as opposed to a few scribbled embryonic trees of descent)—the word phylogeny was coined in 1866 by Ernst Haeckel (Haeckel 1866). By the fifth edition of the Origin, published in 1869, Darwin was able to write on phylogenies: Professor Häckel in his “Generelle Morphologie” and in several other works, has recently brought his great knowledge and abilities to bear on what he calls phylogeny, or the lines of descent of all organic beings. . . . He has thus boldly made a great beginning, and shows us how classification will in the future be treated. (Darwin 1869: 515)

Rather than forty years, there are one hundred that separate Haeckel’s representation of phylogeny from Hennig’s (Figs. 10.4 and 10.5). For ancestors, Haeckel more or less guessed (paraphyly); for Hennig ancestors could be inferred from nodes, found from the characters used to delimit the groups—but it does not really matter whether the inference is made or not—it is the characters that matter, or at least that “different sets of characters, must coincide with each other.” In another discussion of the natural system in relation to the ever-growing resurgence of phenetics, Gareth Nelson notes the words of Antoine Laurent de Jussieu (1748–1836), from his Examen de la famille des Renoncules,7 his monograph on buttercups: Among these characters, some are constant, other vary: each character, taken separately, is found in one or many other families; but their

FIGURE 10.5 After Haeckel, E. 1866, Generelle Morphologie der Organismen: Allgemeine Grundzüge der organischen Formen-Wissenschaft, mechanisch begründet durch die von C. Darwin reformirte Decendenz-Theorie, Taf. 1.

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combination is found only in the family of buttercups; for that family, it is thus combination that constitutes the synapomorphy [the essential and invariable character]. (Nelson 2004a: 136, his translation from Jussieu 1777: 217)

Systematics in general, cladistics in particular, Candolle’s natural classification and the general notion of phylogeny might all be understood as the same: a natural classification (cladistic) that expresses real relationships. CLADISTICS REDUX: REAL RELATIONSHIPS RECONSIDERED

Real relationships, in the sense of occurring in the real world, are not abstract entities. Relationships are observed when, for example, the same forearm manifests itself in different individuals of the same taxon or across different taxa (e.g., compare any arm to the foreleg of any cat) (Ebach 2005). One may ask whether analogies are also real: “Do we not see a wing on a duck and on a dragonfly?” The answer is simple: we do not see the same structure (i.e., a bird’s wing is far removed from the wing of a dragonfly). What we do is link a word to two real things in order to communicate these as ideas. For instance, we can say, “Look how the bird and insect both use wings to fly.” We may refer to images of birds and butterflies or even wax models. What we are using is an abstract concept of a wing in order to communicate an experience. In this sense similarities are forms of communication that are totally abstract; that is, they do not occur in the real world. Similarity means that two objects are “related” in appearance, not in structure. Since appearance is conveyed by language, it is abstract. Appearances are, after all, subjective. We may walk past a potted plant, believing it to be alive, before we do a double take and realize that it is in fact made of plastic. Appearance can deceive our senses. Samenesses—relationships—do not. It confirms a structure or overall relatedness between things. Problems arise in systematics, and particularly in phylogenetics, when we attempt to use similarities in order to quantify sameness (i.e., relationship). Since relationship is not abstract, it cannot be represented as so. Just as similarity cannot be represented in reality, as it is purely abstract. In order to quantify relationship (i.e., using algorithms to find “relationships”), we use similarity as a relationship mimic. Since it cannot be expressed in an abstract form, relationship has been mimicked by similarity in phenetics. The problem occurs when we dismiss relationship for a mimic or a real experiential entity for an abstract concept.

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Imposing phenetics on a real world results in artificial relationships. Some of these similarities may indeed (unwittingly) be real relationships. This indicates that the algorithm is a good mimic—but it does not mean it is the real thing. But what if we take this further—interpreting artificial classification for real relationships? In doing so, we distort a concept or abstract idea with a real event—a genealogical relationship. Classification is meant to make sense of relationships by looking for sameness, which is observable, rather than an event, which is only partially observable. In this sense relative relationships, in the sense of sameness or homology, are better ways to classify and summarize overall taxic relationships than inferring genealogies or phylogenies. An inference is purely abstract, whereas relationships are real. Confusing relationship with similarity (as many authors do) creates an oxymoron—real quantifiable similarities and hypothetical relationships. This confusion has led to the steady increase of phenetics and the dismissal of cladistics. Cladistics addresses this confusion. We offer more credence to measurements of similarity than we do to actual real observable relationships. We may appear to be “99% are” (Silvertown 2008) similar to chimpanzees, but this can never be seen in the real world. The appearance is totally abstract and beyond any human experience or reality, but yet it engages a larger public audience. A better way is via relationship: pronouncing we are more closely related to a salmon than we are to a shark is a real and precise statement of relationship, rather than a simple quantification. This is where the cladistic redux anchors itself—by stating that cladistic relationships are real, similarities abstract.

CANDOLLE: THE MISSING LINK

Possibly because of the poor English translation of Candolle’s Théorie élémentaire de la botanique, the nineteenth- and twentieth-century obsession with fossils, or the philosophy promulgated by the New Systematists and the pheneticists, artificial and natural classifications have been understood to relate to less and more characters, respectively—with the belief that more means natural. That viewpoint has spilled over into the phylogenetic community: “When do you have enough characters? The reconstruction of phylogeny is an open ended process, so in principle you never have enough characters. In practice, you stop when you stop

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getting different answers or different resolutions when you add new data. Even then it is possible for someone to come along and modify what you have done. (Brooks and McLennan 1991: 66; McLennan and Brooks 2001: 26; further commentary in Nelson 2004a: 139)

But Candolle did not mean just the numbers of characters as significant, as he noted that “a method is a key or classification based on all of the organs of a plant,” regardless of whether it is artificial or natural. It is the intended purpose that is relevant, with real relations being found by congruence of relevant characters rather than sheer quantity, which is the general understanding of cladistics. The problem, if there is any, is captured by the following: What, then, of cladistics in relation to the history of systematics? If cladistics is merely a restatement of the principles of natural classification, why has cladistics been the subject of argument? I suspect that the argument is largely misplaced, and that the misplacement stems, as de Candolle suggests, from the confounding goals of artificial and natural systems. (Nelson 1979: 20)

The arguments really do indeed seem misplaced. We offer the view that Candolle is the link between Linnaeus and Hennig, with cladistics, as developed after Hennig in Systematics and Biogeography (Nelson and Platnick 1981), the most comprehensive modern interpretation of Candolle and natural classification coupled with the most comprehensive critique of Haeckel’s phylogenetic trees. So what of some recent initiatives in systematics: the new codes of nomenclature (phylocode), DNA barcoding, the resurgence of paraphyly, and the abandonment of classification altogether? In one way or another, they all seem linked to phenetics, inasmuch as they deviate from primary goal of comparative biology: to discover relationships (homology, taxa). The most charitable way of dealing with these recent efforts, as well as the earlier phenetic episode, is, as has been said of other endeavors, they masquerade as “a sunset mistaken for a dawn.”

Acknowledgments

John Wilkins helped clarify Whewell’s thoughts on classification (see his Evolving Thoughts blog, http://scienceblogs.com/evolvingthoughts/ 2009/02/some_more_of_whewell_on_classi.php), Gareth Nelson kindly

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supplied an English translation of Candolle (1829), and the British Council arranged for the translation of a section of Candolle’s Théorie élémentaire de la Botanique.

NOTES 1. Other definitions seems to relate phenetics directly to the phenotype, as contrasted with the genotype, leading to some alternative resurrections of phenetics (e.g., Morowitz 2003). 2. Sneath was president of the Systematics Association from 1968 to 1970. As outgoing president, he gave the 1970 Presidential Address, barely mentioning cladistics (Sneath 1971); Humphries was president from 2001 to 2003, his Presidential Address, given in 2003, asked what had become of cladistics. 3. “[M]ais comme Linné a le premier distingué, avec soin; la méthode artificielle et la méthode naturelle, qu’il a le permier donné des exemples de l’une at de l’autre” (Candolle 1813: 45). 4. “[L]es classes vraiment naturelles, établies d’après une grandes fonctions du végétal, sont nécessairement les mémes que celles qui sont établies sur l’autre, et je trouve ici un critère très-utile pour reconnaître si une classes est naturale; c’est que, pour la proclamer telle, il faut y ètre arrivé par les deux voies que présente l’organisation végétale.” 5. En combinant ces deux classes d’idées on peut donc établir avec une sorte de logique un ordre fondé sur l’importance réelle des charactères déduits de la reproduction des végétaux; mais comment saurons-nous que, malgré tous nos soins, nous ne nous serons pas trompé? Quelle sera le preuve de cette éspece d’opération arithmétique? La voici: nous referons la même opération d’après la fonction de la nutrition, et nous arriverons á un certain résultat. Maintenant si, en comparant nos deux résultats, nous reconnaissons que nous sommes arrivés par deux voies différentes précisément à la même classification, nous dirons que cette classification est naturelle. (Candolle 1829: 39)

The translation (by Gareth Nelson) is as follows: In combining these two classes of ideas, one may thereby establish, with a sort of logic, a classification founded on the real importance of the characters deduced from the reproductive system of plants; but how are we to know, despite our best efforts, that we are not mistaken? What would be the proof of this sort of arithmetic operation? Here it is: we do the same operation according to the [characters of the] nutritional system, and we arrive at a certain result. Now if, in comparing our two results, we recognize that we have arrived by two different routes at precisely the same classification, we will say that this classification is natural.

6. “Il en elle enfin qui veulent étudier les plantes, soit en elle-mêmes, soit dans la rapports réels qu’elles ont entr’elles.” 7. Not quite 1778, but see Jussieu’s Exposition d’un nouvel ordre des plantes adopté dans les démonstration du Jardin royal (Jussieu 1778).

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ELEVEN

Gordon B. Curr y

MONOGRAPHIC EFFECTS ON T H E S T R AT I G R A P H I C D I S T R I B U T I O N OF BRACHIOPODS

More than 220 years of taxonomic research have resulted in the description of over five thousand different genera of Brachiopoda. The phylum is predominantly known as fossils, but over a hundred genera still live in today’s oceans. Arguably therefore, brachiopod classification is more complicated than for many phyla because it has to cope not just with the intricacies of taxonomic practice as applied to extant organisms but also with the additional problems of studying organisms that are distributed over hundreds of millions of years of Earth history and are at best partially preserved. Yet it is the fact that the mineralized skeletons of brachiopods are so widely distributed over such a long span of geological time that makes them of such interest. These are organisms that already had a long history when dinosaurs first appeared. Brachiopods appear in such numbers and diversity in the Early Cambrian Period that it is clear that their origins lie well over 550 million years ago, long before the widespread development of mineralized shells and skeletons among Earth’s inhabitants. Any group of organisms with a continuous fossil record of over 542 million years is of great significance not just for studies of evolution but also for our understanding of the changing environments and climates

Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘by The Regents of the University of California. All rights of reproduction in any form reserved.

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on Earth. Provided they are well preserved chemically and biochemically (brachiopods are, as their shells are made of very stable low magnesium calcite), abundant (brachiopods dominate many marine communities in the Palaeozoic, and some in the Mesozoic), and widely distributed (brachiopods have a global distribution), then such phyla represent an important “proxy” for conditions on Earth far back in geological time. Long after oceans, atmospheres, and landmasses have disappeared, the abundances and distributions of fossils in rocks, and their geochemical and isotopic characteristics, allows us to investigate the extent and timing of major environmental perturbations because of the effect of such phenomena on the organisms that experienced them. But this is where the heterogeneity of the fossil record and vagaries and inconsistencies of taxonomic practice become significant. There are many different ways in which artifacts can be introduced into the analyses of fossil organisms. The geological record of brachiopods is undoubtedly incomplete, but to an unknown extent because of variability in the fossilization process. Furthermore, some geological horizons are well represented by easily accessible fossiliferous sediments, while others are poorly exposed and hence likely to be underrepresented in analyses of the fossil record (Sepkoski 1975; Smith 2001; Smith et al. 2001; Benton 2004; Smith 2007; McGowan and Smith 2008). There are also significant issues arising from the methods of constructing databases (Cooper and Williams 1952; Ager 1988), from the methods used to assess diversity (Cooper 2004), and from the activities of particular taxonomists (so-called monographic effects—Sheehan 1977; Schopf 1992; Alvarez 2001). So what at first sight may appear as an extinction or radiation event suggestive of a major environmental perturbation or evolutionary phenomenon may actually be no more than an introduced artifact (Boucot 2006; Smith 2007). There is also some concern that major events in the fossil record—for example, mass extinctions—are self-reinforcing; once discussed, there is an increase in taxonomic activity, and a greater tendency to create new taxa on either side of the event. Unraveling the various factors influencing the observed diversity patterns in fossil groups is complicated, but monographic effects due to the activities of individual taxonomists can be more easily investigated now that digital data are available. As brachiopod taxonomy has been carried out for more than 200 years, there is clearly much scope for an undoubtedly valid signal to be obscured by accumulations of numerous and varied artifacts. The extreme viewpoints would be either that human-induced artifacts are so severe as to completely obscure any signal

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from the fossil record, or, alternatively, that artifacts from taxonomic procedures are relatively insignificant and hence can be ignored. It is generally assumed that monographic biases are introduced into palaeodiversity studies by systematists concentrating on a particular taxon, or on a particular stratigraphic period, or on specimens from a particular geographic region, to the neglect of others. It seems likely that their effects are highly variable and hence important to document. This work investigates the influence of the activities of some individual taxonomists over the last 200 years. Such a study is only possible now because of the recent publication of a major international study that has reviewed all brachiopod genera formally described in the taxonomic literature up to September 2006 (Williams et al. 1997, 2000, 2002, 2006, 2007). To an extent never previously possible, the publication of this work, along with digital processing of the data it contains, provides an opportunity to investigate the effects of monographic artifacts on the pattern of brachiopod diversity.

METHODS

The available data have been extracted from the Treatise on Invertebrate Paleontology, part H (revised), which was published in six volumes (containing 3,226 pages) from 1997 to 2007 (Williams et al. 1997, 2000, 2002, 2006, 2007). The techniques used to extract and compile the data from these volumes have been described in detail by Curry and Brunton (2007), and the underlying computational techniques are explained in Curry and Connor (2007, 2008). Briefly, the procedure involves computerized scanning and XML tagging of systematic descriptions, which are so highly structured and consistent from genus to genus, that it is possible for an automated scan to recognize key components of the description because they are invariable in the same position and formatted in exactly the same way. A simple example of this automated data extraction with respect to stratigraphic data from taxonomic descriptions in the brachiopod Treatise, is the following XML-tagged extraction for the genus Pseudolingula (from Holmer and Popov 2000):

Ordovician

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Llanvirn-Ashgill . All the XML tags (shown here in italicized capitals enclosed within angle brackets, < . . . >) have been inserted automatically into the original text (shown in bold text here) by an XML parser than recognizes stratigraphic information and can label the separate components of the cited stratigraphic range (i.e., the particular stages: Llanvirn and Ashgill, which are subsections of the Ordovician Period). The confirmed = “true” indicates whether or not there is any doubt about the stratigraphic distribution, which is indicated in the text by a “?” The XML parser recognizes the stratigraphic information from its position (immediately after the taxonomic description, following a full stop) and from its formatting (all the text is italicized, and the stages are enclosed within brackets). The big advantage of this procedure is that it is fast, captures the original information without having to recode the data, and can handle even very complicated data (Curry and Connor 2007, 2008). Thus, for a slightly more complicated stratigraphic distribution such as the genus Wadiglossa, which occurs in parts of two geological periods (Holmer and Popov 2002), the following XML tagging captures all the relevant information:

Devonian Frasnian

Lower Carboniferous Tournaisian

. Thus, this genus first appears in the Frasnian Stage of the Devonian Period, and is last recorded in the Tournaisian Stage of the Carboniferous

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Period. Once the entire taxonomic description has been tagged using XML for all the genera in the Treatise, the entire dataset can be interrogated to generate a file of all stratigraphic data much more quickly than would be possible to achieve manually, and with complete fidelity to the original published data, which in the case of the Treatise publications has been subjected to comprehensive review not just by the original author but also by the compiler of the Treatise summaries. The end result of all this processing is a series of Microsoft Excel™ spreadsheets that contain, inter alia, the names, authors, and stratigraphic ranges of all brachiopod genera. For the purpose of this exercise all doubtful genera, and all genera with question marks about their stratigraphic range, have been excluded (as described in Curry and Brunton 2007). The result is a data set of 4,226 brachiopod genera, and it is this has been used for the analyses presented in this chapter.

STANDARDIZING THE DATA

A key issue for any analysis of this sort is to minimize inherent variability to ensure that the data being analyzed are as internally consistent as possible. Compiling the brachiopod Treatise was an enormous task, spanning 19 years from planning to completion, and involved about fifty authors from numerous countries. It would have been easy for the resulting data to be so heterogeneous as to make it impossible to compare different parts of the data set with any confidence (a problem facing all palaeontological studies that attempt to analyze data from widespread geographic locations or long stratigraphic ranges). However, a number of key decisions were taken during the preparation of the taxonomic work that were crucial in achieving as high a degree of standardization as is possible with such information.

STANDARDIZED TERMINOLOGY

The authors of the revised brachiopod Treatise discussed and agreed on a standardized glossary of taxonomic terms to be applied to brachiopods (e.g., Brunton et al. 1996). This glossary was not only circulated to all participating authors prior to the writing of the Treatise descriptions

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but also published in the first volume of the series. Morphological and anatomical terms used to describe brachiopods (Williams and Brunton 1997) were subdivided into: . those that can be used for any taxon in the way that they were defined; . those that can normally be used for any taxon, at least to class level within the phylum; . those that describe a feature generally specific to a particular taxonomic group or groups; . those that were considered obsolete. A big advantage of the Treatise format is that the current authors prepare new or revised diagnoses for all published brachiopod genera. As a result, the agreed modern terminology was applied across all brachiopod genera irrespective of their date of first description. This resulted in an unrivaled consistency in use of morphological terms across the more than five thousand genera in the phylum, and it minimized one of the common artifacts introduced by taxonomic procedures.

STANDARDIZED STRATIGRAPHIC COLUMN

The Geological Time Scale, subdividing the ancient history of the Earth over some 3,850 million years, is a rapidly developing science. While everyone welcomes advances in radiometric dating, astronomical dating, and stratigraphic procedure that produced much more accurate and rigorously defined stratigraphic boundaries, such changes are another source of complication for studies of ancient biodiversity. Such variations are by no means trivial, as demonstrated by the fact that the most recent compilation of the Geologic Time Scale (Gradstein et al. 2004; Gradstein and Ogg 2004) provided absolute age ranges for seven out of a total of eleven geological periods that were completely different and nonoverlapping with those published just over 70 years ago (Holmes 1937). With two other periods being cited at radically different ages, it is clear that there have been huge changes in the absolute dating of geological history. Similarly dramatic changes are noticeable in stratigraphic zonation, and the complications are even greater than with the absolute dating scale, as some countries use their own classifications and nomenclatures, which make global correlations very difficult.

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Such problems are particularly acute for global compilations such as the Treatise, and again it was essential for meaningful analyses to standardize the stratigraphic data. A detailed description of how this was achieved has been given by Curry and Brunton (2007), but again the global stratigraphic compilation published in 1989 by the International Union of Geological Sciences (IUGS) in 1989 (Cowie and Bassett 1989) was used as the designated standard. All stratigraphic ranges of brachiopods in the Treatise were either prepared using this zonation system or mapped onto it by the author using a single, consistent correlation scheme (for those genera when the diagnoses unavoidably had to use a different stratigraphic nomenclature). It was important to have as accurate and as refined a stratigraphic framework for this analysis, as it has been shown that updated geochronology does have a significant effect on palaeodiversity analysis (Johnson et al. 2008). As a result, the stratigraphic distribution of all brachiopod genera were mapped onto a zonation that divided the Cambrian to Recent (i.e., 542 million year) geological history of brachiopods into 113 census points, overwhelmingly corresponding to named stratigraphic stages in the 1989 International Union of Geological Sciences (IUGS) chart, with widely accepted refinements in common use up to 1999 (Curry and Brunton 2007). In absolute terms, the mean duration of each stage is 4.8 million years (standard deviation = 3.3 million years), and the stages range in duration from 18.4 million years to 0.2 million years. However, absolute age ranges are not the primary concern here; as discussed earlier, these are constantly changing as new and more refined techniques of absolute age dating are developed. Much more significant is being able to compare the global occurrences of brachiopod genera in individual well-defined subdivisions of geological history that are identifiable globally. The data are not perfect, but they are as good as can be achieved and are a major improvement on previous compilations.

STRATIGRAPHIC DISTRIBUTION OF BRACHIOPODS

Based on this analysis, the overall pattern of brachiopod distribution throughout their geological history reveals a pattern of major “radiations” and “extinctions” (Fig. 11.1). The geological history of brachiopods is characterized by major increases in diversity at the beginning of the Ordovician Period, within the Devonian Period, and at the beginning

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Ordovician

Devonian

Permian 500 400

Extinction

Extinction

Extinction 300 200 100

Cambrian

0 Recent

FIGURE 11.1 Stratigraphic distribution of all brachiopod genera in the Treatise on Invertebrate Paleontology, part H (revised), plotted on a horizontal stratigraphic scale, with the earliest Cambrian Period on the left and the present day on the right. Approximately time span is 542 million years. Vertical axis shows number of genera in each stratigraphic unit. Three major peaks of brachiopod diversity in the Ordovician, Devonian, and Permian Periods are labeled, as are three major extinction events. Most periods begin and end at an extinction event—a legacy of the original definition of geological periods based solely on fossils. Modified from Curry and Brunton 2007.

of the Permian Period, and a variety of other intervals in which the number of brachiopod genera increased to a lesser extent (Fig. 11.1). Similarly there are a number of stratigraphic intervals in which the number of brachiopod genera declined significantly and comparatively rapidly— most particularly at the end of the Ordovician, in mid-Devonian, and at the end of the Permian Period (labeled as “Extinctions” in Fig. 11.1). These are all well-known biodiversification and extinction events in the geological history of marine organisms, consistent with those highlighted by the “Sepkoski Curve” of Phanerozoic marine diversity (Sepkoski 1993), which has been widely accepted as a reliable summary of the palaeodiversity of marine organisms from the Cambrian Period to the present day. The first significant increase in brachiopod diversity occurred during the Great Ordovician Biodiversification Event in which many phyla apart from brachiopods increased their diversity very significantly (Webby et al. 2004; Harper 2006), while the first major decline occurred during the end-Ordovician (Hirnantian) glaciation, the culmination of a global climatic cooling that brought about a dramatic reduction in the diversity of many organisms that had evolved during prolonged intervals of Earth history characterized by predominantly warm global climates (Sheehan 2001; Brenchley 2004).

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Similarly, many phyla record pronounced diversification and decline within the Devonian, which has been attributed to a variety of factors such as exploitation of changing habitats and conditions during a number of pronounced marine transgressions, followed by periods of generic reduction resulting from the widespread development of anoxic conditions in the ocean (House 2002). All but one of the seventeen orders of brachiopod present in the Devonian diversify markedly in the early part of the period, and the phylum reaches its maximum ever diversity before declining to the point that there are fewer recorded genera at the end of the period than at the beginning (Fig. 11.1, modified from Curry and Brunton 2007). In the Permian Period, brachiopods initially flourished, adopting a range of different lifestyles and achieving their second greatest diversity after the Devonian (Fig. 11.1). However environmental conditions fluctuated hugely during the Permian, ranging from greenhouse to icehouse conditions, and the decline in brachiopod numbers in the Late Permian culminated in the Permian-Triassic mass extinction, the biggest mass extinction to affect brachiopods and many other phyla (Wignall and Hallam 1992; Wignall 2001; Erwin et al. 2002; Shen et al. 2006). It is possible that the patterns of diversity of Ordovician, Devonian, and Permian are influenced by factors such as exceptional preservation and ready accessibility of richly fossiliferous sediments, but it is also of interest to investigate the extent to which taxonomic practice has had an impact. It would be easy, for example, for palaeontologists to be influenced by the prevailing perceptions of the Early Ordovician, Early Devonian, or Early Permian as times of rapid diversification, and hence be more likely to describe new taxa from such successions. In an extreme situation, the patterns of biodiversification and extinction would essentially become self-reinforcing. There remains some concern that apparent biodiversification and extinction events in the geological record are, to an unknown extent, a reflection of preservational, monographic, and computational bias (Ager 1988).

BRACHIOPOD ORDERS

Testing for artifacts such as this sort of monographic bias is very difficult for five thousand brachiopod genera described by hundreds of taxonomists over more than 200 years. Having standardized the stratigraphic framework as far as is possible, the interest therefore was in examining

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the stratigraphic distribution of individual brachiopod orders, at which level it is possible to investigate the influences of individual brachiopod taxonomists. Many brachiopod orders have relatively straightforward stratigraphic distributions, involving one or more intervals of rapid diversification, followed by more or less drastic reductions in the number of recorded genera. Many of these events can be correlated with major global biodiversification or extinction events (i.e., as portrayed in the “Sepkoski Curve”; Sepkoski 1993) and at simplistic levels are attributed to major evolutionary or environmental events in Earth history affecting many phyla.

Order Strophomenida

A good example of this is the stratigraphic distribution of the Order Strophomenida. This order first appeared in the Ordovician Period, and representatives survived well into the Carboniferous. Over their 178-million-year history, the 307 genera assigned to the Strophomenida underwent two major radiations (Fig. 11.2): first, at the beginning of the Ordovician Period, during the Ordovician biodiversification event (Webby et al. 2004), and second, during the Devonian Period (Fig. 11.2). The Strophomenida were much reduced in diversity at the end of the Ordovician and again at the end of the Permian at the Permian-Triassic mass extinction. 120 100 80 60 40 20

Cambrian

Recent

0

FIGURE 11.2 Stratigraphic distribution of all Strophomenida brachiopods, plotted on a horizontal stratigraphic scale, with the earliest Cambrian Period on the left and the present day on the right. Vertical axis shows number of genera in each stratigraphic unit.

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Order Rhynchonellida

The situation is very different for the Order Rhynchonellida. A total of 644 genera are included in this order in the analyses presented here, over twice as many genera as in the Strophomenida, and Rhynchonellida genera survived for over 460 million years from the Early Ordovician through to the present day (with 19 extant genera). Unlike the Strophomenida, the Rhynchonellida have a major presence both in the Palaeozoic era (Permian and earlier periods) and in the post-Permian Mesozoic and Cenozoic Eras. However, the biggest difference is readily apparent in the plot of the stratigraphic distribution of Rhynchonellida (Fig. 11.3). The stratigraphic distribution of the Rhynchonellida is different from that of the Strophomenida, and in some respects it is somewhat bizarre (Fig. 11.3). There are numerous relatively rapid changes in generic diversity, but also in some periods there is more than one “cycle” of biodiversification and decline, which is not common. The most dramatic example of this is in the Devonian Period when the Rhynchonellida are at their most diverse. In Figure 11.3, there are two peaks of diversity in the Devonian, the earlier of which coincides with the interval in which overall brachiopod diversity reaches its maximum (Fig. 11.1). However, the second peak in Rhynchonellida diversity occurs in the latest Devonian (Fig. 11.3), during the stage when overall brachiopod diversity has dropped to its lowest level in the Devonian Period, and the

Devonian

70 60 50 40 30 20 10

Cambrian

Recent

0

FIGURE 11.3 Stratigraphic distribution of all Rhynchonellida brachiopods, plotted on a horizontal stratigraphic scale, with the earliest Cambrian Period on the left and the present day on the right. Vertical axis shows number of genera in each stratigraphic unit. The twin peak in diversity in the Devonian is labeled.

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diversity of all brachiopod orders except the Rhynchonellida were declining markedly (e.g., Alvarez 2006). While the first peak in the Devonian diversity of the Rhynchonellida conforms to that portrayed in the Sepkoski Curve, the second peak of diversity in the Devonian does not, as most organisms recorded declines during this stratigraphic interval. Such a pattern may indeed reflect some evolutionary or environmental event or events within, or ecological advantage for, Rhynchonellida as compared to other brachiopods, which would be of considerable scientific interest. But it is also possible that the “abnormal” patterns are a reflection of variations in taxonomic practice among Rhynchonellida specialists, and it is the new digital information extracted from the revised brachiopod Treatise that has been analyzed here to investigate the possibility of such monographic artifacts. AUTHORS OF RHYNCHONELLIDA GENERA

Since the first Rhynchonellida genus was described in 1809, just over two hundred authors have been responsible for the publication of formal taxonomic descriptions of the 644 genera in this analysis. Most of these genera were described in the latter part of the twentieth century, between 1950 and 2000 (Fig. 11.4). In particular, the three decades from 1970 up until 1990 saw 54 percent of all Rhynchonellida genera described (Fig. 11.5). There was a pronounced decline in the number of new

Cumulative number of Genera

700 600 500 400 300 200 100 0 1800

1850

1900 Year

1950

2000

FIGURE 11.4 Cumulative number of Rhynchonellida genera described from 1800 to the present day, showing the sharp increase in new genera since the 1950s.

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140

Number of Genera

120 100 80 60 40 20

18 0 18 0 1 18 0 2 18 0 3 18 0 4 18 0 5 18 0 6 18 0 70 18 8 18 0 9 19 0 0 19 0 10 19 2 19 0 3 19 0 4 19 0 50 19 6 19 0 7 19 0 8 19 0 9 20 0 00

0

Decade

FIGURE 11.5 Number of Rhynchonellida genera described in each decade from 1800 to the present day, with over one hundred new genera in the 1960s, the 1970s, and the 1980s. The last decade (2000) only includes genera described up to 2006, but it is clear that the peak of taxonomic activity has passed.

TABLE 11.1. authors of RHYNCHONELLIDA genera Ranked in Order of the Number of New Taxa Each Author Described

Author Sartenaer Havlícek Buckman Cooper Baranov

Dates

Number of Genera Described

Percentage of Total Genera

1961–2003 1959–1992 1906–1918 1942–1989 1977–1996

69 44 36 34 26

11 7 6 5 4

note: Data refer only to single-author genera; the range of years over which these descriptions were published is also shown.

genera in the decade from 1990 suggesting that the peak of Rhynchonellida taxonomic activity has passed, and indeed only eighteen genera have been described in the 7 years from 2000 until 2006 (Fig. 11.5). The dominant authors, in terms of the number of new genera described, are shown in Table 11.1. Sartenaer is the predominant author of new Rhynchonellida genera, having, over a career spanning over 40 years that still continues

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35 30 25 20 15 10 5

Cambrian

Recent

0

FIGURE 11.6 Stratigraphic distribution of new Rhynchonellida genera described by Sartenaer, plotted on a horizontal stratigraphic scale, with the earliest Cambrian Period on the left and the present day on the right. Vertical axis shows number of genera in each stratigraphic unit. Most taxa are concentrated in the Upper Devonian Period.

unrelentingly, described sixty-nine (11 percent) of the total number of genera. Havlícek has also contributed a large number of new genera (forty-four, or 7 percent) over a 30-year period, as did Cooper over 40 years (thirty-four, or 5 percent) and Baranov over 20 years (twenty-six genera, or 4 percent). Buckman stands out as having produced a comparatively high number of genera over a relatively short time frame, but this was due to the publication of a large number of new genera in a single major monograph, representing the culmination of many years of work. Extracting the genera authored by Sartenaer from the database, and plotting the stratigraphic distribution of these taxa, reveals that they all have a very restricted stratigraphic range. They are predominantly distributed in the upper Devonian (Fig. 11.6). Indeed, plotting the stratigraphic distribution of all other Rhynchonellida (i.e., excluding those described by Sartenaer) reveals that the second peak of diversity in the Devonian has mostly disappeared (Fig. 11.7). Most of the other authors listed have similarly restricted stratigraphic ranges—for example, Havlicek in the Ordovician (Fig. 11.8) and Buckman (Fig. 11.9) in the Cretaceous. Among the dominant authors of Rhynchonellida brachiopods, only Cooper has covered a wide range of stratigraphic stages (Fig. 11.10);

70 60 50 40 30 20 10

Cambrian

Recent

0

FIGURE 11.7 Stratigraphic distribution of all Rhynchonellida brachiopods (except those described by Sartenaer), plotted on a horizontal stratigraphic scale, with the earliest Cambrian Period on the left and the present day on the right. Vertical axis shows number of genera in each stratigraphic unit. The second peak in diversity in the Upper Devonian seen in Figure 11.1 has been greatly reduced.

25

20

15

10

5

Cambrian

Recent

0

FIGURE 11.8 Stratigraphic distribution of new Rhynchonellida genera described by Havlicek, plotted on a horizontal stratigraphic scale, with the earliest Cambrian Period on the left and the present day on the right. Vertical axis shows number of genera in each stratigraphic unit. Most taxa are concentrated in the Ordovician Period.

18 16 14 12 10 8 6 4 2 Cambrian

Recent

0

FIGURE 11.9 Stratigraphic distribution of new Rhynchonellida genera described by Buckman, plotted on a horizontal stratigraphic scale, with the earliest Cambrian Period on the left and the present day on the right. Vertical axis shows number of genera in each stratigraphic unit. Most taxa are concentrated in the Cretaceous Period.

8 7 6 5 4 3 2 1 Cambrian

Recent

0

FIGURE 11.10 Stratigraphic distribution of new Rhynchonellida genera described by Cooper, plotted on a horizontal stratigraphic scale, with the earliest Cambrian Period on the left and the present day on the right. Vertical axis shows number of genera in each stratigraphic unit. The diagram demonstrates the unusually wide stratigraphic range of Cooper’s taxonomic work on Rhynchonellida.

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and it is noticeable that apart from the single-author genera listed here, Cooper has a large number of additional new genera described in conjunction with a variety of collaborators. None of the other authors has collaborated to any significant extent with other workers in the description of new genera (e.g., Sartenaer has collaborated in the description of only five genera, as compared to the sixty-nine single author genera he has created; Table 11.1).

DISCUSSION

So the clear conclusion is that the activities of individual authors can have a pronounced effect on the stratigraphic distribution of brachiopods. More important, it means that simple extrapolations from range plots can be misleading, and that what is important is to have a detailed understanding of the nature of the stratigraphic record, of the taxonomy of the organisms, and of how particular authors deal with the inevitable uncertainties of both. Taking a simplistic approach is likely to generate spurious interpretation. This is well illustrated by the stratigraphic distribution of Rhynchonellida in the Devonian and the impact of Sartenaer’s work. The second Devonian peak in the stratigraphic distribution of this order may well at first sight be interpreted by the uninitiated as a rapid radiation following by an equally rapid decline during the Upper Devonian—events that may be seen as important evolutionary, environmental, or preservational phenomena. However a more rigorous investigation suggests something quite different. Sartenaer is predominantly a biostratigrapher, interested in using the distribution of fossils to help delineate stratigraphic boundaries that can be traced over wide geographic areas (e.g., Sartenaer 1987, 2000). Consequently, Sartenaer’s definition of genera gives more weight to a wide geographic distribution, while many authors do not consider this as an important criterion when describing new brachiopod genera. The bulk of Sartenaer’s work is concentrated on the uppermost parts of the Devonian Period, and because he has been so prolific, his work has had a discernible impact on the stratigraphic distribution of the Rhynchonellida. As indicated in the aforementioned analyses, such an impact by authors is not uncommon in Rhynchonellida. It is also clear, however, that over the history of Rhynchonellida research there have been

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numerous taxonomists who were either expert on Palaeozoic genera (i.e., Ordovician to Permian for this order), or on Mesozoic and Cenozoic genera (i.e., Triassic to Recent). But there are virtually none who worked across the entire range of Rhynchonellida geological history (Cooper being the sole example of an author with a wide stratigraphic range among the major authors of new genera; Table 11.1 and Fig. 11.10). In part, the predominance of regional, short stratigraphic range studies is a reflection of different nomenclatures and techniques being applied to Palaeozoic as compared to later Rhynchonellida, but despite significant efforts to overcome this artificial divide, it remains true that there have been very few taxonomic studies of Rhynchonellida brachiopods on a global scale or on a long geological timescale (Savage et al. 2002). As shown earlier (Figs 11.4 and 11.5), this does not mean that there has been any inhibition in describing new genera; indeed, the numbers of genera in the revised Treatise are nearly three times greater than were described in the previous Treatise (which was published only 37 years earlier). Authors have clearly tended to concentrate their activities regionally and in comparatively narrow stratigraphic ranges, which does pose difficulties for attempts to prepare global syntheses spanning long time periods. Over 87 percent of all Rhynchonellida genera included in this study are restricted to one geological period. This heterogeneity is understandable given the problems associated with comparing variably presented morphological information that differs in, for example, silicified specimens as compared to internal moulds or serial sections (Savage et al. 2002; Alvarez and Brunton 2008). This is a reflection of the fact that periods were originally defined by major changes in fossil diversity. But it is a phenomenon that does create significant problems when attempting to investigate the geological history of Rhynchonellida. Rhynchonellida may be an extreme example given the length of their geological history and the variation in the morphological features that are used, or are available to be used, in different parts of the stratigraphic column, but they are a warning for other orders in which the impact of monographic bias or other artifacts are not so obvious, but equally important for a wide range of applications. An obvious example for brachiopods is the monumental work by Cooper and Grant on the silicified Permian faunas of the Glass Mountains, Texas (Cooper and Grant 1969, 1974, 1975, 1976a, 1976b). Being silicified, the carbonate rocks could be dissolved away to reveal a range of fossils, a number of which would otherwise not be accessible, or so well preserved, in nonsilicified horizons.

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Undoubtedly, this preservational quirk has contributed to an extent to the peak in the diversity of Permian brachiopods (e.g., Fig. 11.1). Recognizing such phenomena can only improve analyses of the fossil record.

Acknowledgments

It is a pleasure to acknowledge the major scientific contribution made by Chris Humphries, for several years a close and valued colleague on the Systematics Association Council. I am also very grateful to Fernando Alvarez and Richard Connor for expert help and comments about brachiopods and computing, respectively.

REFERENCES Ager D.V. 1988. Extinctions and survivals in the Brachiopoda and the dangers of data bases. In: Larwood G. P., editor. Extinction and survival in the fossil record. Oxford: Clarendon Press pp. 89–97. Alvarez F. 2001. Athyridid diversity dynamics in the Prague Basin as shown by studies by Vladimír Havlícek. J. Czech Geol. Soc. 46: 105–108. Alvarez F. 2006. Forty years since Boucot, Johnson and Staton’s seminal paper “On some atrypoid, retzioid, and athyridoid Brachiopoda.” Palaeoworld 15: 135–149. Alvarez F., Brunton, C.H.C. 2008. On the reliability of reconstructing and comparing brachiopod interiors and their morphological variations based solely on serial sections. Proc. R. Soc. Victoria 120: 58–74. Benton M.J. 2004. The quality of the fossil record. In: Donoghue P.C.J., Smith M.P., editors. Telling the evolutionary time: Molecular clocks and the fossil record: Systematics Association Special Volume Series 66. London: Taylor and Francis pp. 66–90. Boucot A.J. 2006. So-called background extinction rate is sampling artifact. Palaeoworld 15: 127–134. Brenchley P. 2004. End Ordovician glaciation. In: Webby B.D., Paris F., Droser M.L., Percival I.G., editors. The great Ordovician biodiversification event. New York: Columbia University Press pp. 81–83. Brunton C.H.C., Alvarez F., MacKinnon D.I. 1996. Morphological terms used to describe the cardinalia of articulate brachiopods; homologies and recommendations. Hist. Biol. 11: 9–41. Cooper G.A., Grant R.E. 1969. New Permian brachiopods from West Texas I. Smithsonian Contr. Paleobiol. 1:1–20. Cooper G.A., Grant R.E. 1974. Permian brachiopods of West Texas, II. Smithsonian Contr. Paleobiol. 15: 233–793. Cooper G.A., Grant R.E. 1975. Permian brachiopods of West Texas, III. Smithsonian Contr. Paleobiol. 19: 795–1298 (part 1, text); 1299–1921, pl. 192–502 (part 2, plates).

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Sartenaer P. 1987. Re-examination of the castanea versus hippocastanea problem in the District of Mackenzie, and establishment of a new early-middle Givetian rhynchonellid genus. Bull. Inst. R. Sci. Nat. Belgique 57: 139–147. Sartenaer P. 2000. Revision of the rhynchonellid brachiopod genus Ripidorhynchus Sartenaer. Geol. Belgica 3: 191–213. Savage N.M., Mancenido M.O., Owen E.F., Carlson S.J., Grant R.E., Dagys A.S., Dong-Li S. 2002. Rhynchonellida In: Kaesler R. editor. Treatise on invertebrate paleontology, Part H (revised), Brachiopoda, vol. 4. New York and Lawrence, KS: Geological Society of America and University of Kansas Press pp. 1027–1376. Schopf J.W. 1992. Patterns of Proterozoic microfossil diversity: An initial, tentative, analysis. In: Schopf, J.W., Klein C., editors. The Proterozoic biosphere. Cambridge: Cambridge University Press pp. 529–553. Sepkoski J.J. 1975. Stratigraphic biases in the analysis of taxonomic diversity. Paleobiology 1: 343–355. Sepkoski J.J. Jr. 1993. Ten years in the library: New data confirm paleontological patterns. Paleobiology 19: 246–257. Sheehan P.M. 1977. Species diversity in the Phanerozoic: A reflection of labor by systematists? Paleobiology 3: 325–328. Sheehan, P.M. 2001. The Late Ordovician mass extinction. Ann.Rev. Earth Planet. Sci. 29: 331–364. Shen S.Z.C., Cao C-Q., Henderson C.M., Wang X-D, Shi G.R., Wang Y., Wang W. 2006. End-Permian mass extinction patterns in the northern peri-Gondwanan region. Palaeoworld 15: 3–30. Smith A.B. 2001. Large scale heterogeneity of the fossil record, implications for Phanerozoic biodiversity studies. Philos. Trans. R. Soc. Lond. B 356: 1–17. Smith A.B. 2007. Marine diversity through the Phanerozoic: Problems and prospects. J. Geol. Soc. Lond.164: 731–745. Smith A.B., Gale A.S., Monks N. 2001. Sea-level change and rock record bias in the Cretaceous: A problem for extinction and biodiversity studies. Paleobiology 27: 241–253. Webby B.D., Paris F., Droser M.L., Percival I.G. (editors) 2004. The great Ordovician biodiversification event. New York: Columbia University Press. Wignall P.B. 2001. Large igneous provinces and mass extinctions. Earth Sci. Rev. 53: 1–33. Wignall P.B., Hallam A. 1992. Anoxia as a cause of the Permo-Triassic mass extinction: Facies evidence from northern Italy and the western United States. Palaeogeogr. Paleoclimatol. Palaeoecol. 93:21–46. Williams A., Brunton C.H.C. 1997. Morphological and anatomical terms applied to brachiopods. In: Kaesler R., editor. Treatise on invertebrate paleontology, Part H (revised), Brachiopoda, vol. 1. New York and Lawrence, KS: Geological Society of America and University of Kansas Press pp. 423–440. Williams A., Brunton C.H.C., Carlson S.J., Alvarez F., Ansell A.D., Baker P.G., Bassett M.G., Blodgett R.G., Boucot A.J., Carter J.L., Cocks L.R.M., Cohen B.L., Copper P., Curry G.B., Cusack M., Dagys A.S., Emig C.C., Gawthrop A.B., Gourvennec R., Grant R.E., Harper D.A.T., Holmer L.E., Hou Hong-Fei, James M.A., Jin Yu-Gan, Johnson J.G., Laurie J.R., Lazarev S., Lee D.E., Mackay S., MacKinnon D.I.,. Manceñido M.O, Mergl M., Owen E.F., Peck

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L.S., Popov L.E., Racheboeuf P.R., Rhodes M.C., Richardson J.R., Rong Jia-Yu, Rubel M., Savage N.M., Smirnova T.N., Sun Dong-Li, Walton D., Wardlaw B., Wright A.D. 1997. Treatise on invertebrate paleontology, Part H (revised), Brachiopoda, vol. 1 (Kaesler R., general editor). New York and Lawrence, KS: Geological Society of America and University of Kansas Press. Williams A., Brunton C.H.C., Carlson S.J., Alvarez F., Ansell A.D., Baker P.G., Bassett M.G., Blodgett R.G., Boucot A.J., Carter J.L., Cocks L.R.M., Cohen B.L., Copper P., Curry G.B., Cusack M., Dagys A.S., Emig C.C., Gawthrop A.B., Gourvennec R., Grant R.E., Harper D.A.T., Holmer L.E., Hou Hong-Fei, James M.A., Jin Yu-Gan, Johnson J.G., Laurie J.R., Lazarev S., Lee D.E., Mackay S., MacKinnon D.I.,. Manceñido M.O, Mergl M., Owen E.F., Peck L.S., Popov L.E., Racheboeuf P.R., Rhodes M.C., Richardson J.R., Rong Jia-Yu, Rubel M., Savage N.M., Smirnova T.N., Sun Dong-Li, Walton D., Wardlaw B., Wright A.D. 2000. Treatise on invertebrate paleontology, Part H (revised), Brachiopoda vols. 2 and 3 (Kaesler R., general editor). New York and Lawrence: Geological Society of America and University of Kansas Press. Williams A., Brunton C.H.C., Carlson S.J., Alvarez F., Ansell A.D., Baker P.G., Bassett M.G., Blodgett R.G., Boucot A.J., Carter J.L., Cocks L.R.M., Cohen B.L., Copper P., Curry G.B., Cusack M., Dagys A.S., Emig C.C., Gawthrop A.B., Gourvennec R., Grant R.E., Harper D.A.T., Holmer L.E., Hou Hong-Fei, James M.A., Jin Yu-Gan, Johnson J.G., Laurie J.R., Lazarev S., Lee D.E., Mackay S., MacKinnon D.I.,. Manceñido M.O, Mergl M., Owen E.F., Peck L.S., Popov L.E., Racheboeuf P.R., Rhodes M.C., Richardson J.R., Rong Jia-Yu, Rubel M., Savage N.M., Smirnova T.N., Sun Dong-Li, Walton D., Wardlaw B., Wright A.D. 2002. Treatise on invertebrate paleontology, Part H (revised), Brachiopoda, vol. 4 (Kaesler R., general editor). New York and Lawrence, KS: Geological Society of America and University of Kansas Press. Williams A., Brunton C.H.C., Carlson S.J., Baker P.G., Boucot A.J., Carter J.L., Gourvennec R., Hou Hong-Fei, Jin Yu-Gan, Johnson J.G., Lee D.E., MacKinnon D.I., Racheboeuf P.R., Rong Jia-Yu, Smirnova T.N., Sun Dong-Li. 2006. Treatise on invertebrate paleontology, Part H (revised), Brachiopoda, vol. 5 (Kaesler R., general editor). New York and Lawrence: Geological Society of America and University of Kansas Press. Williams A., Brunton C.H.C., Carlson S.J., Alvarez F., Ansell A.D., Baker P.G., Bassett M.G., Blodgett R.G., Boucot A.J., Carter J.L., Cocks L.R.M., Cohen B.L., Copper P., Curry G.B., Cusack M., Dagys A.S., Emig C.C., Gawthrop A.B., Gourvennec R., Grant R.E., Harper D.A.T., Holmer L.E., Hou Hong-Fei, James M.A., Jin Yu-Gan, Johnson J.G., Laurie J.R., Lazarev S., Lee D.E., Mackay S., MacKinnon D.I.,. Manceñido M.O, Mergl M., Owen E.F., Peck L.S., Popov L.E., Racheboeuf P.R., Rhodes M.C., Richardson J.R., Rong Jia-Yu, Rubel M., Savage N.M., Smirnova T.N., Sun Dong-Li, Walton D., Wardlaw B., Wright A.D. 2007. Treatise on invertebrate paleontology, Part H (revised), Brachiopoda, vol. 6 (Selden P., general editor). New York and Lawrence, KS: Geological Society of America and University of Kansas Press.

T W E LV E

Diana Lipscomb

T H E E U K A R YO T E T R E E O F L I F E

By the early 1990s, it was becoming clear that the commonly used five kingdom classification schemes were oversimplified and simply inadequate for describing the major divisions of life. At this critical point in time, when morphological data from electron microscopy was beginning to be supplemented with information from DNA sequences, Chris Humphries organized a Linnean Society conference entitled “Modern Views of Kingdoms and Domains” in the spring of 1994 to discuss the new, emerging picture of eukaryotic relationships. The aim of this chapter is to review the general history of the debate over the eukaryote tree of life and describe the progress we have made since that historic conference.

HOW MANY KINGDOMS IN THE TREE OF LIFE?

When Carl Linnaeus presented the catalog of all life using his binomial system of nomenclature in 1758, he described two kingdoms: Plantae and Animalia. He included in the plant kingdom all those forms that are nonmotile and photosynthetic. The animal kingdom contained organisms that are heterotrophic and motile. At the time these definitions Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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FIGURE 12.1 Morphological and molecular data indicate that eukaryotes can be subdivided into seven major groups, but the relationships among them are still largely unresolved, and the position of the root of the tree is uncertain. Opisthokonts have a single posterior flagellum when motile cells exist, mitochondria with flattened cristae, and a unique amino acid insertion in the protein EF1alpha. Amoebozoa have blunt and fingerlike pseudopodia (called lobopodia) for at least part of their life cycle. Eukaryotic photosynthesis first evolved in the Archaeplastida. Excavates have a groove or inpocketing at their anterior end into which they suspension feed using a flagellum, but they rarely form a well-supported monophyletic group in molecular. Alveolates have a cell membrane system that consists of a layer of membrane-bound sacs (alveoli) lying just beneath the plasma membrane. Rhizaria are united by molecular data, and many have thin anastomosing pseudopods (reticulopodia or filopodia). Stramenopiles have a unique flagellum decorated with hollow tripartite hairs, and they use of ß-1,3 (or 1,6) linked glucans as a storage product Stramenopiles that are photosynthetic have chlorophyll a, c1 and c2, thylakoids in stacks of three, and four membranes surrounding the chloroplast with the outermost membrane continuing around the nucleus.

seemed to be obvious, and Lamarck, Cuvier, and most other eighteenthand nineteenth-century biologists placed all the large, obvious organisms in one of these two kingdoms. But as the twentieth century drew near, the discovery and description of new taxa led some biologists to

T H E E U K A R YO T E T R E E O F L I F E / 2 2 1

conclude that the two-kingdom system did not accurately represent all organisms, especially the microscopic unicellular taxa. The unicellular eukaryotes were discovered approximately 300 years ago by Antony van Leeuwenhoek (1632–1723), who considered them to be tiny animals that he called simply “animalcules.” Goldfuss (1817) introduced the name “protozoa” (in Greek, proto means “first,” and zoon means “animal”), but he applied it to a variety of simple organisms, including unicells, sponges, cnidarians, rotifers, and bryozoans. After the cellular nature of living organisms was uncovered and the distinction between unicellular and multicellular organisms was clarified, von Siebold (1845) restricted the protozoa to the “one-celled animals,” considering them to be invertebrates with the most primitive type of organization. As new unicellular forms were described, it became obvious that the protozoa are diverse organisms with divergent lifestyles, morphologies, habits, and reproductive cycles. Scientists began to doubt that all these organisms could be primitive animals or even that they were all closely related to each other and proposed changes to the two-kingdom scheme (Owen 1859; Hogg 1860; Wilson and Cassin 1863; Haeckel 1866). In some new systems, a new third kingdom was formed that was simply a catchall for taxa that were troublesome in the two-kingdom system. Owen (1859) called this the Protozoa; but, since that name was already in use to indicate primitive animals, Hogg (1860) established another name, the Regnum Primigenum. The Regnum Primigenum included two groups: the Amorphoctista (sponges) and the Protoctista (fungi, lower algae, bacteria, and unicellular organisms). Haeckel (1866, 1876, 1894, 1904) tried to create a higher-level classification reflecting phylogeny and evolution. He accepted the idea that life had a single origin and called the hypothetical ancestor of all life the Archigonic Monera. From the Archigonic Monera, he derived what he thought were three monophyletic kingdoms: Protista, Plantae and Animalia. The name protista eventually became synonymous with unicellularity, but this was not its original definition. Haeckel’s kingdom Protista included organisms that he believed lacked sexual reproduction (Haeckel 1876: 69). Into this group, he put the “Neutral Monera,” amoebae, flagellates, labyrinthulids (slime nets), diatoms, Myxomycetes (slime molds), heliozoans, radiolarians, and foraminiferans. The Neutral Monera were the most primitive protists because they lacked nuclei. They included bacteria, enucleated amoebae, and the hypothetical ancestors to the other protists. Haeckel considered the Protista to be a separate monophyletic lineage and not the ancestors of the plants or animals. Instead, he included

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within the plant and animal kingdoms those unicellular forms he believed to be ancestral or related to the multicellular organisms. For example, Haeckel’s plant kingdom included the hypothetical ancestor (“Vegetable Monera”) as well as those organisms he considered to be its descendants, including the cyanobacteria and the unicellular members of the Chlorophyta (green algae) and Rhodophyta (red algae). Owen’s, Hogg’s, and Haeckel’s proposals for a third kingdom were generally not accepted. Kent (1880–1881) objected that the effect of creating a third kingdom was simply to replace a single indefinite boundary between plants and animals with two indefinite boundaries: one between plants and protists, the other between animals and protists. To this, Butschli (1880–1889) added the objection that the organisms grouped together within the third kingdom lacked a unifying characteristic and were far too diverse and fundamentally dissimilar for inclusion in the same group. Therefore, most scientists continued to use the twokingdom system in which the protozoa were included as a phylum of animals and algae were a division of plants. The development of more sophisticated staining techniques in the early twentieth century led to the discovery that the cells of bacteria and blue-green algae lack microtubules, chromosomes, mitochondria, plastids, nuclear membranes, and other membrane-bound organelles. Appreciation of the profound differences between prokaryotic and eukaryotic cells motivated scientists to begin again to question the adequacy of the kingdom-level classification system and to suggest a separate kingdom for the prokaryotes. One such proposal was made by Copeland (1938, 1947, 1956), who presented a classification with four kingdoms: Mychota, Protoctista, Plantae, and Animalia. The kingdom Mychota contained the prokaryotic organisms. Copeland originally (1938) used Haeckel’s term Monera for this group but later rejected it because Haeckel intended Monera to apply to a hypothetical ancestral organism, rather than to a kingdom, and because Haeckel’s own example of an extant moneranlevel organism was not even a prokaryote but an enucleated fragment of an amoeba (Copeland 1947, 1956). Copeland united the eukaryotes that do not have clear plant or animal characteristics into a single kingdom for which he originally used Haeckel’s term, Protista (Copeland 1938), but later switched to Hogg’s Protoctista because it was the older name (Copeland 1947, 1956). He subdivided the Protoctista into eight phyla: Rhodophyta, Phaeophyta (in which the chrysophytes, diatoms, and oomycetes were merged), Pyrrhophyta (the euglenids, dinoflagellates, and cryptomonads), Fungilli (the Apicomplexa, Microspora, Myxozoa,

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and Ascetospora), Opisthokonta (chytrids and relatives), Inophyta (higher fungi), Ciliophora, and Protoplasta (rhizopods, zooflagellates, and slime molds). In his 1938 paper, Copeland suggested that the sponges might be included in the kingdom Protoctista because they formed part of an evolutionary series with unicellular and colonial choanoflagellates and because their embryology seemed unique (Copeland 1938). Subsequently, he was convinced that the embryology of sponges was actually not aberrant and that they should be regarded as true animals (Copeland 1947, 1956). Copeland’s kingdom Protoctista was a “trashcan group” for eukaryotes that were neither plants nor animals. Several of Copeland’s contemporaries (e.g., Rothmaler 1948; Barkley 1949; Hutchinson 1966) modified his system by using Monera instead of Mychota, Protista instead of Protoctista, Metaphyta instead of Plantae, and Metazoa instead of Animalia, but the contents of the kingdoms to which the diverse names were applied were essentially the same. In one of the first classifications to recognize the unique morphology of the fungi, Jahn and Jahn (1949) recognized six kingdoms: Archetista (viruses), Monera (organisms without nuclei, that is, bacteria and blue-green algae), Protista (eukaryotes that are usually unicellular and lack the defining features of plants and animals, including the protozoa, green algae, red algae, and brown algae), Metaphyta (multicellular photosynthetic eukaryotes that are usually sessile), Metazoa (multicellular heterotrophic eukaryotes that are usually motile), and Fungi (the multinucleate eukaryotes in which cell walls or membranes dividing the cytoplasm into typical mononucleate cells are often absent or partial). Jahn and Jahn (1949: 7) thought that this six-kingdom system achieved more distinct boundaries between the kingdoms, but they also recognized that it had some of the same problems as the simpler systems. They admitted that it was difficult to draw a clear separation between the Protista and the plant kingdom because good reasons can be given for placing the unicellular chlorophytes (green algae) in either group. Moreover, the sponges and choanoflagellates could be placed in either the Protista or Metazoa because they saw a continuous gradation from solitary choanoflagellates through colonial choanoflagellates to true sponges. Furthermore, the Myxomycetes could be put in either the Protista or the Fungi because at one stage in their life history they are unicellular amoebas or flagellates and in another stage they are complex masses of spores. Jahn and Jahn (1949) did not say on what grounds they would resolve these questions, but they did include the chlorophytes, Myxomycetes, and choanoflagellates in their key to the protozoa.

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Whittaker’s (1969) well-known five-kingdom system is based on level of cellular organization (unicellular-multicellular) and on type of nutrition (autotrophic-ingesting heterotroph-absorptive heterotroph). The result is a classification almost identical to that of Jahn and Jahn (1949) with the following exceptions: Whittaker included the Myxomycetes in the Fungi rather than the Protista; he put the green, red, and brown algae in the Plantae instead of the Protista; and he did not regard the viruses as part of the tree of life. The kingdoms in Whittaker’s classification may be similar to those of Jahn and Jahn (1949); but, probably because he was an ecologist, the arguments he gives in support of his system are unique. Whittaker (1959, 1969) observed that, in a natural community, three major groups of organisms could be recognized: producers, consumers, and reducers. These three nutritional groups correspond to three major groups of multicellular organisms. The producers are the plants, the consumers are animals, and the reducers are fungi. Whittaker argued that adaptation to mode of nutrition has determined many of the fundamental characteristics of the multicellular organisms and, therefore, that nutrition should be used as the primary character to delineate kingdoms. After observing that members of a closely related group of unicells use all three nutritional modes, Whittaker argued that the cellular organization level, not nutrition, was the important theme in their evolution. In his initial classification, Whittaker (1959) suggested placing all unicellular forms in a single kingdom Protista but later (1969) followed Grant (1963), who modified Whittaker’s system by dividing unicellular forms into the prokaryotes (Monera) and eukaryotes (Protista). Whittaker maintained that classifications should not reflect phylogeny but instead level of adaptation (Whittaker 1969: 158). Nevertheless, his classification was widely accepted and reproduced in basic textbooks. Beginning in the late 1960s, data from transmission electron microscopy began to significantly contribute to our understanding of eukaryote phylogeny. Many researchers continued to recognize the Protista (or Protoctista) as a paraphyletic kingdom serving as an ancestral hub from which all other eukaryotic kingdoms are derived (e.g., Olive 1969; 1975; Margulis 1971, 1974; Margulis and Schwartz 1982, 1988; Corliss 1987). But increasingly, others became convinced that the “Protista” needed to be abandoned and a multiple-kingdom system must be devised. Leedale (1974) constructed a system in which the concept of lower and higher eukaryotes was abandoned and each kingdom was, as far as he could tell, monophyletic. The result was a nineteen-“kingdom” scheme that he considered to be a starting point for discussion rather than a

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completed system. Hence, only a selection of eukaryote phyla are shown, and the “kingdoms” have not been given proper names. Nevertheless, it was a revolutionary attempt to identify the major monophyletic lineages of eukaryotes. In another analysis of eukaryote relationships, Taylor (1976, 1978) made a genuine effort to give explicit reasons for every phylogenetic decision. Like Leedale, Taylor did not intend his phylogenetic tree to be a complete classification but rather an initial inquiry into the relationships of the eukaryotes. He provided detailed discussion of the variability and distribution of about twenty-five cell characteristics within the eukaryotes, but he found the data to be conflicting and difficult to interpret. Thus Taylor, like Leedale, was unable to produce a phylogeny in which the phylogenetic relationships of the eukaryotes were resolved, and he, too, presented many isolated lineages. Subsequently, some systematists attempted to use the ultrastructural data in more rigorous phylogenetic analyses (e.g., Lipscomb 1989, 1991; Taylor 1999; Dewel et al. 2003). All of these struggled with determining homology of organelles across such diverse lineages and with interpreting secondary loss of mitochondria, plastids and locomotory systems. Many of the major lineages found in these studies have also been recovered in more recent molecular analyses, but their relationship to each other remains elusive. For more than a decade, genetic sequence data has been used to reveal the phylogeny of the major lineages of eukaryotes. The first molecular papers heavily relied on small subunit RNA molecule that was considered ideal because it is found in all prokaryotes and eukaryotes, and is large enough (usually >1,500 bases) not to have become saturated with multiple mutations (e.g., Sogin 1989, 1991; Schlegel 1994). Using this gene and relatively few taxa, a ladderlike tree with three main sections was reconstructed. The basal section includes those taxa that lack mitochondria (diplomonads, microsporidians, and parabasialids). The central part of the tree includes the intermediate taxa, which have mitochondria but are still “evolutionarily primitive” such as Euglena and its relatives, the slime molds, and several taxa of the old amoeba group. The crown taxa include the multicellular organisms (fungi, animals, plants, red and brown algae) and the alveolates (ciliates, dinoflagellates, and apicomplexans). This tree was widely reprinted in basic textbooks and seemed to fit the endosymbiotic models of eukaryote evolution in which mitochondria were acquired relatively late and the ladderlike tree. Unfortunately, analyses using additional genes (e.g., large subunit ribosomal RNA, nuclear protein-coding

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genes and mitochondrial genomes), discrete molecular features (e.g., large insertion/deletions in protein sequences, lateral gene transfers or gene replacements, and gene fusions/fragmentations), and more taxa do not agree with its story of eukaryotic history (Steckmann and CavalierSmith 2002; Baldauf 2003; Philippe et al. 2004; Simpson and Roger 2004; Adl et al. 2005; Richards and Cavalier-Smith 2005). Our understanding of the number and content of the major eukaryote lineages is still a work in progress. Despite our failure to find a resolved, robust tree, both ultrastructure and molecules are making the major branches clear so that most diversity can be placed in a few very large supergroups or superkingdoms (see Fig. 12.1).

OPISTHOKONTA

The opisthokonts include the animals and true fungi as well as the unicellular choanoflagellates, nucleariid amoebae, Mesomycetozoa, Ministeria, and Capsaspora. The close relationship between animals and fungi was suggested in morphological studies that showed sponges, choanoflagellates, and chytrid fungi have as a synapomorphy microtubules radiating perpendicularly to the basal body and interconnected by concentric rings of electron-dense material (Barr 1981; Lipscomb 1989, 1991). Initially this relationship was weakly supported by small subunit ribosomal genes (Wainwright et al. 1993), but the trees lacked resolution and significant support for critical nodes (Lipscomb et al. 1998). More recently, phylogenetic analyses of combined multigene data sets recover the clade with stronger support but it now also includes a variety of protist genera (e.g., Lang et al. 2002; Medina et al. 2003; Phillipe et al. 2004; Rodriguez-Ezpeleta et al. 2005; Steenkamp et al. 2006; Hackett et al. 2007; Shalchian-Tabrizi et al. 2008; Yoon et al. 2008). These taxa are united by having a single posterior flagellum when motile cells exist (e.g., sperm, spores, or unicell bodies), mitochondria with flattened cristae, and a unique amino acid insertion in the protein EF1alpha. Within the opistokonts, animals form a monophyletic kingdom distinguished by septate cell junctions; extracellular matrix of collagen, spermatozoa, and basal bodies at right angles to each other in flagellated cells; and usually a blastula stage in development (Nielsen 1995). Their sister group is the choanoflagellates, small single-celled protists that live as individuals or colonies in both fresh and marine waters. A close relationship between animals and the choanoflagellates has been supposed

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since Dujardin (1841), and James-Clark (1866) noted similarities between choanoflagellates and feeding cells (choanocytes) of sponges. Both have a circle of closely packed microvilli forming a collar around the single flagellum; as the flagellum beats, it draws water through the microvilli, and food particles are filtered out. This relationship is supported by a variety of nuclear and mitochondrial genes such as the large subunit ribosomal DNA, elongation factor 1-A, actin, B-tubulin, and HSP70, A-tubulin (Lang et al. 2002; Medina et al. 2003; Phillipe et al. 2004; Steenkamp et al. 2006), mitochondrial genome architecture (Burger et al. 2003; Lavrov et al. 2005), and signaling and adhesion genes, and developmental proteins (King and Carroll 2001; King et al. 2003, 2008; Segawa et al. 2006; Snell et al. 2006). Molecular data have also confirmed that choanoflagellates are not derived from sponges (i.e., are not animals secondarily reduced to a unicellular grade) but instead are a distinct lineage that is the sister group of the animals (Lavrov et al. 2005; Rokas et al. 2005; King et al. 2008). Ministeria, a recently discovered small marine protist, and Capsaspora, a unicellular parasite isolated from snail hemolymph, form a clade that is sister to animals and choanoflagellates in multigene phylogenies (Shalchian-Tabrizi et al. 2008). Both Ministeria and Capsaspora have long filose pseudopods with filamentous cores and have been placed together in a new class, Filasterea (Shalchian-Tabrizi et al. 2008). Following from the animal–choanoflagellate–Minsiteria–Capsaspora clade is the Mesomycetozoa, an enigmatic group of protists that are mostly parasites of fishes, mammals and birds. They form a consistent group using molecular data but lack any clear morphological synapomorphy. The name of the group has also been indistinct; they have been called “the DRIP clade” (an acronym of the original members: Dermocystidium, rosette agent, Ichthyophonus, and Psorospermium) and the class Ichthyosporea (Cavalier-Smith 1998). Existing studies still contain few taxa and incomplete gene sequences, but there is an exciting possibility of learning more about the precursors of genes and domains involved in the morphogenesis of animals by studying the Mesomycetozoa and Filasterea (Shalchian-Tabrizi et al. 2008). Two unicellular groups (nucleariid amoebae and Microsporidia) are related to the fungi. The nucleariids are round amoebae with filose (thin threadlike) nonanastomosing pseudopodia, and they are found in soils and freshwater. Molecular studies indicate they are the sister group to the fungi (Amaral-Zettler et al. 2001; Hertel et al. 2002). Microsporidia are intracellular parasites found primarily in mammals, fish, arthropods,

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and other protists. They have a unique organelle, the polar filament that penetrates the host membrane and carries the spore contents into the host cytoplasm. Early molecular studies based on ribosomal sequences recovered them among the very earliest diverging eukaryotes. Because they also lack many of the typical eukaryote organelles (e.g., mitochondria, peroxisomes, and stacked Golgi dictyosomes), it was hypothesized that the Microsporidia diverged before the mitochondria was acquired by endosymbiosis. This hypothesis was rejected when additional gene phylogenies indicated that Microsporidia evolved within the Fungi (Keeling 2002; Keeling and Fast 2002; Keeling et al. 2005; but also see Tanabe et al. 2002). Microsporidia and Fungi also have similar meiosis (Flegel and Pasharawipas 1995), spores that contain chitin (Bigliardi and Sacchi 2001), and similar mRNA capping reactions (Hausman et al. 2002).

AMOEBOZOA

The Amoebozoa include those amoeboid forms with blunt and fingerlike, pseudopodia (called lobopodia) such as the large spectacular forms Amoeba proteus, Chaos, and Pelomyxa as well as amoeboflagellates living in low oxygen environments such as Entamoeba (Archamoebae) and slime molds (Mycetozoa) (Baldauf et al. 2000; Bapteste et al. 2002; Forget et al. 2003; Smirnov et al. 2005; Nikolaev et al. 2006). Because, when flagellated, cells tend to have just one flagellum, they have been united with opisthokonts (Stechmann and Cavalier-Smith 2003; Richards and Cavalier-Smith 2005), but the presence of two basal bodies in Breviata challenges this hypothesis (see Minge et al. 2009)

ARCHAEPLASTIDA

This group includes three highly distinct photosynthetic lineages: Rhodophyta, Glaucophyta, and Viridiplantae (Adl et al. 2005; Reyes-Prieto et al. 2007; Nowack et al. 2008). The Viridiplantae, or plant kingdom, includes the chlorophytes, charophytes, prasinophytes, and multicellular plants. All of these taxa have chlorophylls a and b, and alpha- (1-4)-linked glucan (amylose/amylopectin) as food storage in their chloroplasts. Just two membranes, as in the rhodophytes and glaucophytes, bound the chloroplast, but the thylakoids are in many-layered grana. Flagellated cells have a stellate flagellar transition region and a cruciate flagellar root system.

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The red algae (Rhodophyta) are a morphologically diverse group that includes small unicellular and filamentous forms, as well as those with large thalli (including calcified crustose and erect forms). They are characterized by chloroplasts bounded by two membranes containing separate thylakoids and lacking an external coat of endoplasmic reticulum (Dodge 1973; Pueschel 1990). They have chlorophyll a (no chlorophyll b), alpha- and beta-carotene, leutein, and zeaxanthin. Other pigments include the water-soluble allophycocyanin, phycocyanin, and phyrierythrin localized in phycobilosomes found on the thylakoids of the chloroplast. Floridean starch is the major storage product and it is found in the cytoplasm rather than the chloroplast. This carbohydrate has a primary chain of alpha- (1,4)-linked glucans with a 1,6-linked branched chains (Raven et al. 1990). There are no flagella, centrioles, or basal bodies, so it is not surprising to find that mitosis in red algae is different from that in Viridiplantae. The spindle forms on a unique nucleus associated organelle (called the NAO), which is located on each division pole. The nuclear membrane remains intact except for small openings at the pole for the spindle to pass through (Scott 1983). Because of this unique morphology, the position of the red algae in the eukaryote phylogenetic tree has been controversial. Molecular studies indicate that the chloroplasts of red algae and Viridiplantae are related, but support from ribosomal or nuclear genomes has been relatively weak (Lipscomb 1998; Baldauf 2000; Rodriguez-Ezpeleta et al. 2005). The Glaucophytes are flagellated, coccoid, and palmelloid freshwater organisms. Like the red algae, their plastids have two membranes, phycobiliproteins, unstacked thylakoids, and just chlorophyll a. The chloroplasts are sometimes called “cyanelles” because they retain a bacterial-like peptidoglycan cell wall between the inner and outer membranes (Steiner et al. 2005). They are not common and are poorly studied; therefore, the relationships between red algae, plants, and glaucophytes are still poorly understood.

“RAS” (RHIZARIA + ALVEOLATES + STRAMENOPILES) (BALDAUF 2008)–“SAR” (STRAMENOPILES + ALVEOLATES + RHIZARIA) (BURKI ET AL. 2007)

The alveolates and stramenopiles are two of the large and diverse groups that have been hypothesized as sister taxa (Patterson 1999; Taylor 1999; Baldauf 2003; Keeling 2004; Harper et al. 2005). Furthermore,

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expressed sequence tag data indicate that this clade, in turn, may be sister to the Rhizaria (= Amoebozoa) (Burki et al. 2007; Hackett et al. 2007). This whole clade has not been formally named and is often called by the acronym formed from the first letter of each of the included groups: SAR (Burki et al. 2007) or RAS (Baldauf 2008). Alveolates

The Dinoflagellata, Ciliophora, Apicomplexa have been linked as sister taxa on the basis of an alveolar membrane system that consists of a layer of membrane-bound sacs lying just beneath the plasma membrane and, beginning with Wolthers (1991), is consistently recovered in molecular studies. The dinoflagellates are a monophyletic group defined by the presence of unique nuclei that lack nucleosomes, have permanently condensed chromosomes and few histones. Platelike deposits of polysaccharide (usually cellulose) within the alveoli may form a permanent armour that give many dinoflagellates their distinctive rigid shapes. In most orders, the body is grooved equatorially to form a girdle occupied by the transverse flagellum. A second groove passes posteriorly from which a posteriorly directed longitudinal flagellum emerges. Some dinoflagellates are photosynthetic and contain chlorophyll a and c2 complex with a unique xanthophyll, peridinin. The ciliates make up one of the largest groups of protists. They are conspicuous members of microbial habitats and play a major role in microbial food webs as predators of bacteria, other protists, algae, and small invertebrates. Ciliate monophyly is supported by the presence of rows of cilia with a unique system of two microtubular and one fibrous roots, two kinds of nuclei (a micronucleus that functions in genetic exchange, and a macronucleus that functions in protein synthesis), a permanent cell mouth (called the cytostome) for ingestion of particulate food, genetic recombination by conjugation rather than gametes, and an equatorial cell division plane. The Apicomplexa are symbiotic and include many major disease-causing organisms (e.g., Plasmodium, which causes malaria). The anterior end of the cell contains a unique complex of organelles (called the apical complex) that function in attachment and penetration of the hosts’ cells. Stramenopiles

The stramenopiles are a diverse assemblage including brown seaweeds (Phaeophyta), diatoms (Bacillariophyta), other, mostly unicellular, golden

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algae (e.g., Chrysophyta, Synurophyta, Eustigmatophyta, Xanthophyta), and various nonphotosynthetic forms such as the oomycetes (formerly classified as fungi), labyrinthulids, bicosoecids, and actinophryids. It may also include the opalinids and their relatives, and the haptophytes. Morphological characters shared by most members of this diverse group are tripartite mastigonemes (hairs) on the flagellum, and use of B-1,3 (or 1,6) linked glucans as a storage product Those forms that are photosynthetic have chlorophyll a, c1, and c2; thylakoids in stacks of three; and four membranes surrounding the chloroplast with the outermost membrane continuing around the nucleus. Actinophryid helizoa lack chloroplasts and flagella, but both molecular and morphological information place them in the straminopile clade (Nikolaev et al. 2004). Because they have axopodia (radiating, thin pseudopods stiffened by complex arrays of microtubules), they were initially put in the superclass Actinopoda with the marine radiolarians, but both electron microscopy and molecular data have now shown that this is a polyphyletic assemblage. Instead, they are related to the helioflagellates (e.g., Ciliophrys), which tripartite mastigonemes on their flagella as well as axopodia and extrusomes similar to those found in actinophryids (Davidson 1982; Smith and Patterson 1986; Mikrjukov and Patterson 2001). Opalinids are common symbionts in the cloacae of amphibians and, because they have rows of cilia, were considered related to ciliates until electron microscopy revealed striking differences. The shared pattern of microtubules supporting folds in the cell membrane and the double transitional helix in the flagellar transition region indicate that opalinids are related to the Proteromonadidae. The posterior end of the proteromonad cell is covered with tubular hairs (the somatonemes) that resemble the mastigonemes on the flagella of straminopiles. Some molecular studies place the Proteromonadidae and opalinids in the stramenopiles (e.g., Silberman et al. 1996; Kostka et al. 2007), but the branch support is weak. Also known as prymnesiophytes, Haptophyta (coccolithophorids and relatives) have been grouped with other Chromista because they have chlorophyll c and similar storage products. However, they lack other ultrastructural features found in the group and have a unique haptonemal complex, so it may be that they are a separate line whose chloroplasts are derived from similar endosymbionts. Based on morphological and swimming behavioural differences, the position of this group has been in question for some time (see Hibberd 1979).

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Rhizaria

Small subunit RNA and actin genes indicate that very diverse organisms including filose testate amoeba, cercomonads, chlorarachniophytes, cercozoan, foraminiferans, and their relatives, the gromiids, plasmodiophorids (= Phytomyxea), haplosporidians, and radiolarians, can be united into a clade (Bhattacharya et al. 1995; Keeling 2001; Burki et al. 2002; Longet et al. 2003; Nikolaev et al. 2004; Ald et al. 2005). These are mostly amoeboflagellates with thin anastomosing pseudopods (reticulopodia or filopodia), but the group is not united by a clear morphological synapomorphy.

EXCAVATES

This group includes Euglenozoa, Heterolobosea and jakobids, Fornicata, and Axostyla. It was proposed because its members have a groove or inpocketing at their anterior end into which they suspension feed using a flagellum (Simpson 2003), but they rarely form a well-supported monophyletic group in molecular analyses (see Parfrey et al. 2006). Some of the subgroups are robust. The Euglenozoa includes kinetoplastids and euglenids, despite the fact that the better-known euglenoid flagellates are photosynthetic (e.g., Euglena) and that the kinetoplastids include heterotrophic parasites such as Trypanosoma and Leishmania, these two groups have been recognized as related taxa for some time (e.g., Leedale 1967). The morphological features they share include linked microtubules underlying the cell membrane and discoidal cristae in the mitochondria. The Heterolobosea are amoeboid or amoeboflagellate cells with “eruptive” pseudopodia (Page and Blanton 1985). Most are soil or freshwater bacterivores (the human pathogen, Naegleria fowleri, is a notable exception), The inclusion of the acrasid slime molds in this group is supported by morphological data (Page and Blanton 1985; Page 1978), and molecular data from glyceraldehyde-3-phosphate dehydrogenase (Roger et al. 1996), tubulin (Roger et al. 1999; Keeling and Doolittle 1996), CCT chaperonins (Archibald et al. 2002), and EF1a (Roger et al. 1999). Jakobids are small free-living protists with two flagella, one of which has the surrounding cell membrane extended into a vane and is posteriorly directed in a ventral groove (O’Kelly 1993). A complex, microtubular cytoskeleton supports the cell’s shape. Their mitochondrial genome retains more than one hundred protein-coding genes, and these are arranged like bacterial operons (Lang et al. 1997).

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Simpson (2003) grouped together some anaerobic unicellular heterotrophic flagellates formerly placed in independent lineages (including Carpediemonas, Dysnectes, Retortamonas, some diplomonads, and possible the parabasillids) into a group called the fornicates. Many of its members (e.g., Giardia) were once considered to represent basal, primarily amitochondriate eukaryotes, the so-called Archezoa. However, it has been shown that this is a secondary loss, rather than the primitive condition. Small subunit RNA genes unite the oxymonads and Trimastix (Dacks et al. 2001). Axostyla includes the oxymonads live almost exclusively in the hindgut of wood-eating insects such as Cryptocercus and termites, while Trimastix (= Tetramitus) is found in anoxic and microaerophilic marine and freshwater habitats.

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PA R T F O U R

BIOGEOGRAPHY

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THIRTEEN

Peter L. Forey

TETHYS AND TELEOSTS

The title of this volume, Beyond Cladistics, is somewhat enigmatic as it may imply preference for systematic methodologies that are outside the traditional practices of cladistics, such as maximum likelihood or Bayesian analysis. It may also imply that there are deep methodological issues within the cladistic realm that remain to be resolved, and this may be true since cladistics is an evolving discipline, and other contributors may well take up some of these. But, as a palaeontologist, I prefer to live in the past and believe that cladistics in its current form is alive and well. For the purposes of this essay, my interpretation of “beyond cladistics” is to use cladograms as phylogenetic trees—that is, as theories of relationship tied to time—and to try and answer questions of tempo and mode of evolution, or the nature of change through time. Given phylogenetic trees, there are a number of lines of inquiry that may be pursued. Although far from exhaustive, there are some immediate questions: 1. Do phylogenetic trees reflect or direct our views of Earth history, either the quality of the fossil record or the implication for palaeobiogeographic inference?

Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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2. Can phylogenetic trees imply anything about the rate of taxic diversity through time? 3. Can phylogenetic trees imply anything about the rate of morphological evolution through time? The first two areas of questioning rely on the existence of a phylogenetic tree but one that is not necessarily inferred through cladistic methodologies, since it is the shape of the tree that is the crucial element. However, for the past 40 years cladistics (or phylogenetic systematics) has been the preferred methodology since the emphasis on delimiting monophyletic groups strips away the subjectivity inherent in paraphyletic “evolutionary grades” that characterized former attempts at analyzing tempo and mode of evolution (e.g., Simpson 1944). For the third area, then, the character information provided by cladistic methodology is crucial to the answers. To exemplify the use to which phylogenetic trees may be put, I am going to look at the evolution of lower teleost fishes through the Cretaceous. First I will briefly explain what these animals are and then why they are of interest to such endeavors. Teleost fishes are the dominant fishes of today—they are the angiosperms of the vertebrate world. There are about 23,000 modern species with a record dating back some 210 million years to the late Triassic. However, they are relatively rare for the first 50 million years of their existence and, as recorded in the fossil record, their history did not really get going until the late Jurassic, about 150 million years ago. During the late Jurassic and the succeeding Cretaceous period, many of modern groups of teleosts appeared. Figure 13.1 outlines some of the elements of this early history: the spindles reflect the relative abundance, as measured by numbers of families through time, and the phylogeny given at the bottom shows a commonly accepted diagram of relationships delimiting monophyletic crown groups from Osteoglossomorpha at the left to Myctophiformes to the right. Collectively these teleosts are known as “lower teleosts,” which is admittedly a paraphyletic assemblage; it includes such familiar food and sport fishes as herrings, true eels, minnows, catfishes, salmon, and trout, as well as the less familiar viperfishes and lantern fishes. Within this paraphyletic assemblage there are many smaller monophyletic clades, including some that are extinct, successively more closely related to crown group teleosts. It is from these smaller monophyletic clades that the following examples are drawn since they have been the subject of phylogenetic work and the fossil record, by vertebrate standards, is good.

FIGURE 13.1 Teleost phylogeny. Top. Spindle diagram showing the number of families of modern groups of lower teleosts through time. Note that the Cretaceous (greyed area) witnessed the early radiations of many of these groups. Bottom. Phylogeny of lower teleosts. Those lineages starred are used as examples in the text. Based on Patterson (1994).

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Although not the subject of discussion, it is worth emphasizing that the majority of teleosts (sixteen thousand modern species) belong in the clade Acanthomorpha. These are the spiny-rayed teleosts (cod, plaice, tuna, snapper, bass, and perches are familiar examples). The acanthomorphs had their origin in the mid-Cretaceous but did not really diversify until the early Tertiary. For my purposes here, these are less useful for two reasons. First, the phylogeny for many of the spiny-rayed teleosts is far from resolved, and since this essay is based on the availability of phylogenetic trees derived through cladistic analysis, these fishes are currently less suitable. Second, by far the greater part of acanthomorph evolution took place during the Cenozoic era, post-Tethys. Nevertheless, when such hypotheses become available, the acanthomorphs will probably provide even more useful evidence for general studies of tempo and mode of evolution. The phase of the early evolution of lower teleosts was taking place in a world of continental breakup and during times when there were very significant changes in sea levels and world temperatures. In fact, there were very few periods of Earth history as geologically active as the Cretaceous (Skelton 2003). In Figure 13.2, some of the major changes of geography are illustrated and, as I will show, can be correlated with the phylogenetic histories of various groups of lower teleosts. Some of the more productive localities are indicated as circles. A word about environments may be in order. Most palaeobiogeographers concentrate their attention on terrestrial or freshwater organisms because they are tied to landmasses that are recognizably easier to track through geological time. However, there is no reason why marine organisms should not be used, although with some caution. In the modern world many marine organisms are tied to narrow geographic areas by factors such as temperature, physical environmental parameters, light and salinity regimes, and so forth. For fishes, a glance through the many FAO (Food and Agriculture Organisation) guides in which geographic distributions are plotted show that most coastal (including reef fishes) are geographically tightly constrained. Indeed, for many fishes it is the oceanic basins that provide the barriers. Parenti (2008), in studying the evolution of diadromy in fishes (a situation where part of the individual life cycle is spent in freshwater, part in the sea), has argued that ecology plays a key role in cladistic biogeographic inference—a view that I endorse here. There must be a caveat to the expectation that all marine fish species are closely tied to coastlines. There are some examples where fishes are much more widely distributed. In the modern world, tuna,

FIGURE 13.2 Illustration showing major land–sea configurations through the Jurassic and Cretaceous during the evolution of Tethys. Major fish localities are indicated (a more complete inventory is in Cavin et al. 2007: Appendix 1): black circles are marine localities; white circles are freshwater (estuarine and deltaic are grouped with marine). Note that there is an increase in the number of localities in the mid-Cretaceous.

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sailfishes, and their allies are obvious examples. And many species of mesopelagic fishes, such as lantern fishes, have broad geographic ranges that spread throughout the world’s oceans. The fossil record does not readily preserve the mesopelagic or abyssal-dwelling fishes. The open water surface-dwelling oceanic fishes can often be recognized because of their morphology reflecting fast, continuous swimming. Thus, it is possible to screen out some of the fish groups as being less suitable for biogeographic inference. When teleosts originated in the late Triassic, the world’s continents that made up Pangaea were compact and surrounded by the single ocean of Panthalassa. By the mid-Jurassic at 175 million years ago (Fig. 13.2A), the large oceanic indent of Tethys had developed as continental masses began to separate into what were to become the northern and southern landmasses. By the late Jurassic at 145 million years ago (Fig. 13.2B), the northern continents were separating from the southern continents. Tethys was extending west to sever the Americas into North and South. By the early Cretaceous (120 million years ago; Fig. 13.2C), the present-day Southern Hemisphere continents were gaining their identity; for instance, India, Antarctica, and Australia were becoming distinct. In addition, and most important for this essay, a rift was opening up between South America and West Africa. By the mid-Cretaceous (92 million years ago; Fig 13.2D), the Tethys Ocean was fully developed between the Northern and Southern Hemisphere continents, leaving many large islands that were to become the Iberian Peninsula. The precise geographic location of these islands is not accurately known. At the same time, the North Atlantic was opening up, separating North America from Europe. This is the palaeogeographic background to early teleost evolution, so it is pertinent to ask how they responded. For some clades of lower teleosts, there is concordance between phylogeny and palaeogeography.

DISTRIBUTIONS Aspidorhynchids

The Aspidorhynchidae (Fig. 13.3) are an extinct group of teleosts known from the mid-Jurassic until the late Cretaceous and show a good match between phylogeny, geography, and time. The group is predominantly marine and consists of three genera and about eighteen species, and it

A. crassus

Eur

A. euodus

Eur

Aus Brz

Leb

B. crassirostris

B. sp

B. sp B. sp

B. dorsetensis

Mex

B. sphaeroides

V. sweeti

V. sp

V. sp

A. arawaki

Cub

Eur

Upper Jurassic

Ant

A.sp

A, fisheri

Lower Cretaceous

A. sphekodus

Middle Cretaceous

A. acutirostris

Aspidorhynchus

V. comptoni

Vinctifer

B. longirostris

Belonostomus

Ch N.Am

B. cinctus

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Eur

Mor

Mex

Eur

Arg

Eur

Middle Jurassic

FIGURE 13.3 Phylogeny of aspidorhynchid teleosts based on Brito (1997) with supplementary information from Forey et al. (2003). Some species have yet to be named. Geographic localities: Ant, Antarctica; Arg, Argentina; Aus, Australia; Brz, Brazil; Ch, Chile; Cub, Cuba; Eur, Europe; Leb, Lebanon; Mex, Mexico; Mor, Morocco; N. Am, North America.

has been most extensively revised in recent years by Brito (1997). We are uncertain of much of the species-level phylogeny, basically because species are poorly construed, being based on ornament patterns of scales and skull fragments rather than entire fishes. However, the genera are very well differentiated. In the Jurassic the plesiomorphic genus Aspidorhynchus has species that collectively show a worldwide distribution. Aspidorhynchus can be dated to the Middle Jurassic when there was a single continent. It is sister taxon to Vinctifer plus Belonostomus and the latter can be dated to the Upper Jurassic, where the first occurrence of Belonostomus species are known from Europe. Vinctifer species are known from the Southern Hemisphere with an occurrence in Mexico. Belonostomus is known from the Northern Hemisphere and also from Morocco, Lebanon, and Mexico. There is a partial phylogeny for Belonostomus in which a group of four species from Mexico, Morocco, and Lebanon is sister to a European–North American pairing.

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In essence, the phylogeny of these fishes tracks the fragmentation of the continents both geographically and temporally with two provisos. First, Belonostomus that is predominantly Northern Hemisphere has representatives in localities that at the time were attached to the north African coast. Second, Mexico has representatives of both northern (Belonostomus) and southern (Aspidorhynchus) clades. Although there is general concordance between phylogeny, geography, and time, the occurrence of one species (Belonostomus tenuirostris) in the late Cretaceous of North America and Chile (Brito and Suárez 2003) suggests a late dispersal along the western edge of the Americas.

Ellimichthyiforms

The ellimichthyiforms (sometimes called paraclupeids; Fig. 13.4) are an extinct sister group of modern herrings. There are about twenty-five species ranging in time from the early Cretaceous to the Middle Eocene. Unlike aspidorhynchids, they do not have Jurassic representatives. In the

FIGURE 13.4 Phylogeny of ellimichthyiforms after Forey (unpub. ms.). Some species have yet to be named. Geographic localities: Brz, Brazil; Chin, China; Eur, Europe; Leb, Lebanon; Mex, Mexico; Mor, Morocco; N. Am, North America; Sp, Spain; W. Afr, West Africa. Sister species belonging to the genus Diplomystus and occurring in the early Tertiary have been included, but their history is unlikely to involve Tethys.

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Lower Cretaceous, the representatives are mostly freshwater, and there are species in Spain, China, Brazil, Mexico, and West Africa. Several very different phylogenetic hypotheses are available for this group of fishes (Grande 1985; Chang and Maisey 2003; Forey 2004; Zaragüeta-Bagils 2004; Alvarado-Ortega et al. 2008); not all have been computer generated, and they include different complements of taxa and are therefore not easy to compare or summarize. That of Zaragüeta-Bagils (2004) is different from all others in that the group is resolved as paraphyletic, but this appears to be an extreme position and can (Forey, unpub. ms.) and indeed has (Alvarado-Ortega et al. 2008) been questioned. However, all agree that there is sister group pairing between species from Brazil and West Africa. The phylogenetic position of the early Cretaceous Spanish occurrence differs. In the phylogeny in Figure 13.4, it is sister species to Upper Cretaceous taxa occurring in Morocco, Lebanon, Europe, and Mexico. In the phylogeny of Alvarado-Ortega et al. (2008), it is sister to early Cretaceous taxa of China, South America, West Africa, Morocco, Lebanon, and Mexico. Clearly, more comprehensive phylogenetic work needs to be done. Excluding the Spanish occurrence then the Upper Cretaceous forms show strong sister group relationships between taxa from Mexico in the west to Lebanon and Israel in the east in an arch that stretches around the northern rim of Tethys. There are similarities with the aspidorhynchid pattern described earlier in that there is a clade that includes Northern Hemisphere representatives linked with taxa from Mexico, Morocco, and Lebanon. There is also a southern clade as sister group, but this includes a sister taxon in China. This is not easy to explain. This was either a much earlier vicariant event or one demanding a dispersal explanation.

Chanoids

Chanoids (Fig. 13.5) have about fifteen species including one modern representative that today inhabits shallow marine waters and estuaries in the Indo-Pacific. The most plesiomorphic member is late Jurassic age and is located in present-day Germany but at that time was much closer to southern continents. In the Cretaceous, there were clear sister group pairings between a West African–Brazilian clade and a Lebanon–Israel clade. This is similar to the early Cretaceous ellimichthyids. Spain, which appeared in the preceding example, is now unequivocally linked to the Southern Hemisphere clade (in the previous example, it depended on which of the alternative phylogenies was accepted).

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FIGURE 13.5 Phylogeny of Chanoids after Grande and Poyato-Ariza (1999). Geographic localities: Brz, Brazil; Eur, Europe; Isr, Israel; Leb, Lebanon; Sp, Spain; W. Afr, West Africa.

Summar y

Considering these three examples, some generalities that can be distilled. Figure 13.6 shows the superimposed phylogenies of the three monophyletic taxa discussed. Not all areas are represented in all phylogenies, but there are some concordant patterns. There is a clear spilt between Southern Hemisphere and Northern Hemisphere distributions that was in place by the Lower Cretaceous. However, the distributions do not completely follow the continents, in the sense that the northern distributions take an arc from Mexico in the west to Europe and then to Israel, Lebanon, and Morocco in the east. Mexico and Morocco are the joint ends of distributions that follow the northern and southern coasts of Cretaceous Tethys (Fig. 13.7). It should be noted that although Morocco is today clearly on a southern continent, it was closely tied with Lebanon and Israel in the Cretaceous. These localities were on highstands within Tethys, and their precise location is unknown. Although this chapter is concerned with teleosts, it may be noted that a very similar distributional pattern, for the same period of time, was deduced for the Vidalamiinae, a group of amiid fishes (Grande and Bemis 1998). I would suggest, therefore, that there is a causal relationship between Earth and phylogenetic history of these lower teleosts (Fig. 13.8). By the Upper Cretaceous, there is a clear split between North America and Europe—Lebanon. The Lower Cretaceous

FIGURE 13.6 Phylogenies of three monophyletic taxa plotted against time and superimposed on one another. Long dashed line, aspidorhynchiforms; solid line, ellimichthyiforms; short dashed line, chanoids. There is a degree of congruence, but Spain and Mexico show up as “hybrid” areas. Abbreviations as before.

FIGURE 13.7 Map of Tethys in Lower Cretaceous times showing the “tracks” of Northern and Southern Hemisphere taxa distilled from the three phylogenies. Map based on Philip et al. (1993).

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FIGURE 13.8 Biogeographic conclusions, showing the common geographic elements of the three phylogenies considered here. Lebanon, Morocco, and Israel localities are gathered within the “Northern” distributions. In Cretaceous times these localities were on highstands within the Tethys, and their precise location is unknown. Abbreviations as before.

split between South America and Africa has been extensively documented from both the geological and biotic points of view (Maisey 2000). Not all clades show such overlapping patterns. Ichthyodectiforms (Fig. 13.9) are an extinct clade of about thirty species that have some very large representatives (up to 8 meters), and some were almost certainly open water swimmers, unlike any of the fishes dealt with so far. The plesiomorphic members are widely distributed (Europe, Australia, Lebanon). There are, however, two closely similar species of Cladocyclus, one found in Brazil and the other in Africa, repeating many similar patterns, not only of fishes but also of turtles and dinosaurs. And there are also several sister group pairings of ichthyodectiforms between North America and Europe in the Upper Cretaceous. By and large, however, the basal phylogeny of these fishes is not harmonious with the phylogeny of the Earth. It may be that these fishes were extremely widely distributed, as are modern tuna and sailfish species, and that they had a more oceanic lifestyle. All except the most basal members are streamlined fishes with deep high-aspect ratio tails designed for fast, sustained open-water swimming. Cavin (2008) has also documented patterns in the Cretaceous fish world and has looked at a broader range of taxa. He attempted to distinguish between vicariance, dispersal, and radiations according to

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FIGURE 13.9 Phylogeny of ichthyodectiforms after Taverne and Chanet (2000). Geographic localities: Aus, Australia; Brz, Brazil; Eur, Europe; Leb, Lebanon; N. Am, North America; W. Afr, West Africa.

some rules he devised and derived from the phylogeny, time, and location. I have not adopted these here because of the distortion that may be caused by the vagaries of the fossil record, but we agree on several key conclusions. There were clear vicariant events during late Jurassic times between Northern and Southern Hemisphere continents, and these imposed a geographic pattern reaching from Mexico in the west, along the northern edge of Tethys to North Africa in the east. During Lower Cretaceous times, vicariant events separated taxa living in South America (Brazil) and West and North Africa and, maybe, Australia. During the Upper Cretaceous, there were clear vicariant events between North America and Europe.

RATE OF TAXIC EVOLUTION

Another use to which the results of cladistic analysis of lower teleosts may be put is the investigation of the rate of taxic evolution. If we measure standing diversity of marine teleost fishes throughout the Cretaceous, we notice a marked peak about 100 myr ago, about the middle of the Cretaceous (during the Cenomanian Stage). The problem we have is that this is coincident with a maximum number of fish localities as well as availability of potentially fossiliferous rock (Smith 2001) (Fig. 13.10). So it may be difficult to tell if the peak is due to a real

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FIGURE 13.10 Fossil fish record and rock record. Left: Relative numbers of localities yielding marine teleosts from the Triassic to the Pleistocene, plotted by stages. Stars indicate the number of localities at which more than thirty species are recognised. Right: Rock outcrop record from northwestern Europe compiled by Smith (2001). Note coincidence of maximum localities and rock record.

biological event or simply the sampling of the fossil record—a lagerstatten effect. As Smith notes, “The only realistic way to distinguish between sampling and biological patterns is to gather phylogenetic information. The key here is the recognition of ghost lineages” (Smith 2001: 363). The ghost lineage is the amount of stratigraphic range that must be inserted to comply with a particular phylogenetic tree (see Norell 2001 for definitions of different aspects of “ghost lineage”; here I group range extensions and ghost lineages into one). So, in Figure 13.11 we would have to insert ten units of time that are currently not represented by fossils. Taking time slices in turn, we can calculate the average amount of ghost lineage duration that must be assumed and measured across all equally ranked taxa occurring in that particular time slice (Fig. 13.12). The theoretical expectation is that if the rise in standing diversity is due to a sampling variation, then the average ghost lineage duration for successive time slices should track the diversity. However, if there is a real rise in diversity that is not a result of a better fossil record, then there will be a drop in the average ghost lineage duration because cladogenesis will speed up. The theory is illustrated in Figure 13.13, taken from Cavin and Forey (2007).

c

c

d

a Time slices

Sister group

d

a G b

b

a

b

c

d

G

G

FIGURE 13.11 Ghost lineage calculation. Given four taxa with stratigraphic distributions shown at top left and a phylogeny at bottom left, there are ten segments of time that must be inserted to account for the phylogeny. This is called the ghost lineage. Calculations of ghost lineage duration in situations where the phylogenies are not completely resolved are explained in Cavin and Forey (2007).

FIGURE 13.12 Calculation of average ghost lineage duration (from Cavin and Forey 2007).

a

Rate of diversification 3 12

Standing Cladogenetic Average ghost diversity events lineage duration 3 2 4 6 12 1 2 3 4 5

j i h g f e d c b 25 75 % of a preservation

b

Rate of diversification 3

12

2

4

6

3

12 1 2 3 4 5

Standing Cladogenetic Average ghost diversity events lineage duration 2

4

6

3

12 1 2 3 4 5

2

4

6

3

12 1 2 3 4 5

j i h g f e d c b 25 75 % of a preservation

FIGURE 13.13 Relationship between average ghost lineage duration and cladogenesis. In the top diagram, the “true” phylogeny is shown, with actual records (standing diversity) shown as black bars. Note that in time slice h, there is a real increase in cladogenesis. In this instance, we would expect a decrease in average ghost lineage duration. In time slice d, there is a rise in standing diversity but no increase in number of cladogenetic events. In other words, the observation is a reflection of sampling. In the lower diagram, the phylogeny is given only relative to those observed taxa. Note that, although there is a slight rise in cladogenetic events in both time slices d and h, the average ghost lineage duration drops in h, implying real increase in cladogenesis (after Cavin and Forey 2007).

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For the phylogenetic database, Cavin and Forey (2007) compiled a “supertree” of marine lower teleosts. This was constructed at genus level since, within a palaeontological framework, genera are usually recognized on unique characters and are demonstrably monophyletic (cf. species that are often differentiated on body proportions, scale counts, stratigraphic, and/or geographic criteria) (Forey et al. 2004). The details of the construction of the supertree can be accessed through Cavin et al. (2007). It is not a supertree in any of the accepted methods (Roshan et al. 2004) because published phylogenies of Cretaceous actinopterygian subgroups generally deal with taxonomically limited clades with little or no taxon overlap. Also, a data set embracing the morphological diversity of all lower teleosts would include a large number of questions marks covering “nonapplicable” character state descriptions. Instead, the tree was built using a backbone phylogenetic tree from Patterson and Rosen (1977) on to which were grafted the phylogenies of the many clades. Sixteen approximately equal time segments (each corresponding to 3 myr) between the Aptian to Maastrichtian were chosen, and the average ghost lineage durations were calculated for each and plotted (Fig. 13.14). It can be seen that the average ghost lineage duration dropped markedly, coincident with the rise in cladogenetic events as predicted from the phylogeny. From this Cavin and Forey (2007) concluded that there was a real rise in the rate of teleost cladogenesis in the mid-Cretaceous. Several reasons could account for this (Cavin et al. 2007), but the rise of taxic diversity seen here is most closely correlated with inferred sea surface temperatures (Fig. 13.14). This has its modern analogue in species richness and latitudinal gradients where temperature and diversity are correlated for fishes (Rhode 1992) and other groups. We must also be aware that the mid-Cretaceous was a time of maximum sea-level height, increasing the potential for much greater areas of near shore marine niches to become differentiated. Ultimately, both temperature and sea-level rise may be due to an increase in oceanic crust production and/or oceanic volcanism, having started in the Aptian (see Gale 2000 for an overview).

RATE OF MORPHOLOGICAL EVOLUTION

A third area to which information from a cladogram may contribute is the exploration of the rate of morphological evolution. This time character change information measured by optimizing characters on to the phylogenetic tree is used directly.

FIGURE 13.14 Top: Graph showing changes in standing diversity, number of cladogenetic events, and average ghost lineage duration across sixteen approximately equal time slices through the Cretaceous. Note the increase in standing diversity is broadly coincident with the fall in average ghost lineage duration and the increase in the number of cladogenetic events. The latter two parameters are artificially smeared backward by about one time slice because of the assumption that causative events precede the observed standing diversity. Bottom: Graph showing standing diversity superimposed with changes in sea surface temperature (after Cavin et al. 2007).

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FIGURE 13.15 Measurement of disparity through time used here. Phylogeny of six taxa (black boxes) with character changes on branches indicated (gray boxes). Pairwise comparisons are made and averaged against the numbers of taxa occurring in each time slice. In this case, taxa in time slice 2 are considered more disparate than those in time slice 1; therefore, the rate of morphological evolution has increased.

In the previous section, I suggested that there was an increase in the taxic diversity in the mid-Cretaceous. So we may ask, Does morphological evolution follow the same course? Just because cladogenesis increases this does not mean there is concomitant increase in morphological diversity. In this exercise, we can measure morphological divergence—some would call it disparity—across time during the evolution of these lower teleosts fishes through the Cretaceous. There are several ways to measure disparity and, indeed several meanings of disparity. Most of these have been succinctly outlined in Wills (2002). The measure I use here is phylogeny dependent and measures the average number of character changes that had separated members of a lineage at any one time. I do emphasize that there are other measures; but the reason I chose to use this one is the fact that it is constrained by some estimate of evolutionary history. The method, shown in Figure 13.15, measures disparity between taxa in successive time slices. Figure 13.15 illustrates a phylogeny of six taxa (black boxes) with character changes on branches indicated (gray boxes). Pairwise comparisons are made and averaged against the numbers of taxa occurring in each time slice. In this case, taxa in time slice 2 are considered more disparate than those in time slice 1, and the rate of morphological evolution therefore has increased. For teleost fishes, there are very few cases where the same terminal taxon used is represented in more than one time slice and therefore little duplication of character assessment (for some invertebrate taxa

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with long stratigraphic ranges, this may not be true). Comparisons of disparity across four broad time slices, each of approximately 30 million years ranging from Upper Jurassic to Lower Tertiary, was measured (Tithonian–Barremian, Aptian–Cenomanian, Turonian–Maastrichtian, Palaeocene–Eocene). It would clearly be better to use finer divisions of time, but, in general, the teleost record is not capable of being sufficiently densely sampled. There are some instances where finer divisions are possible and indeed preferable since the geological range of the particular lineage is much shorter. For the purposes of this chapter, I have kept to these broad time divisions. Figure 13.16 shows the results of comparing disparity through time for five monophyletic clades. These are groups for which data matrices include details of autapomorphies as these are part of the measurements of disparity. More clades could be added in the future. The Amiidae is not a teleost group, but the phylogeny and matrix offered by Grande and Bemis (1998) provide a good framework for such studies. Not all time slices have results, implying either that monophyletic groups are unrepresented or that there is only one taxon (comparisons are therefore unavailable). For four of the groups, the maximum disparity occurs in the mid-Cretaceous; and for ellimichthyiforms, chanoids, and ichthyodectiforms, this is coincident with maximum taxic diversity. This is a result that we might expect. For the amiids, there is a slight increase in disparity in the mid-Cretaceous even though there is one less taxon compared to the previous time slice. For osteoglossomorphs, the Cretaceous record is very poor, even though the lineage extends back to the Upper Jurassic. Here the maximum disparity occurs in the early Tertiary where there is maximum taxic diversity. If the osteoglossomorph record were extended to the Recent world, then it would be probable that the value for the mean pairwise comparison would increase substantially. If mean pairwise comparisons are averaged over the number of taxa, then for three of the five groups this value will follow the numbers of taxa. However, for the osteoglossomorphs and ichthyodectiforms, this is not the case. For the osteoglossomorphs, the late Cretaceous showed the greatest amount of disparity per taxon, implying that the greatest amount of morphological evolution was happening then. For ichthyodectiforms, the greatest amount of change occurred early in the history of the group such that earlier taxa were more diverse than later members. This is a rate trajectory that has been mentioned several times before for other groups of fishes (Westoll 1949; Schaeffer 1952) as well as other groups of organisms (Wills 1998).

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FIGURE 13.16 Rates of morphological evolution. The top graph shows mean pairwise comparison of character changes over four time slices throughout the Cretaceous and the early Tertiary within five clades. The x-axis denotes time slices. Phylogenies used are amiids (Grande and Bemis 1998); Osteoglossomorphs (Li and Wilson 1996); ellimichthyiforms (Alvarado-Ortega et al. 2008); chanoids (Grande and Poyato-Ariza 1999): ichthyodectiforms (Cavin and Forey, unpub. ms.). The bottom graph shows same data averaged against the number of taxa within each time slice.

CONCLUSION

The use of phylogenetic trees to answer more general questions of the tempo and mode of evolution has a long and varied history. The rise of cladistics gave great impetus to that inquiry (Smith 1994) and allowed quantification to largely anecdotal accounts (see Briggs and Crowther 2001 for summaries of many aspects). More precise measures of the

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quality of the fossil record (Norell and Novacek 1992; Benton et al. 2000) gave credence to some accounts and questioned others. This chapter has concentrated on a small part of that inquiry; and, in using just one group, it is necessarily restrictive. However, the conclusions that the fragmentation of Pangaea has influenced both the distributions and rates of taxic and morphological evolution can be tested by similar enquiries of different organisms. The key is the time element (Upchurch 2007) for the investigation of unique historical events.

Acknowledgments

I would like to thank David Williams and Sandy Knapp for inviting me to contribute to this volume dedicated to Chris Humphries, whom I regarded as a lifelong friend and with whom I shared too many beers and not enough time. In the seventies and eighties, we spent many hours with colleagues Colin Patterson, Dick Vane-Wright, and Brian Gardiner, cornering people, pointing out the error of their evolutionary systematic ways, and persuading them to come into the enlightened world of cladistics. I well remember Chris as being one of the most efficient enlighteners, not least because he was prepared to invest his time in supervising so many students as well as take such an active role in the early days of the Willi Hennig Society. Although dedicated to cladistic theory, and somewhat intolerant of views that deviated from the true path, Chris always regarded the practical application of cladistics through biogeography as both the strength and justification for Willi Hennig’s legacy. It was Chris who enlivened my interest in such matters.

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FOURTEEN

P a u l i n e Y. L a d i g e s , M i c h a e l J . B a y l y, and Gareth J. Nelson

E A S T – W E S T C O N T I N E N TA L V I C A R I A N C E I N E U C A LY P T U S S U B G E N U S E U C A LY P T U S

The eucalypt group (Myrtaceae) totals seven genera, including small rain forest genera, and species-rich sclerophyll genera that dominate Australian vegetation (Ladiges et al. 2003). Living taxa occur throughout Australia but extend to New Caledonia, New Guinea, and Malesia (to the southern Philippines; Williams and Brooker 1997). Macrofossils of eucalypts extend this range to South America (Early Eocene; Gandolfo et al. 2007) and New Zealand (Early Miocene; Pole 1989, 1993). The largest of the seven genera in the eucalypt group is Eucalyptus L’Hér. with about six hundred species, although Brooker (2000) includes additional species having lumped two of the other genera, Angophora Cav. and Corymbia, Hill and Johnson into Eucalyptus. Brooker’s generic revision has not been followed in Australian herbaria, although his infrageneric groupings are generally accepted. Within Eucalyptus, Pryor and Johnson (1971) recognized a major clade that they informally referred to as subgenus Monocalyptus (i.e., outside the formal Code), equivalent to Brooker’s subgenus Eucalyptus. Related, small subgenera were recognized also by Pryor and Johnson, including Idiogenes (E. cloeziana) and Gaubaea (E. curtisii and E. tenuipes). Eucalyptus curtisii was treated formally by Brooker as subgenus Acerosae, with E. tenuipes as subgenus Cuboidea.

Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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In addition, Brooker erected a further monotypic subgenus Primitiva for E. rubiginosa “alluding to the developmentally primitive nature of the species compared to the advanced sister subgenus Eucalyptus” (Brooker 2000: 124). Subgenus Eucalyptus (the “monocalypts”), with 111 species (Brooker 2000; Table 14.1), is well supported as a monophyletic group, with flowers characterized by a single petaline operculum (Drinnan and Ladiges 1989), lack of free sepals, and anatropous ovules arranged in two rows per loculus (with a few species exceptions). Subgenera Acerosae, Cuboidea, Idiogenes, and Primitiva also have anatropous ovules but vary among themselves in regard to other floral and seed characters. Both morphological and molecular phylogenetic analyses to date suggest that Acerosae (E. curtisii) is an early-diverging lineage, possibly sister taxon to the whole genus Eucalyptus (Ladiges et al. 1995; Steane et al. 1999, 2002; Udovicic and Ladiges 2000); Cuboidea is the sister taxon to Idiogenes plus subgenus Eucalyptus; Idiogenes (E. cloeziana) is the sister taxon to subgenus Eucalyptus; but Primitiva appears to be nested within the latter (Steane et al. 2002) despite having four rows of ovules. The monocalypts have long been of interest to biogeographers and ecologists. Subgenus Eucalyptus is distributed in both western and eastern Australia (Fig. 14.1), and it is most common in southern coastal and upland regions (Gill et al. 1985). Only one species, E. diversifolia (Fig. 14.2), occurs in both the southwest and southeast, being tolerant of coastal calcareous soils. The clade is absent from far northern Australia and the arid (Eremean) zone. In eastern Australia, species range from the wet tropics (lat. 16° S) to the cool temperate forests of southern Tasmania (44° S), including the mountain ash forests dominated by E. regnans (Fig. 14.2), the tallest hardwood tree in the world, and subalpine snow gums (E. coccifera and E. pauciflora). In Western Australia, species occur in the South Western Botanical Province (e.g., the jarrah forests, E. marginata, lat. 32°–35° S) and adjacent drier interzone region, but only as far north as near Mount Lesueur (E. todtiana, 30° S; Ladiges et al. 1987). The four related monotypic subgenera all occur in eastern Australia: Acerosae (E. curtisii), Cuboidea (E. tenuipes), and Primitiva (E. rubiginosa) have a restricted distribution in southeastern Queensland; Idiogenes (E. cloeziana) occurs with these taxa but is morphologically variable and has a wider, disjunct distribution in eastern Queensland (Boland et al. 1984). In terms of ecological traits, various authors have commented on the distribution of the eucalypt subgenera (e.g., Noble 1989; Wardell-Johnson

TABLE 14.1. classification of subgenus EUCALYPTUS Sections (11), Series (20), Number of Species (111), and Related Monotypic Subgenera (4)

Subgenus Acerosae E Cuboidea E (outgroup) Idiogenes E Primitiva E Eucalyptus E&W

Section

Series

Examples and Total Number of Species E. curtisii (1) E. tenuipes (1)

1. Amentum Mahoganies E 2. Pseudophloius E 3. Aromatica E Peppermints

Radiatae (mainland) Insulanae (Tasmania)

4. Capillulus E Stringybarks

Pachyphloius

Limitares 5. Nebulosa E 6. Eucalyptus E Green ashes

Regnantes Eucalyptus Strictae

Contiguae 7. Longitudinales E 8. Cineraceae E Blue ashes, snow gums, scribbly gums

Fraxinales

Pauciflorae Psathyroxylon

Stenostomae Piperitales Sphaeocarpae

E. cloeziana (1) E. rubiginosa (1) E. umbra, E. latisinensis (6) E. pilularis (2) E. croajingolensis, E. dives, E. radiata (5) E. coccifera, E. nitida, E. pulchella (6) E. baxteri, E. globoidea, E. muelleriana, E. serraensis, E. verrucata (28) E. deuaenesis (1) E. olseniia (1) E. regnans, E. fastigata (2) E. obliqua (1) E. paliformis, E. spectatrix, E. stricta, E. triflora (9) E. kybeanensisa (1) E. mitchelliana, E. moorei (3) E. fraxinoides, E. delegatensis (4) E. pauciflora, E. lacrimans (3) E. sieberi, E. remota, E. haemastoma, E. rossii (9) E. stenostoma (1) E. piperitaa (1) E. sphaerocarpa (1) (Continued)

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TABLE 14.1. ( CONTINUED ) Subgenus

Section 9. Insolitae E 10. Pedaria W 11. Longistylus W Subsect. Arboreae Trees, tingle, jarrah

Series

Examples and Total Number of Species

Jacksoniae

E. planchoniana (1) E. brevistylis (1) E. jacksonii (1)

Occidentales Subsect. Fruitices Mallees

Patentes Diversiformae

Angulares Muricatae Calcicolae Preissianae Proximae Subereae Subsect. Unicae

E. marginata, E. staeri (2) E. patens (1) E. buprestium, E. diversifolia, E. pachyloma, E. platydisca, E. todtiana (9) E. angularisa (1) E. exilis, E. sepulcralis (3) E. calcicola, E. ligulata (2) E. aquilina, E. megacarpa, E. preissiana (4) E. acies (1) E. suberea (1) E. insularis (1)

note: From Brooker (2000); Nicolle and Brooker (2006). Exemplar species listed include those in the molecular ITS analysis. E, eastern Australia; W, western Australia. aMonotypic series not sequenced.

et al. 1997). Florence (1981), for example, suggested that the monocalypts tend to occur on more acidic, low-nutrient soils and in areas of better water availability than the large subgenus Symphyomyrtus. Majer et al. (1992) reported that monocalypts also support a less diverse herbivore fauna than symphyomyrts. Early cladistic analyses of groups within subgenus Eucalyptus, including the so-called peppermints, stringybarks, green ashes, blue ashes, and Western Australian taxa (Ladiges et al. 1983, 1987, 1989, 1992; Ladiges and Humphries 1986), were based on adult and seedling morphology. Molecular analyses of Eucalyptus have to date only included a small fraction of these taxa, with the largest data set based on sequences of the nuclear ribosomal internal spacer region, ITS (Steane et al. 1999,

FIGURE 14.1 Current distribution of the monocalypts, Eucalyptus subgenus Eucalyptus; twenty-six species occur in southwestern Western Australia and eighty-five in eastern Australia; one species, E. diversifolia, extends from west to east on the coastal fringe, on calacerous soils over limestone.

FIGURE 14.2 Examples of monocalypts. A, Eucalyptus diversifolia (soap mallee), a multistemmed mallee species, on calcareous outcrops, southern Australia; B, tall open forest of E. regnans (mountain ash), near Toolangi, Victoria.

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2002). A comprehensive phylogenetic analysis of the monocalypt group has the potential to contribute not only to improved classification and taxonomy, but to an understanding of the evolutionary history of Australian continental bioregions and ecology of the flora, particularly the history of the southwestern sclerophyll biome, which is a recognized region of high endemism and biodiversity (Hopper and Gioia 2004), and its disjunction from eastern Australia. We present here a synthesis of previously published morphological data, an expanded ITS data set and a new data set based on the nuclear ribosomal external transcribed spacer region, ETS. For ITS, we have identified pseudogenes (Bayly and Ladiges 2007; Bayly et al. 2007), enabling us to avoid nonhomologous comparisons. A comprehensive phylogenetic tree for subgenus Eucalyptus is presented for the first time, allowing assessment of the biogeographic history and age of a plant group that shows strong east–west disjunction across the Australian continent.

METHODS Plant Material

DNA was obtained from new collections or from genomic extracts used in the earlier studies of Udovicic and Ladiges (2000), Parra-O. et al. (2006), Bayly and Ladiges (2007), Bayly et al. (2008), and Gibbs et al. (2009). For new collections, fresh leaf material was sampled from the field and from living collections and dried using silica gel. Additional ITS and ETS sequences came from GenBank, based on both our own studies and those of Steane et al. (1999, 2002). Taxa included are shown in Table 14.1, and details of voucher specimens are given in Appendix 14.2 at the end of this chapter.

Isolation, Amplification, Sequencing, and Alignment of Nuclear DNA

Isolation, amplification, and sequencing of DNA followed the protocols of Parra-O. et al. (2006) for ETS and Bayly and Ladiges (2007) for ITS (using the primers ITS4 and ITS5 of White et al. 1999). Contiguous sequences were assembled using Sequencher v. 3.0 (Gene Codes Corporation, USA), aligned using ClustalX v. 1.82 (Chenna et al. 2003), and the alignment then manually edited using Se-Al Sequence Alignment Editor

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v. 2.0a11 (Rambaut 1996). Individual sequences are available from GenBank (accession numbers in Appendix 14.2), and the aligned data sets are lodged in TreeBASE. The ITS data set included sequences for fifty-nine ingroup and six outgroup accessions (twenty-nine new in this study); the ETS data set included forty-one ingroup and six outgroup accessions (thirty-nine new in this study).

Morphological Characters

Thirteen morphological characters that could be scored across all taxa are listed in Table 14.2 and are based on those of Ladiges and Humphries (1986), Ladiges et al. (1983, 1987, 1989, 1992), Chippendale (1988), Brooker (2000), and EUCLID (2006). Seed type (character 2) and leaf arrangement in seedlings (character 8) were two multistate characters, treated as unordered. Plesiomorphic states were determined by comparison with the outgroup: E. cloeziana, E. tenuipes, and E. curtisii.

Phylogenetic Analyses

All data sets were analyzed in PAUP* 4.0 beta 10 (Swofford 2002) using maximum parsimony. Starting trees were obtained by a stepwise addition sequence using the CLOSEST option (retaining one tree at each step) and then subjected to TBR branch swapping, with the MULPARS option on. The ITS and ETS data sets were analyzed separately and in combination for taxa that had both regions successfully sequenced. Analyses of ITS and ETS data sets produced many equally parsimonious trees, so the following search strategy was used. The initial tree search was stopped at thirty thousand trees, and a strict consensus was calculated. A second analysis searched only for trees that were not consistent with this strict consensus and used one thousand random addition sequences, each followed by TBR branch swapping, aborting each replicate when five thousand trees (of a length exceeding those of the first analysis) were obtained; the purpose of this was to ascertain whether the strict consensus was likely to adequately represent the full set of equally most parsimonious trees, even though these could not all be retained. Bootstrap analysis was carried out using the heuristic search option and one thousand replicates with a MAXTREES of five thousand for each replicate. Bootstrap supported nodes can be treated as informative characters to allow a combination with different datasets (e.g., Sanderson et al. 1998).

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TABLE 14.2. Number 1 2

3 4 5 6 7 8

9 10 11 12 13

morphological characters Character

Anthers: oblong opening by vertical slits (0); reniform opening by confluent slits (1), e.g., E. marginata group, and eastern species Seed: red brown-brown, small, no wing (0); red brown-brown, small with margin winged (1); gray-black, large, no wing (2); black or black-brown, large, no wing (3); black to dark brown, large, and with lateral wing (4); black, small, no wing (5) Seedlings: without (0) or with (1) radiating hairs on emergent oil glands, e.g., stringybarks Fruit: without (0) or with (1) distinct lobes over valves, e.g., E. megacarpa Adult leaves: discolorous and with drip tip, e.g., E. jacksonii (0); concolorous without drip tip (1) Flower buds: not in stellate clusters (0); in stellate clusters (1), e.g., E. mitchelliana, E. moorei Adult leaf venation: moderate to densely reticulate with side veins at a broad angle (0); sparse reticulation and acute veins (1), e.g., eastern species Juvenile leaf arrangement: opposite up to about ten pairs then alternate (0), e.g., E. patens, stringybarks; opposite to five to six nodes, then alternate, petiolate, and bluish (1), e.g., blue ashes; petiolate at early nodes (2), e.g., E. marginata; opposite, sessile for many nodes (3), e.g., E. pilularis, peppermints; opposite for a very few pairs, becoming petiolate, pendulous, green (4), e.g., E. obliqua, green ashes Inflorescence: axillary (0); terminal (1), e.g., E. rubiginosa and mahoganies Adult leaf venation: not parallel (0); parallel (1), e.g., E. mitchelliana, snow gums Flower buds and fruits: not ridged (0); ridged (1), e.g., E. ligulata, E. calcicola Rough bark: stringy (0); corky (tessellated, 1), e.g., E. patens, E. suberea Flower bud clusters: upright (0); pendulous (1), e.g., E. acies, E. insularis

note: Eucalyptus subgenus Eucalyptus is monophyletic based on anatropous ovules arranged in vertical rows of two, and a single operculum.

In the strict consensus tree from the combined ITS + ETS analysis were eleven nodes coded as binary characters. One exception was the node grouping E. muelleriana, E. regnans, and E. pilularis, which had only 52 percent support and was not coded as a character. These species are not related based on any previous analyses or classifications (e.g., Brooker 2000). An additional node (showing E. megacarpa and E. aquilina as

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sister taxa) that had stronger support of 74 percent in the bootstrap analysis of the combined data set, but that was not recovered in the strict consensus tree, was included as an eleventh character. Two nodes in the ITS only analysis and one in the ETS only analysis were scored as three more characters. These data were added to the morphological data set of thirteen characters, resulting in a matrix of forty-four ingroup taxa and twenty-seven characters. An all zero outgroup was included to root trees. As well as analyzing the data in binary form, characters were coded as three-items using the program TAX (Nelson and Ladiges 1999) followed by parsimony analysis using PAUP (heuristic search, starting trees obtained by a CLOSEST addition sequence, TBR branch swapping, MULPAR option on).

RESULTS Nuclear rDNA

The ITS data set included 640 aligned nucleotides, together with 3 binary indel characters, giving a total of 101 variable characters including 47 parsimony informative characters (PICs). The ETS data set included 467 aligned nucleotides, including 51 variable characters and 28 PICs. The combined ITS and ETS data set, based on a subset of taxa, included 143 variable characters and 72 PICs (ITS 44; ETS 28). No pseudogenes were detected in the rDNA data sets using the criteria outlined by Bayly and Ladiges (2007). As such, all sequences in these data sets are assumed to represent functional orthologues that can be reasonably combined for the purpose of phylogenetic analyses.

Phylogenetic Analyses

The ITS analysis was stopped at thirty thousand trees and a strict consensus tree calculated; further searches found no trees of the same or shorter length with topologies conflicting with this consensus. Each most parsimonious tree had a length of 154, CI = 0.74, RI = 0.87. The strict consensus tree (Fig. 14.3) has seventeen resolved nodes, twelve with bootstrap support (bs) >50 percent. One of the outgroups, E. cloeziana, clusters with two ingroup species, at the base of the tree, but has a long branch length as illustrated for one of the most parsimonious trees shown in Figure 14.4. Early lineages are among the Western Australian

FIGURE 14.3 Strict consensus tree based on the ITS data set. Selected nodes are numbered, and bootstrap support values are given below branches.

FIGURE 14.4 One of the equally most parsimonious trees based on the ITS data set, showing branch lengths (values given for all branch lengths >1). E. cloeziana, an outgroup taxon considered the likely sister to subg. Eucalyptus on morphological grounds, groups here with “basal” ingroup taxa but sits on a very long branch (the longest on the tree).

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species, including sister taxa E. patens and E. todtiana; E. suberea; E. megacarpa, and E. aquilina; and a clade of wet forest species, E. brevistylis, E. jacksonii (sequence identical to E. staeri), and E. marginata. The position of E. todtiana was not expected based on the classification of Brooker (2000) and earlier analyses (Ladiges et al. 1987), but three accessions show consistency in the results based on ITS. The remaining Western Australian species group with the eastern species at node 3 (low bs of 59 percent; Fig. 14.3), and the eastern species are monophyletic at node C but lacking bootstrap support. Node D shows all other eastern species as a clade with the Queensland species E. planchoniana (node C) as its sister. The ETS analysis, with a reduced number of sequences, was stopped at thirty thousand trees and a strict consensus tree calculated; further searches found no trees of the same or shorter length with topologies conflicting with this consensus. Each most parsimonious tree had a length of sixty-nine steps, CI= 0.80 and RI = 0.90. Nine nodes were resolved in the strict consensus tree (not shown), only three with support (each >70 percent bs support). The results are consistent with the ITS strict consensus tree, showing all but one eastern species as a monophyletic group (node with 68 percent bs support) nested within a clade of Western Australian species together with the Queensland E. planchoniana and outgroup E. cloeziana (subgenus Idiogenes). The branch leading to the latter was relatively long. The analysis based on the combined ITS + ETS data set was stopped at thirty thousand trees and a strict consensus tree calculated (Fig. 14.5); further searches found no trees of the same or shorter length with topologies conflicting with this consensus. Each most parsimonious tree had a length of 220 steps, CI = 0.73 and RI = 0.84. Fifteen nodes were resolved, fourteen with >50 percent bs support. Three nodes show relationships among four of the outgroup species, E. tenuipes (subgenus Cuboidea) and three eudesmid species (subgenus Eudesmia), which are in a polytomy with outgroup E. curtisii (subgenus Acerosae). Outgroup E. cloeziana is at the basal node 1 (96 percent bs) with ingroup taxa. At node 1 are sister species E. marginata and E. brevistylis, E. suberea, sister taxa E. patens and E. todtiana, and sister taxa E. megacarpa and E. aquilina. Node 5 (66 percent bootstrap support) groups the remaining western species with the eastern clade (node 7, 80 percent bs). Within the eastern clade, E. rubiginosa (classified as subgenus Primitiva by Brooker 2000) is related to E. sphaerocarpa and the mahogany E. umbra, which are the sister groups to the other eastern species at node 10 (65 percent bs).

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FIGURE 14.5 Strict consensus tree from the ITS and ETS combined data set. Bootstrap support values are given below branches.

Parsimony analysis of the combined data set (Appendix 14.1) based on morphology and the nodes from the combined nrDNA tree (Fig. 14.4) was run to completion, finding 28,750 trees, each of length 46, CI = 0.74, RI = 0.93. The 50 percent majority rule consensus tree is shown in Figure 14.6, with nodes not resolved in the strict consensus tree indicated. Three item analysis (after deleting taxa with the same string of character scores) resulted in 2,268 most parsimonious trees, each of

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FIGURE 14.6 A 50 percent majority rule consensus tree based on coding nodes from the ITS + ETS strict consensus tree as characters together with the morphological character data set (see Appendix 14.1). Nodes are numbered, and bootstrap support values are given below branches. Dashed lines indicate branches not present on the strict consensus.

length 18,286, CI = 0.93, RI = 0.92. The tree topology (not shown) was very similar to the standard parsimony analysis, with one polytomous node resolved and one taxon moving position (as detailed later). The clade of the wet forest species E. marginata (jarrah) + E. brevistylis (which also would include E. staeri and E. jacksonii) is the first lineage and sister to the other taxa. Apart from the DNA support for

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their relationship, all taxa have discolorous leaves with a drip tip and reniform anthers, a contentious character but clearly a parallelism with the eastern taxa. Node 2 is a polytomy, including the lineage of E. suberea, E. patens and E. todtiana (nodes 4 and 5, which would also include E. lateritica and E. johnsoniana not sampled here for DNA analysis). Eucalyptus megacarpa and E. aquilina are also at node 2 and together with E. coronata are a clade (node 6), with distinctive, similar buds and fruits grouped in units of threes and a mallee growth habit. Node 7 shows E. platydisca and E. diversifolia (the latter the only western species to occur on the margin of the Nullarbor and the east of Southern Australia) as related to the remaining taxa. At node 8, E. preissiana is sister taxon to a polytomous node (9), including the following: E. ligulata and E. calcicola as sister taxa with similar ribbed fruits (node 10); sister taxa E. insularis and E. acies with flower buds in pendulous clusters (node 11); E. buprestium and E. pachyloma with large winged seeds (node 12); and E. sepulcralis (including E. exilis and E. pendens unsampled), which has a weeping habit. In the three-item analysis, E. preissiana is grouped with the E. megacarpa clade (node 6), and the polytomy at node 9 was resolved, with the Western Australian mallee species monophyletic. The eastern monocalypts are a monophyletic group at node 13, with the Queensland species E. planchoniana sister to all the other sampled taxa. Also at the next node (14), the Queensland species E. rubiginosa (subgenus Primitiva), E. sphaerocarpa, and E. umbra (representing the mahoganies, node 15) form a clade sister to the remainder of the eastern taxa at node 16. A number of eastern lineages at node 16 represent recognized taxonomic groups; peppermints (node 17); green ashes (node 18); blue ashes (node 19), including subgroups such as the black-seeded species (node 21), snow gums together with the “stellulata” group (nodes 22–23); and stringybarks (node 20). The position of E. pilularis is equivocal (node 16) but may be related to the peppermints based on juvenile leaves remaining opposite for many nodes. The positions of the representatives of the scribbly gums (E. haemastoma and E. rossii) also are equivocal within the blue ash group (node 19).

DISCUSSION

The summary phylogeny (Fig. 14.6) confirmed clades of previous studies but also reinterpreted other relationships. The combined molecular data (Fig. 14.5) confirmed subgenus Idiogenes (E. cloeziana) as closest to the

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monocalypts among the outgroup taxa included. Eucalyptus cloeziana is classified as a subgenus separate from subgenus Eucalyptus (monocalypts) based on having small, free sepals and four rows of ovules, but that are anatropous similar to the monocalypts. Classification of other infrageneric taxa in Chippendale (1988) and Brooker (2000) requires formal revision (to be published elsewhere). In particular, subgenus Primitiva (E. rubiginosa) requires sinking into subgenus Eucalyptus and grouping with eastern mahoganies. The Western Australian species are not a monophyletic group, and hence Brooker’s section Longistylus requires revision (see Table 14.1). At lower taxonomic rank, some changes also are required, including the removal of E. todtiana from subsection Fruitices and into a taxon that includes the species that are related to E. patens. The summary phylogeny also contributes to the discovery of the biogeographic history of subgenus Eucalyptus. The present-day distribution spans a wide latitudinal range from 16° S to 44° S, from wet tropical to cool temperate and subalpine environments, but does not extend into arid, desert regions. How has this distribution and evolution of clades been influenced by past environments and over what time scale?

Age and Palaeo-distribution of the Eucalypts

There is evidence that Eucalyptus dates back at least to the early Palaeogene, and it can be argued that the eucalypt group has its roots into the Late Cretaceous (Ladiges et al. 2003). This supposition is supported by molecular dating for Myrtaceae lineages (Sytsma et al. 2004) and the eucalypt group (Crisp et al. 2004). According to Martin (1994), eucalypt-like fossil pollen, known as Myrtaceidites eucalyptoides, has been recorded from the Lake Eyre Basin, central Australia, as early as Late Paleocene (60–55 Ma), and a rarer fossil, Myrtaceidites tenuis, is of Eocene age (Hill et al. 1999). With regard to macrofossils of Eucalyptus, extra-Australian records from South America that are of Early Eocene age (52 Ma; Gandolfo et al. 2007) and others from Early Miocene deposits in South Island New Zealand (Pole 1989) suggest that the eucalypt lineage was present in Gondwanan fragments. For Australia, early reports of Paleogene fossil eucalypt-like fruits are from an inland locality near Woomera (Lange 1978) but are now considered to be of Neogene age. Greenwood (1991, cited in Hill et al. 1999) reported, but did not describe, Eucalyptus macrofossils from mid-Eocene silcretes in the Eyre Formation, and Rozefelds (1996) illustrated eucalypt-like fruits from Paleocene

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or Eocene Redbanks Plains flora, Queensland. Two types of leaf impressions from the mid-Miocene Chalk Mountain Formation, Warrumbungle Mountains, New South Wales, are evidence of the coexistence at that time of the Angophora/Corymbia and Eucalyptus lineages (Holmes et al. 1982). Preserved flower buds with exposed anatropous ovules in two rows, from Late Miocene deposits at Bacchus Marsh in Victoria, are undoubtedly subgenus Monocalyptus and resemble the stringybark group (J. Blazey, illustrated in Ladiges 1997). Hill et al. (1999) noted the absence of eucalypt macrofossils from nearcoastal sites in southeastern Australian Paleocene to Oligocene floras, and they referred to the hypothesis of Lange (1980) that in the middle Cenozoic, the continental margins of Australia supported mesic, noneucalypt vegetation, and that eucalypts were farther inland in more xeric environments, becoming displaced to the continental margin with increased aridity. Alternatively, the eucalypts were more widespread in the Palaeogene but not prominent, and possibly not likely to appear in the fossil record.

Australian Past Environments

Australian past environments from the Late Cretaceous have been influenced by geological evolution of the continent resulting from separation from Antarctica in Gondwana, global and regional climate change, weathering of landforms, and marine incursions. Rapid seafloor spreading beginning about 83 Ma opened a narrow seaway south of Australia, with the final separation of Tasmania from Antarctica about 35 Ma. During rifting there was associated uplift of the southern margin of Australia related to the southeastern highlands, providing habitat for plants at significant elevation in that region of the continent from the early Cenozoic (Frakes 1999). As Australia moved to lower latitudes, climate became warmer and more humid, but there were also periods of progressive cooling and drying experienced worldwide. From the Paleocene to the Late Eocene, the climate was very humid and warmer than today, even at middle to high latitudes. Based on evidence of palaeosols, in Western Australia, near Perth, deep weathering and laterite is associated with the high rainfall of the Early and Late Eocene (Frakes 1999). At the end of the Eocene and into the Oligocene (c. 35 Ma), marked cooling was experienced (MacPhail et al. 1994), but southeastern Australia continued to have high humidity due to topography (Frakes 1999). Irregular warming was experienced from the Oligocene to the

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mid-Miocene, with drying cycles initiated in the mid-Oligocene and additional lateritization in regions during the mid- and Late Miocene. Silcretes and calcretes provide evidence of increased dryness in the interior of Australia during the Neogene, with widespread drying from the Late Miocene to the Pliocene. A succession of high sea levels resulted in extensive flooding into basins in the southwest and south of Australia during the Eocene. Carbonate sedimentation under warm conditions spread irregularly during the Middle to Late Eocene onto southern marginal basins, including the Bremer, Eucla, and St. Vincent basins, and marine deposits occur as far inland as Norseman (Frakes 1999). There was a major fall in sea level in the middle of the Oligocene due to Antarctic ice formation. Later, in the Early Miocene, extensive marine transgression occurred once again and flooded the Eucla Basin, depositing the Nullarbor limestones. The Nullarbor, which was uplifted about 14 Ma, is a karst plain dominated today by chenopod shrubland, with mallee eucalypts found along the coastal fringe and inland on the margins of the Great Victoria Desert (Fox 1999).

Monocalypt Clades in Southwestern Western Australia

Hill et al. (1999) note that the palynological record from southwestern Australia shows increased provincialism from the Eocene, and a flora different from that of the east—“features that hint at the present strong endemism in the flora [SW] having a long history” (p. 293). The warm wet Eocene was a period of major development of rain forests, with angiosperm dominance (Hill et al. 1999), but may have been the period also of early monocalypts. At a site near Zanthus, Western Australia, macrofossils (although not well dated) show a great diversity of sclerophyllous Proteaceae and Myrtaceae that possibly evolved in response to low soil nutrients under warm, wet conditions (Hill et al. 1999). Much of the southwest is dominated today by a deeply weathered plateau, dissected by rivers on its western and southern margins. Rarely higher than 500 meters in altitude, areas of high relief are confined to small granitic and quartzite ranges and parts of the plateau along these margins (Hopper 1979). According to our phylogenetic analyses, the earliest lineages of the monocalypts to differentiate are endemic to the southwest of the continent. The earliest divergence leads to the group represented today by the tall red tingles (E. brevistylis and E. jacksonii) and jarrah (E. marginata) recognized as the Jarrah bioregion (clade 1, Table 14.3) found in the high rainfall areas on well-drained, loamy soils and river valleys or, for E. marginata, on

summary of hypothesized clades, their distribution, and environment

TABLE 14.3.

Clade

Distribution and Environment

WESTERN CLADES

1 E. brevistylis, E. jacksonii, E. marginata, E. staeri

2 E. patens, E. suberea, E. lateritica, E. todtiana, E. johnsoniana

3 E. megacarpa, E. aquilina, E. coronata

4 E. platydisca and E. diversifolia (?paraphyletic)

SW Jarrah and Tingle Forests: From north of Perth to Albany in the south, wet, tall forest, up to 1,250 mm rainfall on deep loams and adjacent areas of creeks; E. marginata becomes a shorter tree on poorer laterite and mallee on northern sands, rainfall to 625 mm SW Jarrah Forest bioregion: E. patens, medium to tall tree, occurs with E. marginata on moist, loamy soils in valleys not generally on laterite; Swan Coastal Plain bioregion: E. suberea and E. lateritica, small trees or mallees, north of Perth, east of Jurien Bay near Mt. Lesueur on lateritic uplands, edges of outcrops and breakaways; E. todtiana on white sandplain from north of Perth to east of Geraldton, with E. johnsoniana at the northern end of the range SW Coastal, Warren bioregion: E. megacarpa, tree on damp sands, ranging from south of Perth to Cape Leeuwin and eastward to the Albany district (375–625 mm rainfall), mallee form on peaks of Stirling Ranges; E. aquilina and E. coronata restricted distributions on south coast granites and quartzite hills Southern Goldfields: Granite outcrops near Norseman (E. platydisca); Southern Australia, coastal limestone from Madura, WA, eastward to Eucla, Eyre Peninsula, Kangaroo Island, SA, and Cape Nelson, Vic. (E. diversifolia) (Continued)

TABLE 14.3. ( CONTINUED ) Clade 5 E. preissiana

6a E. acies, E. insularis

6b E. calcicola, E. ligulata

6c E. buprestium, E. pachyloma, E. erectifolia 6d E. exilis, E. pendens, E. sepulcralis

Distribution and Environment South coast, Esperance bioregion: Lower slopes of the Stirling Ranges to the coast east of Esperance; lateritic or stony clay soil; mallee or shrub. Note that the three-item analysis places this species with clade 3. South coast: Low mallees on sands and rocky slopes; E. acies Fitzgerald National Park west toward Albany, Thumb Peak, Middle Mt. Barren, on high dunes, Cheyne Beach; E. insularis restricted North Twin Peak Island and Cape Le Grand, base of granite rocks and cliffs South coast: Low mallees, E. calcicola on calcareous soils over limestone between Cape Freycinet and Cape Hamelin, Bremer Bay; E. ligulata on granitic sand, Stirling Ranges, Haul Off Rock, east of Esperance, Cape Le Grande area South coast: Mallees, sandy soils, from lower slopes and foothills of Stirling Ranges to Bremer Bay Mallees of inland heaths: North West: east of Jurien bay, near Mt. Lesueur, on lateritic sandhills (E. exilis, E. pendens). South coast region: stony and sandy soils on quartzite eastern part of Fitzgerald River National Park (E. sepulcralis).

EASTERN CLADES

7 E. planchoniana

8 E. rubiginosa, E. sphaerocarpa, E. umbra + other mahoganies

South East Qld and McPhersonMacleay region: Low ridges and slopes in open forests, Qld to NSW (E. planchoniana) Wet tropics to McPherson-Macleay region: E. rubiginosa on sandstone, Isla Gorge Qld; E. sphaerocarpa sandstone of Blackdown Tableland Qld; mahoganies in Qld, north to near Atherton, and NSW, ridges, hills, sandstone plateaus, and coastal flats

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TABLE 14.3. ( CONTINUED ) Clade

Distribution and Environment

9a E. radiata and other peppermints; ?E. pilularis

South East: Peppermints, cool temperate, dry sclerophyll forests and woodlands, SE NSW, Vic., and Tas. E. pilularis tall forest tree, fertile south-east coastal plains, SE NSW to SE Qld. Eastern Qld and South East: Range from tall, montain, wet forests on fertile soils to small trees and mallees on shallow soils on sandstone from Qld to Tas. and SA Eastern Qld and South East: Usually dry sclerophyll forest or woodland, SA, Vic., NSW to Qld, absent from Tas. Eastern Qld and South East: Cool, wet, tall forests to low, open forests, mountains and high plateaus to coastal ranges, ridge tops and flat areas

9b E. obliqua, E. regnans and other green ashes, e.g., E. stricta

9c E. olsenii, E. muelleriana, E. deuaensis and other stringybarks 9d E. remota, E. sieberi, E. fraxinoides and other blue ashes; E. pauciflora, E. lacrimans and other snow gums, E. mitchelliana, E. stellulata, E. moorei; E. haemastoma, E. rossii and other scribbly gums; ?E. piperita

note: See also Ladiges et al. (1987). NSW, New South Wales; Qld, Queensland; SA, South Australia; Tas., Tasmania; Vic., Victoria; WA, Western Australia.

upland massive laterites (Fig. 14.7A). These three eucalypts have retained primitive characteristics of discolorous leaves with drip tips, associated with wet environments. Eucalyptus marginata (which includes three subspecies) and the related E. staeri (which has concolorous leaves and a more depauperate habit) also extend today to poorer lateritic soils and sands. Wheeler and Byrne (2006) provide evidence for some local adaptation in E. marginata correlated with divergent chloroplast lineages between present-day populations in the Swan Coastal Plain and Darling Plateau. Eucalyptus patens, in the next clade (clade 2, Table 14.3), has a geographic distribution overlapping with jarrah, occurring on moist loamy sites in valleys and some lowlands. Relatives of E. patens (E. suberea, E. lateritica, E. todtiana, and E. johnsoniana) occur to the north (Fig. 14.7B), where they grow on lateritic breakaways and outcrops or surrounding sand plain (the Swan Plain), on lower-nutrient soils. Differentiation and speciation within this lineage relates to weathering of the plateau, development of siliceous sandy soils, as well as drying cycles initiated in the mid-Oligocene or in the Neogene.

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FIGURE 14.7 Maps of Western Australian clades. Clade numbers are based on Table 14.3. The distribution of E. diversifolia (D) extends east of the margin of this map, as far as Cape Nelson in southwest Victoria.

Of similar relative age (node 2, Fig. 14.6) but to the south (Fig. 14.7C) is the lineage of E. megacarpa, E. aquilina, and E. coronata (clade 3, Table 14.3). Eucalyptus megacarpa is a subcoastal tree on damp sands, ranging from south of Perth to Cape Leeuwin and then eastward to the Albany district (the Warren bioregion) and inland to the Stirling Range. The other two species are restricted endemics of the south coastal plains

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(the Esperance bioregion), growing on stony soils on granitic and quartsize hills. These three species share a number of morphological characteristics, including large black seeds, flowers in clusters of threes, and large obconical fruits with lobes over the valves. Two, E. aquilina and E. coronata, are mallees (multistemmed shrubs). Specht (1996) correlates the mallee growth habit with low-nutrient status soils and nutritional problems of calcareous, solonized soils. Eucalyptus preissiana (clade 5, Table 14.3) is an isolated taxon, with distinctive morphology, including large flowers with yellow stamens, brown seeds that resemble chaff, and unusual trichomes on seedlings that are not recorded for any other monocalypt (Ladiges et al. 1987). It is a mallee or shrub of the south growing on subcoastal lateritic or stony soil (Fig. 14.8). The summary

FIGURE 14.8 Australia during the Early Oligocene (35.5 Ma) showing estimated shoreline (dashed line) and nonmarine sediment (stippled), after Veevers (2000). Of note is the substantial marine incursion (horizontal shading, plus arrow) over southern Australia at this time.

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phylogeny placed it at a higher position (node 8, Fig. 14.6), but the three-item analysis related it to the E. megacarpa clade, with which it shares similarities in fruit and bud shape. Eucalyptus platydisca (Nicolle and Brooker 2006) is found inland in the Southern Goldfields, on two granitic hills near Norseman (clade 4, Table 14.3; Fig. 14.7D). Possibly related is the soap mallee E. diversifolia (Fig. 14.2A), which has a disjunct distribution across southern Australia (Fig.14.7) on coastal limestone, from Western Australian Madura eastward to Eucla, Eyre Peninsula, Kangaroo Island (South Australia), and Cape Nelson (Victoria). Given the position of E. diversifolia in the phylogeny, its current distribution is explained by more recent range expansion eastward from a source population in the west, probably aided by low sea level and exposure of suitable habitat farther south into the Great Australian Bight. The species exhibits morphological and genetic variation, with three subspecies recognized (Wright and Ladiges 1997). There is evidence of a number of other sister groups within the remainder of the Western Australian monocalypts (Table 14.3), which are all placed in an unresolved polytomy in the summary phylogeny (at node 9, Fig. 14.6) but which are resolved as one clade in the three-item analysis. Brooker (2000) classified all of these mallee species in subsection Frutices, inferring their monophyly, which is supported by the three-item results (although Brooker included also E. platydisca, E. diversifolia, E. preissiana, and the E. megacarpa clade). These mallee species occur in the transitional rainfall zone (300–800 mm per year) between the highrainfall forested zone and the inland arid region, where no monocalypts occur (Hopper 1979). Some species are narrow-range, coastal endemics and may have evolved as relatively isolated populations. Byrne and Hopper (2008), in a genetic study of E. caesia, which exists as small isolated populations confined to granite outcrops, describe these habitats in southwestern Western Australia as “ancient islands in old landscapes.” Hopper (1979) also noted that during maximum marine intrusions, a mosaic of numerous islands and peninsulas would have flanked the southwestern coastline of Western Australia. It is hypothesized that differentiation within the identified clades at node 9 (Fig. 14.6) is associated primarily with edaphic factors. On the south coast, low mallees occur on granitic sands, on rocky slopes, or at the base of granite rocks and cliffs (E. acies and E. insularis, clade 6a, Table 14.3; Fig. 14.7E). Other sister taxa are differentiated by acidic or alkaline soils, with E. ligulata on granitic and quartzitic (Stirling Range) sands and E. calcicola on calcareous soils over limestone (clade 6b;

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Fig. 14.7F). The clade (6c) of E. buprestium, E. pachyloma, and E. erectifolia occurs on sandy soils on lower slopes and foothills from the Stirling Range to Bremer Bay (Fig. 14.7G). The clade of mallee inland heaths (6d) occurs in the northwest, near Mount Lesueur, on lateritic sandhills (E. exilis and E. pendens) and also the south coast region (Fig 14.7H), on stony and sandy soils on quartzite, in the eastern part of Fitzgerald River National Park (E. sepulcralis).

WEST–EAST VICARIANCE ACROSS SOUTHERN AUSTRALIA

Node 13 (Fig. 14.6) shows a significant split between west and east, with eighty-five species forming a monophyletic group endemic to the east. The southwestern and southeastern biotas of Australia are now separated by the limestone karst plain of the Nullarbor, acting as a major edaphic barrier. Furthermore, the arid climatic zone, which extends today to the Great Australian Bight from Esperance to Ceduna on the southern coast (Fox 1999), is an additional major climatic barrier. Crisp and Cook (2007) recently analyzed geographic patterns among multiple plant lineages and concluded from molecular dating that there is a congruent signal, interpreted as a vicariant event, for sixteen of twenty-three groups, clustering about the period when the Nullarbor region was inundated (mean 16–14 Ma with 95 percent confidence limits extending to approximately 30 Ma). Green (1964), Nelson (1974), and Crisp and Cook (2007) each suggested that for some plant taxa western and eastern populations could have remained connected north of the Eucla Basin in central Australia on extensive siliceous soils during warmer and wetter conditions in the Early Miocene but were isolated in the north once Miocene aridification occurred. Estimated dates by Crisp and Cook (2007) also show some west–east divergences among plants that are older, with Banksia 2 and Allocasuarina 1 having the oldest mean dates of the taxa sampled (27.5 and 21.7 Ma, respectively, with confidence limits extending up to 40 Ma), correlating with earlier marine inundation, cooling, and drying. We argue that the west–east vicariance of the monocalypts is more likely to correlate with Eocene marine inundation (Fig. 14.8) and the major climatic change experienced at the Eocene/Oligocene boundary (35 Ma), similar to the divergence estimates for Banksia and Allocasuarina (see earlier discussion in this chapter; Crisp and Cook 2007). This is

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plausible given the fossil age of Eucalyptus. Since the eastern clade includes many tall forest species adapted to wet environments (such as the mountain ash forests—Fig. 14.2B—that abut cool temperate rain forest), the first major climatic change of the Cenozoic may well have been the main driver of vicariance, subsequent to a period of physical isolation by marine transgression. Eastern Australia

Continued high humidity in southeastern Australia provided conditions for wet forests, with fossil evidence of a variety of habitat types and distinctive communities. The Murray Basin fossil record first shows a shift from Nothofagus rainforest to “dry” rain forest dominated by Myrtaceae, Casuarinaceae, Araucaria, and podocarps in the Late Oligocene to Early Miocene, and macrofossils of Eucalyptus are also first recorded in coastal southeastern Australia from this period (Hill et al. 1999). We note that E. cloeziana (subgenus Idiogenes), which is the sister taxon to the monocalypts, grows associated with rain forest in part of its range in eastern Queensland. Eastern Clades

A detailed biogeographic area analysis of eastern taxa is not presented here, since only a sample of species was included in the molecular phylogeny, but a general overview is provided. The eastern monocalypts do not occur far inland of the Great Dividing Range (Fig. 14.1, Table 14.3), where they are restricted westward by low rainfall and heavy cracking clay soils, which formed since the Late Miocene from unconsolidated alluvium (Specht 1996). Noble (1989) suggested that monocalypt species tend to be found on more acidic and lower-nutrient soils than other eucalypt subgenera, but they occur on a range of nutrient levels. Northward drift of the continent over a hot spot resulted in periodic volcanic activity in eastern Australia, producing basaltic flows on which developed red loams and krasnozems that support forest species today (Specht 1996). The earliest eastern lineages are in the warmer tropical to subtropical climates of the north, with temperatures similar to those experienced throughout the Cenozoic. The sister taxon to all other eastern monocalypts is E. planchoniana (node 13, Fig. 14.6), a presumed relictual taxon growing in open forest in coastal Queensland and New South Wales. The next lineage in the phylogeny is the clade (node 15) of E. rubiginosa

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(subgenus Primitiva) endemic to a small area, Isla Gorge, Queensland; the tall forest tree E. sphaeocarpa, on sandstone plateaus of the Blackdown Tableland, Queensland; and the mahoganies, which occur in wet sclerophyll forests extending from northern Queensland (near Cape Tribulation) south into New South Wales, north of Sydney. All other eastern lineages are more southerly, in warm to cool temperate climates. Regionalization of southeastern taxa relate to various factors, including sharp discontinuity in topography, temperature, and rainfall between elevated tablelands and adjacent coast in New South Wales and eastern Victoria; more gradual latitudinal gradients from north to south; geology and soil; the sea barrier between Tasmania and the mainland; Miocene marine incursion of the Murray Basin; and climatic swings of the Pliocene and Pleistocene. The peppermint clade (node 17) includes two groups, one restricted largely to New South Wales and Victoria and the other endemic to Tasmania (Ladiges et al. 1983). The green ashes (node 18) include the tallest wet forest species as well as small mallees growing on rocky sites. Green ashes, characterized by brown seeds and green pendulous juvenile leaves, extend from the northern New South Wales Tablelands and adjacent southern Queensland, south of the Macleay–McPherson bioregion, to South Australia and Tasmania (Ladiges et al. 1989). The blue ashes (node 19) have a similar range (Ladiges et al. 1992). They include a group (node 21) of species characterized by black seeds that range from tall wet forest species, such as E. fraxinoides, to the small tree E. remota endemic to Kangaroo Island. The related snow gums and “stellulata” group (node 22) occur at high altitude, an environment that has existed throughout the Cenozoic in the southeast. The stringybark clade (node 20) is a series of twenty-eight species of trees and mallees, generally growing on lownutrient soils and some of the driest sites of monocalypts (e.g., E. arenacea in semiarid desert of northwest Victoria). The clade extends from South Australia to Queensland (Ladiges and Humphries 1986), and its absence from Tasmania may relate to climate rather than to the various periods of high sea level that isolated the southern state.

CONCLUSION

Eucalyptus subgenus Eucalyptus occurs largely in the wetter regions of southwestern and eastern Australia. A large number of species has evolved in a range of habitats, from tall wet forest forms to mallees,

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which are adapted to low-nutrient soils. The phylogeny of the group points to early differentiation of clades in the southwest of the continent during the Paleogene, with the oldest represented in the Jarrah and Tingle forests and the more derived on the coastal plains. A major west–east vicariant event across the south of the continent is evident, arguably associated with environmental changes before or near the Eocene–Oligocene boundary. Eastern taxa are a monophyletic group, with the oldest lineages (including E. planchonia, E. rubiginosa, and mahoganies) found in eastern Queensland, where temperatures are similar to those experienced in the early history of the subgenus; more derived taxa are predominantly in southeastern Australia.

Acknowledgments

We are grateful for the invitation to participate in this Festschrift for Chris Humphries, who participated in our work on the eucalypts. Dean Nicolle provided access to plants at Currency Creek Arboretum and assisted with sampling there. Other plant material or DNA was provided by Phil Ladd, Laura Shirley, and Frank Udovicic. A plant-collecting permit was granted by the Victorian Department of Sustainability and Environment. This work was funded by an Australian Research Council (ARC) Linkage grant, including financial support from the Maud Gibson Trust, RBG Melbourne, and RBG Sydney.

APPENDIX 14.1: DATA MATRIX FOR THE SUMMARY ANALYSIS OF FORTY-THREE INGROUP TAXA AND AN ALL-ZERO OUTGROUP

Characters 1–11 are nodes with >50 percent bootstrap support in the ITS + ETS strict consensus trees, characters 12–24 morphology, and 25–27 three additional resolved nodes in the molecular analysis (two from ETS with bootstrap support, and one from ITS node C, Fig. 14.3 but without bootstrap support). Multistate characters were treated as unordered. Eucalyptus spp.

Characters (27) 00000000011 1111111122222 222 12345678901 2345678901234 567

outgroup

00000000000 0000000000000 000

patens

10110000000 0000100000010 000

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todtiana

10110000000 0100100000010 000

suberea

10000000000 0000100000010 000

marginata

11000000000 1000000200000 000

brevistylis

11000000000 1000000200000 000

megacarpa

10000000000 0201100100000 100

aquilina + coronata

10000000000 0201100100000 100

platydisca

10001000000 0000100000000 000

diversifolia

10001000000 0000100000000 000

exilis

10001100000 0300100000000 010

ligulata

10001000000 0300100100100 010

calcicola

10001000000 0300100100100 010

sepulcralis

10001000000 0300100100000 010

insularis

10001000000 0300102100001 010

preissiana

10001000000 0001100000000 010

buprestium

10001100000 0400100100000 010

pachyloma

10001000000 0400100100000 010

acies

10001000000 0300100000001 010

planchoniana

10001000000 1300100100000 011

sphaerocarpa

10001011100 1000100000000 011

rubignosa

10001011000 1000100010000 011

umbra

10001011100 1000100010000 011

pilularis

10001010010 1000100300000 011

nitida

10001010011 1000101300000 011

radiata

10001010011 1000101300000 011

regnans

10001010010 1000101400000 011

obliqua

10001010010 1000101400000 011

triflora

10001010010 1000101400000 011

spectatrix

10001010010 1000101400000 011

paliformis

10001010010 1000101400000 011

stenostoma

10001010010 1100101100000 011

sieberi

10001010010 1100101100000 011

haemastoma

10001010010 1000101100000 011

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lacrimans

10001010010 1100101101000 011

fraxinoides

10001010010 1100101100000 011

rossii

10001010010 1000101100000 011

muelleriana

10001010010 1010101000000 011

deuaensis

10001010010 1010101000000 011

APPENDIX 14.2: SOURCES OF PLANT MATERIAL AND DNA SEQUENCES

Species are listed alphabetically, and for each accession the following information is given (in order): GenBank number for ITS sequence/ GenBank number for ETS sequence; collecting locality (and MELU voucher number) or reference to place of original publication. Abbreviations: CCA, Currency Creek Arboretum (with numbers indicating the row/plant numbers of trees in the arboretum; Nicolle 2003); NSW, New South Wales; Qld, Queensland; SA, South Australia; Vic., Victoria; WA, Western Australia. E. acies, EF051489/FJ494737, ITS from Bayly and Ladiges (2007), ETS from the same genomic DNA; E. amygdalina 2, AF058496/–, Steane et al. (1999); E. aquilina, FJ494708/FJ494738, CCA 68/36, ex Lucky Bay, WA (MELU 105390); E. arenacea, FJ494709/–, Grampians, Vic. (MELU 105392); E. brevistylis, AF390527/–, Steane et al. (2002); E. brevistylis, –/FJ494739, CCA 76/24, ex Mt Frankland, WA (MELU 105386); E. buprestium, FJ494710/FJ494740, CCA 44/11, ex Wellstead, WA (MELU 103674); E. calcicola subsp. unita, FJ494711/FJ494741, CCA 137/29, ex Hauloff Rocks, WA (MELU 103676); E. cloeziana, AF190366/FJ494742, ITS from Udovicic and Ladiges (2000), ETS from same genomic DNA; E. coccifera 1, AF058502/–, Steane et al. (1999); E. coccifera 2, AF058501/–, Steane et al. (1999); E. conglomerata, FJ494712/–, CCA161/5, ex Beerwah, Qld (MELU 105522); E. croajingolensis, AF058497/–, Steane et al. (1999); E. curtisii, AF390524/–, Steane et al. (2002); E. curtisii, –/DQ352530, Parra-O. et al. (2006); E. delegatensis 1, FJ494713/FJ494743, Lake Mt, Vic. (MELU 105393); E. delegatensis 2, AF058480/–, Steane et al. (1999); E. deuaensis, FJ494714/FJ494744, CCA 141/27, ex Deua NP, NSW (MELU 105363); E. diversifolia, AF058483/–, Steane et al. (1999); E. diversifolia, –/FJ494745, CCA 152/7, ex Portland, Vic. (MELU 105389); E. dives, AF058503/–, Steane et al. (1999); E. erythrocorys, AF190365/–, Udovicic

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and Ladiges (2000); E. erythrocorys, –/FJ654422, Gibbs et al. 2009; E. eudesmioides, AF390468/–, Steane et al. (2002); E. eudesmioides, –/FJ654416, Gibbs et al. 2009; E. exilis, FJ494715/FJ494746, Ex Boyagin Rock, WA (ATSC seedlot 17671) (MELU 105524); E. fraxinoides, FJ494716/FJ494747, CCA 51/34, Mt Budawang, NSW (MELU 105361); E. gamophylla, AF390469/–, Steane et al. (2002); E. gamophylla, –/FJ654415, Gibbs et al. 2009; E. globoidea, EF051491/FJ494748, ITS from Bayly and Ladiges (2007), ETS from the same genomic DNA; E. haemastoma, FJ494717/–, CCA 35/13, ex Sydney, NSW (MELU 105362); E. insularis, EF051493/FJ494749, ITS from Bayly and Ladiges (2007), ETS from the same genomic DNA; E. jacksonii, AF390529/–, Steane et al. (2002); E. lacrimans, EF051495/FJ494750, ITS from Bayly and Ladiges (2007), ETS from the same genomic DNA; E. latisinensis, AF390532/–, Steane et al. (2002); E. ligulata, FJ494718/FJ494751, CCA 208/23, ex Cape Le Grand NP, WA (MELU 105360); E. marginata, AF390530/–, Steane et al. (2002); E. marginata, –/FJ494752, Murdoch, WA (MELU 105398); E. megacarpa 1, AF390528/–, Steane et al. (2002); E. megacarpa 2, FJ494719/DQ352533, ETS from Parra-O. et al. (2006), ITS from same genomic DNA; E. mitchelliana, FJ494720/FJ494753, Mt Buffalo, Vic (MELU 103570); E. moorei subsp. serpentinicola, FJ494721/FJ494754, CCA 91/20, ex Mt Myra, NSW (MELU 105352); E. muelleriana, FJ494722/FJ494755, CCA 142/26, ex Bodalla, NSW (MELU 105351); E. nitida, AF058481/–, Steane et al. (1999); E. nitida, –/FJ494756, CCA 163/1, ex Tullah, Tas (MELU 103675); E. obliqua, AF058484/–, Steane et al. (1999); E. pachyloma, FJ494723/FJ494757, CCA 228/18, ex Darkan, WA (MELU 105359); E. paliformis, EF051497/ FJ494758, ITS from Bayly and Ladiges (2007), ETS from same genomic DNA; E. patens, FJ494724/FJ494759, CCA 76/5, ex Manjimup, WA (MELU 105353); E. pauciflora, AF058489/–, Steane et al. (1999); E. pilularis, AF190367/FJ494760, ITS from Udovicic and Ladiges (2000), ETS from same genomic DNA; E. planchoniana, FJ494725/FJ494761, CCA 55/11, ex Gibraltar Ra., NSW (MELU 103679); E. platydisca, FJ494726/FJ494762, CCA 11/2, ex Mt Norcott, WA (MELU 105388); E. preissana subsp. preissiana, FJ494727/FJ494763, CCA 230/1, ex Frankland, WA (MELU 105358); E. pulchella 1, AF058487/–, Steane et al. (1999); E. radiata, AF058482/–, Steane et al. (1999); E. radiata, –/FJ494764, Aireys Inlet, Vic (MELU 105394); E. regnans, AF058488/–, Steane et al. (1999); E. regnans, –/DQ352536, Parra-O. et al. (2006); E. remota, –/FJ494765, CCA 69/36, ex Kangaroo Id, SA (MELU 103677); E. rossii, FJ494728/FJ494766, Black Mt, ACT (MELU 105391);

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E. rubiginosa, AF390526/–, Steane et al. (2002); E. rubiginosa, –/DQ352537, Parra-O. et al. (2006); E. sepulcralis, EF051499/FJ494767, ITS from Bayly and Ladiges (2007), ETS from same genomic DNA; E. serraensis, FJ494729/–, Wonderland Ra., Grampians NP, Vic (MELU 105523); E. sieberi, AF058495/–, Steane et al. (1999); E. spectatrix, EF051501/FJ494768, ITS from Bayly and Ladiges (2007), ETS from same genomic DNA; E. sphaerocarpa, FJ494730/FJ494769, CCA 151/26, ex Blackdown Tableland, Qld (MELU 105354); E. staeri, AF390531/–, Steane et al. (2002); E. stenostoma, FJ494731/–, CCA 193/29, ex Tuross R., NSW (MELU 105355); E. suberea, FJ494732/FJ494770, CCA 226/16, Badgingarra, WA (MELU 105356); E. tenuipes, AF390523/–, Steane et al. (2002); E. tenuipes, –/FJ799979, grown from RBG Sydney Seedbank, seed parent 961716,

ex Isla Gorge National Park, QLD (Same genomic DNA as Gibbs et al. 2009); E. todtiana 1, FJ494735/FJ494773, CCA 169/26, ex Darling Ra., WA (MELU 103678); E. todtiana 2, FJ494733/FJ494771, Leeming, WA (MELU 105395); E. todtiana 3, FJ494734/FJ494772, Mt Lesueur NP, WA (MELU 105396); E. triflora, EF051503/FJ494774, ITS from Bayly and Ladiges (2007), ETS from same genomic DNA; E. umbra, AF058505/–, Steane et al. (1999); E. umbra, –/FJ494775, CCA row 196, ex West Head, NSW (MELU 105387); E. verrucata, FJ494736/–, Mt Abrupt, Vic (same population as MELU 105190, JC Marginson 180).

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Crisp M.D., Cook L.G. 2007. A congruent molecular signature of vicariance across multiple plant lineages. Mol. Phylogenet. Evol. 43: 1106–117. Crisp M.D., Cook L.G., Steane D.A. 2004. Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Philos. Trans. R. Soc. Lond. B 359: 1551–1571. Drinnan A.N., Ladiges P.Y. 1989. Operculum development on Eucalyptus cloeziana and Eucalyptus informal subg. Monocalyptus. Pl. Syst. Evol. 166: 183–196. EUCLID. 2006. Eucalypts of Australia. Collingwood, Australia: CSIRO. Florence R.G. 1981. The biology of the eucalypt forest. In: Pate J.S., McComb A.J., editors. The biology of Australian plants. Nedlands: University of Western Australia Press pp. 147–180. Fox M.D. 1999. Present environmental influences on the Australian flora. In: Orchard A.E., Thompson H.S., editors. Flora of Australia, vol. 1, 2nd ed. Melbourne: ABRS/CSIRO pp. 163–203. Frakes L.A. 1999. Evolution of Australian environments. In: Orchard A.E., Thompson H.S., editors. Flora of Australia, vol. 1, 2nd ed. Melbourne: ABRS/ CSIRO pp. 163–203. Gandolfo M., Gonzalez C.C., Zamaloa M.C., Cuneo N.R., Wilf P. 2007. Eucalyptus (Myrtaceae) macrofossils from the early Eocene of Patagonia, Argentina. Abstract. 5th International Southern Connection Conference, 21–25th January, 2007, Adelaide, South Australia. Gill A.M., Belbin L., Chippendale G.M. 1985. Phytogeography of eucalypts in Australia. Australian Flora and Fauna series No. 3. Canberra: Bureau of Flora and Fauna. Gibbs A.K., Udovicic F., Drinnan A.N., Ladiges P.Y. 2009. Phylogeny and classification of Eucalyptus subgenus Eudesmia (Myrtaceae) based on nuclear ribosomal DNA, chloroplast DNA and morphology. Austral. Syst. Bot. 22: 158–179. Green J.W. 1964. Discontinuous and presumed vicarious plant species in southern Australia. J. R. Soc. West. Austral. 47: 25–32. Greenwood D.R. 1991. Middle Eocene megafloras from central Australia: Earliest evidence for Australian sclerophyllous vegetation. Amer. J. Bot. Suppl. 78: 114–115. Hill R.S., Truswell E.M., McLoughlin S., Dettmann M.E. 1999. Evolution of the Australian flora: Fossil evidence. In: Orchard A.E., Thompson H.S., editors. Flora of Australia, vol. 1, 2nd ed. Melbourne: ABRS/CSIRO pp. 251–320. Holmes W.B.K., Holmes F.M., Martin H.A. 1982. Fossil Eucalyptus remains from the Middle Miocene Chalk Mountain Formation, Warrumbungle Mountains, New South Wales. Proc. Linn. Soc. N.S.W. 106: 299–310. Hopper S.D. 1979. Biogeographical aspects of speciation in the southwest Australian flora. Ann. Rev. Ecol. Syst. 10: 399–422. Hopper S.D., Gioia P. 2004. The southwest Australian floristic region: Evolution and conservation of a global hot spot of biodiversity. Ann. Rev. Ecol. Syst. 10: 399–422. Ladiges P.Y. 1997. Phylogenetic history and classification of eucalypts. In: Williams J., Woinarski J., editors. Eucalypt ecology: Individuals to ecosystems. Cambridge: Cambridge University Press pp. 1–15.

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Ladiges P.Y., Humphries C.J. 1986. Relationships in the stringybarks, Eucalyptus L’Hérit. informal subgenus Monocalyptus series Capitellatae and Olsenianae: Phylogenetic hypotheses, biogeography and classification. Austral. J. Bot. 34: 603–632. Ladiges P.Y., Humphries C.J., Brooker M.I.H. 1987. Cladistic and biogeographic analysis of the Western Australian species of Eucalyptus L’Hérit. informal subgenus Monocalyptus Pryor & Johnson. Austral. J. Bot. 35: 251–281. Ladiges P.Y., Humphries C.J., Brooker M.I.H. 1983. Cladistic relationships and biogeographic patterns in the peppermint group of Eucalyptus (informal series Amygdalininae, subgenus Monocalyptus) and the description of a new species, E. willisii. Austral. J. Bot. 31: 565–584. Ladiges P.Y., Newnham M.R., Humphries C.J. 1989. Systematics and biogeography of the Australian “green ash” eucalypts (Monocalyptus). Cladistics 5: 345–364. Ladiges P.Y., Prober S.M., Nelson G. 1992. Cladistic and biogeographic analysis of the “blue ash” eucalypts. Cladistics 8: 103–124. Ladiges P.Y., Udovicic F., Drinnan A.N. 1995. Eucalypt phylogeny—molecules and morphology. Austral. J. Bot. 8: 483–497. Ladiges P.Y., Udovicic F., Nelson G. 2003. Australian biogeographic connections and the phylogeny of large genera in the plant family Myrtaceae. J. Biogeogr. 30: 989–998. Lange R.T. 1978. Carpological evidence for fossil Eucalyptus and other Leptospermeae (subfamily Leptospermoideae of Myrtaceae) from a Tertiary deposit in the South Australian arid zone. Austral. J. Bot. 26: 221–233. Lucas E.J., Harris S.A., Mazine F.F., Belsham S.R., Nic Lughadha E.M., Telford A., Gasson P.E., Chase M.W. 2007. Suprageneric phylogenetics of Myrteae, the generically richest tribe in Myrtaceae (Myrtales). Taxon 56: 1105–1128. Majer J.D., Recher H.F., Ganeshandadam S. 1992. Variation in foliar nutrients in eastern and western Australia. Austral. J. Ecol. 17: 383–393. Martin H. 1994. Australian Tertiary phytogeography: Evidence from palynology. In: Hill, R.S., editor. History of the Australian vegetation: Cretaceous to Recent. Cambridge: Cambridge University Press pp. 104–142. MacPhail M.K., Alley N., Truswell E.M., Sluiter R. 1994. Early Tertiary vegetation: evidence from spores and pollen. In: Hill, R.S., editor. History of the Australian vegetation: Cretaceous to Recent. Cambridge: Cambridge University Press pp. 189–261. Nelson E.C. 1974. Disjunct plant distributions on the south-western Nullarbor Plain, Western Australia. J.R. Soc. West. Austral. 57: 105–107. Nelson G., Ladiges P.Y. 1999. TAX: MSDOS Program for Cladistic Systematics, ver. 3.3. New York and Melbourne: Authors. Nicolle D. 2003. Currency Creek Arboretum (CCA) eucalypt research. Vol. 2. Adelaide, Australia: Author. Nicolle D., Brooker M.I.H. 2006. Formal recognition of Eucalyptus platydisca (Myrtaceae), an arid-zone monocalypt from south-western Australia. Nuytsia 16: 87–94. Noble I.R. 1989. Ecological traits of the Eucalyptus L’Hérit. subgenera Monocalyptus and Symphyomyrtus. Austral. J. Bot. 37: 207–224.

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Parra-O., C., Bayly M.J., Udovicic F., Ladiges P.Y. 2006. ETS sequences support the monophyly of the eucalypt genus Corymbia (Myrtaceae). Taxon 55 : 653–663. Pole M.S. 1989. Early Miocene floras from central Otago, New Zealand. J.R. Soc. New Zeal. 19: 121–125. Pole M.S. 1993. Early flora of the Manuherikia Group, New Zealand. 7. Myrtaceae, including Eucalyptus. J. R. Soc. New Zeal. 23: 313–328. Pryor L.D., Johnson L.A.S. 1971. A classification of the eucalypts. Canberra: Australian National University Press. Rambaut A. 1996. Se-Al: Sequence alignment editor. Available at http://evolve. zoo.ox.ac.uk/ Rozefelds A.C. 1996. Eucalyptus phylogeny and history: A brief summary. Tasforests 8: 15–26. Sanderson M.J., Purvis A., Henze C. 1998. Phylogenetic supertrees: Assembling the trees of life. Trends Ecol. Evol. 13: 105–109. Specht R.L. 1996. The influence of soils on the evolution of the eucalypts. In: Attiwill P.M., Adams M.A., editors. Nutrition of eucalypts. Collingwood, Australia: CSIRO pp. 31–60. Steane D.A., Nicolle D., McKinnon G.E., Vaillancourt R.E., Potts B.M. 1999. ITS sequence data resolve higher level relationships among the eucalypts. Mol. Phylogenet. Evol. 12: 215–223. Steane D.A., Nicolle D., McKinnon G.E., Vaillancourt R.E., Potts B.M. 2002. Higher-level relationships among the eucalypts are resolved by ITS sequence data. Austral. Syst. Bot. 15: 49–62. Swofford, D. L. 2002. PAUP*. Phylogenetic analysis using parsimony (* and Other Methods). Version 4. Sunderland, MA: Sinauer Associates. Sytsma K.J., Litt A., Zjhra M.L., Pires C., Nepokroeff M., Conti E., Walker J., Wilson P.G. 2004. Clades, clocks, and continents: Historical and biogeographical analysis of Myrtaceae, Vochysiaceae, and relatives in the southern hemisphere. Int. J. Pl. Sci. 165: S85–S105. Udovicic F., Ladiges P.Y. 2000. Informativeness of nuclear and chloroplast DNA regions and the phylogeny of the eucalypts and related genera (Myrtaceae). Kew Bull. 55: 633–645. Udovicic F., McFadden G.I., Ladiges P.Y. 1995. Phylogeny of Eucalyptus and Angophora based on 5S rDNA spacer sequence data. Mol. Phylogenet. Evol. 4: 247–256. Veevers J.J. 2000. Billion-year earth history of Australia and neighbours in Gondwanaland. Sydney: GEMOC Press. Veevers J.J., Powell C.McA., Roots S.R. 1991. Review of seafloor spreading around Australia. 1. Synthesis of the patterns of spreading. Austral. J. Earth Sci. 38: 373–389. Wardell-Johnson G.W., Williams J.E., Hill K.D., Cumming R. 1997. Evolutionary biogeography and contemporary distribution of eucalypts. In: Williams J. Woinarski J., editors. Eucalypt ecology: Individuals to ecosystems. Cambridge: Cambridge Univ. Press pp. 92–128. Wheeler M., Byrne M.A., McComb J.A. 2006. Little genetic differentiation within the dominant forest tree, Eucalyptus marginata (Myrtaceae) of southwestern Australia. Silv. Genet. 52: 254–259.

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Williams J.E., Brooker M.I.H. 1997. Eucalypts: An introduction. In: Williams J. Woinarski J., editors. Eucalypt ecology: Individuals to ecosystems. Cambridge: Cambridge University Press pp. 1–15. Wright I., Ladiges P.Y. 1997. Geographic variation in Eucalyptus diversifolia and the recognition of new subspecies E. diversifolia subsp. hesperia and E. diversifolia subsp. megacarpa. Austral. Syst. Bot. 10: 651–680.

FIFTEEN

Lynne R. Parenti and Malte C. Ebach

WALLACEA DECONSTRUCTED

A triangular-shaped area in the middle of the Indo-Australian Archipelago was delimited by Roy Ernest Dickerson and colleagues (1928) in a collaborative volume on the distribution of plants and animals of the Philippine Archipelago: “We might compare Wallacea to a narrowbased, elongated triangle lying between Sundaland and Papualand, the Lesser Sunda Islands and Timor forming its base, Luzon forming its apex” (Dickerson et al. 1928: 302). The theoretical triangle, which we approximate on the Dickerson et al. (1928) map (Fig. 15.1), encompassed the Philippines (minus Palawan and associated smaller islands), Sulawesi (formerly the Celebes) and associated islands, and the Lesser Sunda Islands (minus Bali), as well as the seas between them. We know that Dickerson et al. (1928) thought the area to be of special biogeographic significance because they gave it a name: Wallacea. The name honored the legendary British naturalist Alfred Russel Wallace. Seventy years earlier, in 1858, Wallace wrote a letter from Amboina, now Ambon, Indonesia, to colleague Henry Bates in London to report his observation of a dramatic biogeographic boundary between the Asian and Australian biota (see Wallace 1860, 1863), which was to become known as Wallace’s Line.1

Beyond Cladistics: The Branching of a Paradigm, edited by David M. Williams and Sandra Knapp. Copyright ‘ by The Regents of the University of California. All rights of reproduction in any form reserved.

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FIGURE 15.1 Wallacea, approximately the area delimited by the triangle, bounded by a modified Wallace’s Line (also known as Huxley’s Line) to the west and Weber’s Line to the east (modified from Dickerson et al. 1928: fig. 4) and the seas in between. The original caption for the map reads, “Wallacea, the unstable area between Asia and Australia.”

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Wallacea was proposed formally as the name of this area. Dickerson et al. (1928: 101) explicitly stated that they proposed a new name: “Wallacea (new geographic name).” They placed it in a classification of major zoological divisions of the Earth (Dickerson et al. 1928: 24–25) as part of the Oriental Region, assigned it a rank, indicated a synonym, and gave a brief description that was elaborated elsewhere in the text: “East Malayan Subregion (Wallacea of this book): Timor, Celebes, and Philippines, in part.” Wallacea was characterized by Dickerson et al. (1928: 27) as the “unstable area between Asia and Australia.” The instability referred to was not tectonic, but largely geologic and hydrographic: Dickerson et al. (1928: 29) explicitly restated the “General Principles” under which Alfred Russel Wallace (e.g., 1881) interpreted biogeographic history, among them “the permanence of the oceans and the general stability of continents throughout geologic time.” The stability of the Asian, or Sunda, Shelf and the Sahul, or Australian, Shelf was contrasted with the relative instability and recent formation of the topography of Wallacea (Dickerson et al. 1928: 101–102; Fig. 15.2): The present form of Wallacea has been largely attained during Pleistocene and Recent times. The sudden changes from the depths of ocean to the narrow shelf seas, the unnumbered marine step terraces veneered at times with coral-reef material, the general lack of barrier reefs and atolls, and the numerous deeps bordered by steep-sided mountain islands are the principal features that contrast strongly with those of the Sahul and Sunda shelves.

Despite the dramatic hydrographic and geologic description of Wallacea, as compared to its bordering, inferred stable continental shelves, Dickerson et al. (1928: 301) could attribute to it no special role in the formation of biogeographic distribution patterns: “Wallacea may be interpreted as a transition zone wherein Asiatic and Australian types mingle.” Likewise, Rensch (1936) and Woltereck (1937)2 called the area a “Zwischengebiet,” a transitional or intermediate zone. Croizat (1964: 822–825; 1968) somewhat reluctantly used Wallacea for an area of overlap or interdigitation between the Indian Ocean and Western Pacific biotas. In a general review of the many boundary lines that had been proposed between the Asian and Australian biotas, Simpson (1977: 118) maligned such ambiguous characterizations of Wallacea and rejected assigning “the intervening islands [between the Sunda and Sahul

FIGURE 15.2 The Malaysian Region showing the Asiatic (horizontal hatching) and Australian (vertical hatching) continental shelves (from Dickerson et al. 1928: pl. 40). Wallace’s Line (modified; also known as Huxley’s Line) and Weber’s Line (original) delimit the intermediate, triangular area Dickerson et al. (1928:26) called Wallacea (see Figure 15.1).

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shelves] to any region, subregion, transitional or intermediate zone, or the like. [Not naming the area] will not inhibit, in fact it should promote, study of the faunas on these islands.”

WALLACEA: THE ANALYTICAL PHASE

The test of Wallacea as a unique biogeographic region was largely ignored by biogeographers until interest in the area was stoked by the work of Christopher J. Humphries and others (see later discussion).3 Humphries (1990), like Simpson (1977), had little use for Wallacea as a biogeographic concept, but for starkly different reasons. Simpson rejected the classification of areas within Wallacea, whereas Humphries pointed out that a rigorous analysis that proposed a testable hypothesis of area relationships, an area classification, was needed but had never been executed. To Humphries, Wallacea was part of the descriptive and narrative phase of biogeography. The analytical phase of biogeography in which areas are defined and diagnosed rigorously and testable hypotheses of relationships among areas are proposed had yet to be broached. The Sunda Shelf (west of Wallace’s Line) and the Sahul Shelf (east of Weber’s Line) were home to readily identifiable endemic biotas. What lived in the middle could be related to Sundaland or Sahuland taxa, or taxa elsewhere in the world. Wallacea, therefore, was “an ad hoc solution to recognise the unresolved biogeographic area sandwiched between the Weber and Wallace Lines. . . . Wallacea is merely the third area of an unresolved three-area problem added to the former two-area division of Sundaland and Papualand [= Sahuland]” (Humphries 1990: 8). A comparative biogeographic analysis sensu Parenti and Ebach (2009) of Wallacea should address at least two broad questions: what are the areas of endemism contained within Wallacea, and how are they related to each other and to areas in the rest of the world? Analytical biogeography of Wallacea, in whole or in part, and adjacent areas was revived in the mid-1980s through a series of papers on a range of plant and animal taxa, including Schuh and Stonedahl (1986), Holloway (1987), Kitching et al. (1987), Cracraft (1988), Humphries (1990), Parenti (1991), Michaux (1994), and de Boer and Duffels (1996). It has continued unabated; for example, see Heads (2003), Evans et al. (2003), van Welzen et al. (2003), Brown et al. (2006), and Carstensen and Olesen (2009). Biogeographic methods applied to the region include a broad range

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Malaya/Sumatra Borneo Philippines Java/Bali Sulawesi Sula Islands/South Moluccas New Guinea/North Moluccas

FIGURE 15.3 Areagram for seven areas of the Indo-Australian archipelago as inferred from relationships of the butterfly genus Idea and the moth genus Narosa (after Humphries 1990: fig. 1a). Wallacea is not recovered as a single area in this analysis (see text for further discussion).

of phenetic and cladistic approaches interpreted within vicariance or dispersalist paradigms (see Parenti and Ebach 2009). Humphries (1990) posed a three-area problem: what are the relationships among Wallacaea, Sundaland, and Papualand? He combined the distribution patterns and relationships of the butterfly genus Idea (Kitching et al. 1987) with those of the moth genus Narosa (Holloway 1987) to produce a general areagram for the region (Fig. 15.3). The general areagram was well resolved and provided significant information about the relationships among its seven areas. Wallacea, including the Philippines and Sulawesi, was not recovered as a single area. More important, the major islands throughout the archipelago—Borneo, Sulawesi, and New Guinea—are well-known biological and geological composites (see Hall 2002), yet this had been ignored in the descriptions of areas. Sulawesi was resolved by Humphries (1990) as sister to Sula Islands/South Moluccas and New Guinea/North Moluccas, but we do not know which part of the geologically complex Sulawesi. As the islands are composites, why not draw lines through, rather than between, them (see Parenti 1991)? Yet, many biogeographic analyses still equate areas of endemism with islands or islands groups (e.g., van Welzen et al. 2003) or readily recognized political areas, such as the Philippines. The basic units of biogeographic analysis should be areas of endemism—areas circumscribed by taxa, not solely geography—as implemented 70 years ago by two malacologists, Franz and Maria Schilder (see Parenti and Ebach 2009). The Schilders equated distribution and taxonomy. They defined areas of endemism throughout the Indo-West Pacific based on mollusk distributions (Fig. 15.4; Schilder and Schilder

FIGURE 15.4 Schilder and Schilder’s (1938–1939) eighteen areas of endemism of the Indo-West Pacific (map from Powell 1957). Areas are African, Erythraean, Persian, Lemurian, Indian, Sumatran, Java, Sulu Sea, Japanese, Moluccan, Dampierian, Queensland, Melanesian, Micronesian, Oceanic, Samoan, Hawaiian, and Polynesian. A nineteenth area, South Australian, is illustrated but is not part of the analysis.

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African Melanesian Samoan Micronesian Oceanic

A

Hawaiian Queensland Dampierian Lemurian Indian Sulu Sea Japanese

B

Moluccan Sumatran Java Sea Polynesian

FIGURE 15.5 General areagram representing the combined area relationships of eleven clades of plants, fish, and invertebrates that live throughout the Indo-West Pacific (from Parenti and Ebach 2009: Fig. 9.8; see text for further discussion).

1938–1939). Note that the large, complex islands of Borneo, Sulawesi, and New Guinea, as well as Madagascar, are each part of more than one of the Schilders’ areas. These areas were used as a starting point for discovery of natural areas of endemism throughout the Indo-West Pacific in a comparative biogeographic analysis of the distribution and relationships of eleven clades of plants, fish, and invertebrates by Parenti and Ebach (2009; Fig. 15.5).

AREA MONOPHYLY

Monophyly in systematics, recognition of a natural group or clade (see Nelson and Platnick 1981), is mirrored in comparative biogeography with the recognition of area monophyly: a group of areas that share an evolutionary history that is not shared by other areas. Wallacea is not recovered as a single area but is included as part of three of Schilders’ areas: Java Sea, Sulu Sea, and Moluccan (Fig. 15.5). As an area of

WALLACEA DECONSTRUCTED / 311

endemism, Wallacea cannot withstand the test of area monophyly. Areas included within Wallacea have closer relationships to other areas than they do to areas within Wallacea itself. Wallacea has descriptive value, but it does not convey a notion of relationships; therefore, we reject it in an area classification.

INTERPRETING AND NAMING AREAS

Each comparative biogeographic analysis provides this opportunity to reassess the limits and meaning of the input areas of endemism. We reject Wallacea, but what of the areas it comprised? All are included in a larger clade in the general areagram (Fig. 15.5) that Parenti and Ebach (2009) referred to as Subregion B, or Indo-Malayan, as named by Wallace (1863). Subregion A is more broadly distributed and spans the Indian Ocean as it includes Schilders’ African area as well as seven areas east of Wallacea. Polynesian is sister to the Indo-Malayan (Subregion B) and Subregion A sister areas.4 We interpret the biogeographic meaning of Subregion A using two kinds of information: Relationships of taxa and relationships of areas. Interpreting biotic relationships with respect to Earth history is the premise of area cladistics (sensu Ebach 2003). When two biotic areas are more closely related to each other than they are to any other biotic area, we may infer that they were physically closer together during biotic divergence. On a modern globe, we might describe the distribution of Subregion A as disjunct (Fig. 15.4). On a paleomagnetic reconstruction of tectonic plates in the Early Oligocene (30 mya; Fig. 15.6), the areas in Subregion A are not disjunct but form an uninterrupted distribution across a large portion of the ancient southern continent, Gondwana. From this map, we infer that the biotic diversification event between Subregions A and B occurred at least 30 million years ago during Gondwanan breakup. The ingenuity of area cladistics is that it not only tells us the proximal distances of biotic areas but also gives a minimum estimate of when biotic divergence occurred. This is more relevant than molecular clock estimates of divergence times because it is based on more than one taxon, some or all of which may have no fossil representatives. These two Subregions became reunited during assembly of the modern Indo-Australian archipelago (see especially Hall 2002). The confluent borders of the two regions are well-documented areas of biotic overlap and interdigitation (see Croizat 1964, 1968; Vane-Wright 1991,

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FIGURE 15.6 Subregions Pandora and Indo-Malayan drawn on an Early Oligocene (30 mya) reconstruction of global tectonic plate arrangement (map from University of Texas Institute for Geophysics). The asterisk (*) approximates the location of the South Pandora Ridge in North Fiji (see text for further discussion).

among many others). Wallacea is not unique in this regard. As noted by Humphries (1990) and others, many other biogeographic regions could equally be chosen to highlight a complex, composite biota. Madagascar has long been known as another such complex area (see Regan 1922; also discussed later in this chapter). Recognition of an area of endemism based on one set of taxa is a prediction that other taxa will also be found to be endemic throughout that region. Testing such predictions is a critical part of biogeography. Madagascar was divided by the Schilders into two biogeographic areas, African and Lemurian, which in the current analysis are part of Subregion A and Subregion B, respectively. Madagascan freshwater fishes reflect this paradoxical distribution (see Sparks and Stiassny 2003). Atherinomorph fishes exhibit both patterns: Fishes of the family Aplocheilidae, order Cyprinodontiformes (sensu Parenti 1981), live in Africa, Madagascar, and throughout the Indo-Australian Archipelago as far east as Sulawesi; whereas fishes of the family Melanotaeniidae, order Atheriniformes (sensu Dyer and Chernoff 1996), live in Madagascar, Australia, New Guinea and eastern Indonesia. The geographic distributions of the subfamilies overlap in Madagascar and Sulawesi, resulting in two complex regions at the border of Subregions A and B. The complex relationships

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of Madagascar and Africa are also reflected in the distribution of taxa that live in West Africa and India, but not Madagascar. The families Notopteridae, Bagridae, Synbranchidae, and Channidae, for example, are absent from East Africa as well as Madagascar (Berra 2001). Distributions that span Subregion A, such as that of the family Melanotaeniidae, are not unusual, but because they have been viewed on modern globe, they are described as “disjunct.” Terapontid perches of the genus Mesopristes are represented in Madagascar by one species, M. elongatus, endemic to east coast drainages (Vari 1992). The other species of Mesopristes live in the Philippines, New Guinea, Fiji, and adjacent regions, what Vari (1992:6) suggested as “a more extensive historical pattern between Madagascar and the Australasian–west Pacific regions.” We agree and name this region below.

SYSTEMATIC BIOGEOGRAPHY

Because we recognize Subregion A as an area of endemism and, therefore, of biogeographic significance, we name it according to the guidelines set forth in the International Code of Area Nomenclature or ICAN (Ebach et al. 2008).5

Subregion Pandora

Diagnosis: The biogeographic region currently spanning the Indian and western Pacific oceans and comprising the following areas of Schilder and Schilder (1938–1939; Figs. 15.4, 15.6): African (including part of Madagascar), Dampierian, Queensland, Melanesian, Micronesian, Oceanic, Samoan, and Hawaiian. Description: Terrestrial and marine habitats of the aforementioned areas that include a wide range of endemic taxa, including the provannid gastropod Ifremeria nautilei Bouchet & Warén, 1991, described from hydrothermal vents in the West Pacific, including the North Fiji basin. Type locality: South Pandora Ridge named by Kroenke et al. (1989) to denote a chain of seamounts and banks in the northern part of the North Fiji Basin (see Price et al. 1990). Etymology: The subregion is named after the South Pandora Ridge in North Fiji Basin.

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Remarks: Designation of a type locality is an important part of biogeographic nomenclature. Should future work reveal that the subregion Pandora as described here is not natural and, therefore, that it be rejected in a biogeographic classification, the name is still available and could be used for that portion of the region that includes the South Pandora Ridge, for example. No such type locality was indicated for Wallacea, for example, so that name is not associated with any particular subarea (Fig. 15.1). We are unable to delimit precisely the region of Madagascar and Sulawesi included in Pandora. The Schilders placed southern Madagascar in their African region; freshwater fish distribution has traditionally divided Madagascar into the western and eastern slopes, although more detailed knowledge of distribution patterns has obscured that strict east–west division (see Sparks and Stiassny 2003). Likewise, the Schilders did not recognize a separate southeastern Sulawesi which is part of Pandora (Fig. 15.6).

THE FUTURE OF WALLACEA

Humphries (1990) argued that Wallacea could act as a touchstone, giving subtle encouragement to biogeographic study in the Indo-Australian Archipelago. One well-known program, Operation Wallacea (www.opwall.com), formed in 1995, has supported exploration and conservation in Indonesia and since expanded its efforts more broadly throughout the tropics. Although we reject Wallacea in a systematic biogeographic classification of areas, it still remains an effective and popular banner for tropical biodiversity studies and conservation. After all, it encourages and promotes interest in the life and work of Alfred Russel Wallace.

Acknowledgments

We thank Sandy Knapp and Dave Williams for the invitation to participate in the Linnean Society symposium to honor the life and work of Christopher J. Humphries, where a version of this chapter was presented. We are indebted to Chris Humphries for his many collaborations and years of friendship. Plate tectonic reconstruction maps were obtained through the courtesy of Lisa Gahagan and Lawrence Lawver, University of Texas Institute for Geophysics, The Plates Project (http://www.ig.utexas.edu/research/ projects/plates/). Tony Gill discussed some of these ideas with us.

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NOTES 1. The history of Wallace’s Line and that of other such biogeographic boundaries throughout the Indo-Australian Archipelago is well documented and need not be repeated here. The reader is referred to George (1964, 1981, 1987), Mayr (1944), Scrivenor et al. (1943), Simpson (1977), Camerini (1993), and van Oosterzee (1997) for discussion and reviews. 2. Woltereck (1937) cited authorship of the “Zwischengebiet Wallacea” as Dickerson-Merrill, singling out the contributions of E.D. Merrill in development of the concept of Wallacea among those of the other collaborators in the 1928 volume. 3. Throughout, we assess Wallacea as a biogeographic term; Wallacea Baly 1859 is a valid name for a genus of chrysomelid beetles (Woodley 2001). 4. Polynesian should not be interpreted as ancestral. Polynesian is sister to areas A and B. 5. See Zaragüeta-Bagils et al. (2009) and Parenti et al. (2009) for further discussion of the ICAN.

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Index

Acanthomorpha, 246 Acerosae, 267, 268, 269 Ackery, P. R., 48 Actinophryid helizoa, 231 Adanson, Michel, 82, 179 Adaptation of island organisms, 92, 94, 95, 96–97 in Macaronesian region, 111, 113, 117 Aeonium, 102, 103, 108, 111 Aiton, William, 129, 136, 137, 139 Alberch, P., 38 Algae, classification of, 222, 223, 224, 229, 231 Allocasuarina, 291 Alveolates, 220, 229, 230 Amoebae, 227 Amoebozoa, 220, 228 Amorphoctista, 221 Anacyclus, 22, 23, 26 Ancestry, 161, 184 common real relationships in, 183–184 relative recency of, 147 compared to descent, 151 Andrews, S., 82 Andrus, N., 103 Angiosperms, pollen wall layers of, 38–41 Animal kingdom, 219, 221, 222 Anthemideae, 25–27 Anthropocentrism, 61 Apicomplexa, 230 Apomorphy, 55, 154

Arabidopsis, 38, 39, 40, 41, 42 Archaeplastida, 220, 228–229 Archetista, 223 Areagrams, 310, 312, 313 Area monophyly, 312–313 Argyranthemum, 82, 111, 113, 115 Cuninghame collection of, 131, 132 distribution of, 110 Humphries research on, 20, 21, 25, 26, 82, 101, 131 The Ark, 130 Armstrong, J., 59 Arteaga de La Guerra, Isidoro, 131 Artemisia, 26 Artifacts and monographic effects on stratigraphic distribution of brachiopods, 197–215 Artificial system of classification, 81, 187, 188 differentiated from natural method, 181, 182 Asia, and Wallacea as transition zone to Australia, 305–317 Aspidorhynchidae, 248–250 phylogeny of, 249, 253 Aspidorhynchus, 249, 250 Asplenium hemionitis, 134–135 Asteraceae, 20, 25, 92 Atkinson, Ian, 52 Atomism, 53, 56, 57, 61 Australia, 28, 29 Eucalyptus in. See Eucalyptus in Australia 319

320 / INDEX

Australia (continued) past environments of, 283–284 and Wallacea region as transition zone to Asia, 305–317 Autapomorphy, 153, 155 Axostyla, 232, 233 Azores, 101, 102, 125, 136 Azorina, 114, 115 Back-dispersal from Macaronesian region to continent, 102, 108 Bacteria, classification of, 223 Baillie, Jonathan, 50 Baker, Herbert, 93 Baker’s rule, 93, 97 Baldwin, B. G., 111 Banks, Joseph, 137, 138, 140 Banksia, 291 Baranov, V. V., 209, 210 Barcoding, DNA, 69–70, 155–157, 158–160 Barker, D., 169 Barnacles, Darwin study of, 83 Barratt, Spencer, 93 Bassett, L., 59 Bates, Henry, 305 Bather, Francis, 179 Baum, B. R., 24 Bayesian analysis, 243 Beagle expedition, 140, 141 Beaufort, Duchess of, 129 Belonostomus, 249, 250 Bemis, W. E., 262 Bentham, George, 25 Bertalanffy, L., 149, 150, 152, 162 Besnard, G., 108 Bias, and monographic effects on stratigraphic distribution of brachiopods, 197–215 Bidens, 93 Biodiversity of brachiopods, 204–208 monographic artifacts affecting interpretation of, 197–215 calculus of, 49, 56 conservation of, 47–61 currency of, 50, 60 in Great Ordovician Biodiversification Event, 204, 206 importance of taxonomic information on, 70–73, 78 island hot spots of, 91–92 potential impact of climate change on, 91–98 in Macaronesia, 102, 113, 117 measures of, 111 presentist approach to, 160, 161

range size rarity measure of, 111 root weight measure of, 49, 50, 51–56 specialists with limited interest in, 68 taxonomic distinctness in, 51, 52 of teleost fish, 255–259, 260 Biogenetic law, 37 Biogeography, 20–21, 36 area monophyly in, 312–313 cladistic, 27–28 of Eucalyptus in Australia, 267–299 historical, 27–28 of Macaronesian plant groups, 103, 110 of teleost fish, 243–264 vicariance, 27–28 of Wallacea region, 305–317 Biogeography and Conservation Laboratory, 49 Bioinformatics, 180 Blackmore, Stephen, 20, 36–37, 38, 40, 41 Borda, Jean Charle, 140 Bosea yervamora, 129 Botany cladistics in, 21–25, 28, 36 and impact of climate change on island biodiversity, 91–98 of Macaronesia flora, 101–141 early British collectors and observers of, 125–141 endemism and evolution of, 101–117 Brachiopods, stratigraphic distribution of, 203–208 monographic artifacts affecting, 197–215 Bradshaw, A. D., 96 Bramwell, David, 20 Branch lengths, 53, 56 Breeding systems of island plants, 93, 96, 97 Bremer, Kåre, 23, 24, 25, 26, 28 British collectors and observers of Macaronesian flora, 125–141 Brito, P. M., 249 Brooker, M. I. H., 267–268, 278, 282 Broussonet, Auguste, 140 Brown, G. K., 309 Brundin, Lars, 24, 27, 28 Brunton, C. H. C., 199, 203 Buckman, S. S., 209, 210, 212 Butschli, O., 222 Buttercups, 184–186 Butterflies, 310 mimetic, 48 Byrne, M., 290 Bystropogon canariensis, 129 Cabo Espichel, 102, 108, 110 Cain, Arthur, 171, 178, 179, 180 Callose cell wall, variations in, 38

INDEX / 321

Campanula, 115 Canary Islands, endemic flora of, 101, 108, 109 dispersal ability of, 110 distribution of, 111, 112 diversity of, 111, 112, 113 early British observers and collectors of, 125, 128–134, 136 molecular phylogenetic analysis of, 103 Plukenet writings on, 134 Candolle, Augustin Pyramus de, 181–183 translations of work of, 182, 183, 187 Cape Verdes, 101, 102 Capsaspora, 227 Carine, M. A., 102, 103, 113 Carlquist, Sherwin, 92, 97, 110 on island syndrome, 92–98 Carstensen, D. W., 309 Catalogue of Life, 78 Causally integrated systems, 155 Cavin, L., 254, 258, 259 Cell lineages, 162 Cellular organization as basis of classification, 224 Cenozoic, Australian environment in, 283, 292 Chalker, Lynda, 49, 56 Chanoids, 251 disparity of, 262, 263 phylogeny of, 252, 253 Character advanced, 37 morphological of Eucalyptus, 273, 274 importance of, 83 of teleost fish, rate of evolution, 259–262, 263 in phenetics, 171–172 in phylogeny reconstruction, 187–188 primitive, 37 reciprocal illumination in reevaluation of, 80 Chelsea Physic Garden, plant hunting for, 128–130 Chippendale, G. M., 282 Chlorophyta, 222 Choanoflagellates, 226–227 Chorological method, 28 Chrysanthemum, 26 Cicero, C., 156 Ciliophora, 230 Clades, 154 Cladistically resolved unit, 153–154 Cladistic Biogeography (Humphries and Parenti), 28 Cladistics in biodiversity conservation, 47–61

biogeographic, 27–28 botanical, 21–25, 28, 36 classification in, 147, 176, 186, 188 compared to phenetics, 171, 176 definition of, 170–171, 174–175 hierarchy in, 147–153 inferences on relationships in, 54 in Macaronesia flora analysis, 102–103, 110–111, 114, 116–117 pattern and process in, 147 real relationships in, 187 shared ancestral characters in, 180 species category in, 153–160 Cladistics journal, 24 Cladocyclus, 254 Cladograms, 71 interpretation of, 147 in root weight measure, 49–50, 51–52 lability problem in, 54–56 terminal taxa in, 51–52 used as phylogenetic trees, 243 Classification artificial, 81, 187, 188 differentiated from natural method, 181, 182 in cladistics, 147, 176, 186, 188 of Eucalyptus, 267–270 of eukaryotes, 219–233 information content of, 51 natural, 81, 82, 173, 182–183, 188 differentiated from artificial method, 181, 182 number of kingdoms in, 219–225 in phenetics, 176, 177–178, 179, 180 in systematics, 180 terms and components in, 51 Class-inclusion hierarchy, 149, 151 Climate change, potential impact on island biodiversity, 91–98 Coevolution, 48 Collapse (Diamond), 98 Collins, N. M., 48 Complementarity principle, 49, 53 Compositae, 25, 35–36 pollen walls of, 41 tribal relationships in, 36 Concatenation concept, 172 Conservation International, 91 Conservation issues, 21, 47–61 complementarity principle in, 49, 53 critical faunas analysis in, 48, 49 ethical questions in, 57–58 importance of taxonomic information in, 70–73 for islands, 94–95, 98 root weight measure in, 49, 50, 51–54 species rights and equality in, 50–51, 56

322 / INDEX

Convolvulus, 102, 108, 109, 114 Cook, L. G., 291 Cooper, G. A., 209, 210, 212, 213, 214 Copeland, H. F., kingdoms in classification system of, 222–223 Copernican revolution, 58 Copernicus, Nicolaus, 58–59 Cordier, Pierre Louis Antoine, 140 Cotula, 25 Cracraft, J., 309 Crane, P. R., 38, 40, 41, 153 Crawford, D. J., 93 Creating a Taxonomic E-Science (CATE), 78 Cretaceous Australian environment in, 283 brachiopods in, 210 Eucalyptus in, 282 geological activity in, 246 land-sea configuration in, 247, 248 teleost fish in, 244, 246, 248, 250–251 disparity of, 262, 263 distribution of, 252–255 diversity of, 255–259, 260 vicariant events in, 255 Crisp, M. D., 291 Critical faunas analysis, 48, 49 Croizat, L., 27, 181, 307 Cuboidea, 267, 268, 269 Cuninghame, James, 127, 135 Canary Islands plant collection of, 130–134 “Current Concepts in Plant Taxonomy” (Humphries and Funk), 36 Curry, G. B., 199, 203 Cuvier, Georges, 179, 220 Danser, Benedictus, 22 Darwin, Caroline, 140 Darwin, Charles, 59, 60, 72, 83, 127, 140–141, 170 on Natural System, 184 Darwinian revolution, 58 Dawkins, Richard, 57 de Boer, A. J., 309 Dendrograms, 172, 173–174, 175 Depauperation in island plants, 92, 93 Derived traits, 23 woodiness of island plants as, 114, 115 Descendants compared to ancestors, 151 in division hierarchy, 150, 161 in genetic hierarchy, 150 Haeckel on, 184 Hennig on, 151, 161

Descriptive taxonomy, 69, 77–84 compared to name lists, 78–79, 81, 84 importance of, 77–84 Devonian period, brachiopods in, 203–204, 205, 206, 207–208, 210 monograph artifacts affecting interpretation of, 213 Diadromy in fish, 246 Diamond, Jared, 98 Dickerson, Roy Ernest, 305, 307 Dinoflagellata, 230 Dioecious island plants, 93, 97 Diphyletic groups in Macaronesian flora, 108 Disparity measures of, 261 of teleost fish, and rate of morphological evolution, 261–262 Dispersal in biogeography, 27 of island organisms, 92, 94, 97 of Macaronesian flora, 110–111 and back-dispersal from Macaronesian region to continent, 102, 108 of pollen, 38 of teleost fish, 254–255 Distinctness, taxonomic, 52 index of, 51 Distribution of Anthemideae, 25–26 in biodiversity conservation, 49 of brachiopods, stratigraphic, 203–208 monographic artifacts affecting, 197–215 and eco-geographical specialization, 21–22 of Eucalyptus in Australia, 267–299 historical biogeography in analysis of, 27–28 of teleost fish, 243–264 Diversity, biological. See Biodiversity Division hierarchy, 147–152, 161 DNA sequence data, 36, 79, 80 on Anthemideae, 26–27 in barcode, 69–70, 155–157, 158–160 on Eucalyptus, 272–281, 295–299 as intrinsic property of organism, 160 in species recognition, 155–157 Donoghue, M. J., 155 Doody, Samuel, 129, 135 Dracaena draco, 125 DRIP clade, 227 Duffels, J. P., 309 Dujardin, F., 227 Dwarfism of island organisms, 115

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Ebach, M. C., 21, 309, 313 Echium, 102, 113, 114, 115 distribution of, 110 EDGE program, 50 Ellimichthyiforms, 250–251 disparity of, 262, 263 phylogeny of, 250, 253 Encyclopedia of Life, 78 Endemic species in Indo-West Pacific, 311, 312 in island hot spots, 91, 93 in Macaronesian region, 101–141 early British collectors and observers of, 125–141 evolution of, 101–117 in Wallacea, 313 “Endemism and Evolution in Macaronesia” (Humphries), 20, 22, 102, 116 Eocene Australian environment in, 283, 284 Eucalyptus in, 282, 283, 284, 291 Epigenetic events, 40–41, 42 Equivalence, taxonomic, 52 Erehendorfer, F., 97 Essentialism, 178, 179 ETS data set on Eucalyptus, 272–275 combined with ITS data set, 278, 279, 281 Eucalyptus in Australia, 20, 28, 267–299 age and palaeo-distribution of, 282–283 classification of, 267–270 current distribution of, 268, 271 data matrix for summary analysis of, 295–296 distribution and environment of, 285–291 DNA sequence data on, 272–281, 295–299 in eastern region, 292–293 methods of study, 272–275 morphological characters of, 273, 274 phylogenetic analysis of, 273–281, 284 sources of plant materials studied, 272, 297–299 in southwestern region, 284–291 vicariance in, 267–299 Euglena, 225 Euglenozoa, 232 Eukaryotes, 219–233 Euphorbia, 102, 108, 135 Evans, B. J., 309 Evo-devo research, 37, 42 Evolution belief in, affecting research funding, 68–69 in cladistics, 153

distribution and eco-geographical specialization in, 21–22 and diversity measurements, 53 of island organisms, 93, 94, 97 in Macaronesian region, 101 of mimicry, 48 species as basic unit of, 154, 161 of teleost fish, 243–264 morphological, 259–262, 263 taxic, 255–259 Evolutionary significant unit, 155, 156 The Evolving Biosphere, 29 Excavates, 220, 232–233 Extinction of brachiopods, 198, 203–205 monographic artifacts affecting interpretation of, 197–215 and importance of taxonomy, 70, 71 of island organisms, 92, 94, 95, 97, 98 of teleost fish, 248–251, 254 Extrinsic properties of organisms, 160 Faith, Dan, 50 Fallacy of misplaced concreteness, 55 Farris, J. S., 24–25 Fauna, critical analysis of, 48, 49 Felsenstein, J., 171, 176, 177, 179–180 Fermi, Enrico, 71 Fernandez, L. O., 59 Ferrespecies, 155 Feuillée, Louis, 135, 140 Feynman, Richard, 70 Fish diadromy in, 246 teleost, 243–264 Flora Europaea, 19–20 Flora of Macaronesian region, 101–141 early British collectors and observers of, 125–141 endemism and evolution of, 101–117 Floras, compared to monographs, 80–82 Flore françoise (Lamarck), 81, 181 Florence, R. G., 270 Floristics, 81, 82 Forey, P. L., 25, 28, 29, 36, 258, 259 Fornicata, 232, 233 Fossils, 73 of brachiopods, monograph artifacts and biases affecting stratigraphic distribution of, 197–215 of teleost fish, 243–264 ghost lineages in, 256–259 Friends of the Earth, 49 Fruitices, 282, 290 Fundamentals of Comparative Biology (Rieppel), 53 Funding of taxonomy research, 69, 77

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Fungi, classification of, 221, 223, 224, 226 Funk, D. J., 156 Funk, V. A., 23, 24, 36 Gaia theory, 56 Gardiner, B. G., 28, 36 Genetic hierarchy, 150, 152 Genetics DNA sequence data in. See DNA sequence data and epigenetic events, 40–41, 42 and qrt mutations, 41 in Arabidopsis, 38, 39, 40 Geologic Time Scale, 202 Ghost lineages, 256–259, 260 Gigantism of island organisms, 115 Gilmour, J. S. L., 178, 179 Givnish, T. J., 94 Glaucophyta, 229 Glebionis, 26 Global Biodiversity Information Facility, 78 Goldfuss, G. A., 221 Gondwana, 313 Grande, L., 262 Grant, V., 224 Graybeal, A., 155 Great Ordovician Biodiversification Event, 204 Green, J. W., 291 Gregg, J. R., 148, 149, 151, 152 Grimes, J. W., 81 Ground plan divergence method, 22 Growth forms of Macaronesian flora, 113–116, 117 woodiness in. See Woodiness of island plants Guédès, Michel, 179 Gymnosperms, pollen wall layers of, 38–41 Habitat destruction affecting island organisms, 92, 95 Haeckel, Ernst, 170, 184, 185, 188 kingdoms in classification system of, 221–222 Harborne, Jeffrey, 25 Harrison, G. A., 171 Havlicek, V., 209, 210, 211 Hawaii, 93, 110, 113, 114 Heads, M. J., 309 Hebert, P. D. N., 156 Heliantheae, 36 Heliconius, 48 Hennig86, 26 Hennig, Willi, 22, 27, 48, 72 on hierarchy, 148–149, 150, 151, 152 on monophyletic taxa, 161, 170

phylogenetic system of, 153, 174, 180 reciprocal illumination concept of, 79–80 relationship diagram of, 174–175 Henslow, John S., 140, 141 Heterolobosea, 232 Heywood, Vernon, 20, 25, 35 Hierarchy, 147–153 class-inclusion, 149, 151 division, 147–152, 161 genetic, 150, 152 Hennig interpretation of, 148–149, 150, 151, 152 Linnaean, 148–152 of monophyletic groups, 151, 152, 153, 161–162, 173 nested, 152 phylogenetic, 147, 151, 173 in root weight measures, 53 of similarity, 149 spatial, 150 Hill, C. R., 153 Hill, R. S., 283, 284 Historical biogeography, 27–28 Hogg, J., 221, 222 Holistic approach in root weight measures, 53 Holloway, J. D., 309 Holon, 56 Homology, 37, 175, 179, 180 assessment of, 80 hypothesis of, 83 and natural affinity, 183 in phenetics, 178 in pollen wall layers of angiosperms and gymnosperms, 38–41 and similarity, 187 Homoplasy, 55, 179 Homozygosity, escape from, 93 Hopper, S. D., 290 Horti Sicci collection of Sloane, 126, 128, 130, 131, 132 Hughes, A. L., 171 Hull, D. L., 148, 149, 157, 177, 178 Human-Earth relationship, 61 revolutions in perspective on, 58–59 Humphries, Chris, 273 acknowledgments mentioning, 61, 74, 117, 162, 215, 264, 294, 316 Anthemideae work of, 25–27 appointment to Botany Department in Natural History Museum, 19, 36, 48 Argyranthemum research of, 20, 21, 25, 26, 82, 101, 131 bibliography of works by, 3–18 in biodiversity conservation movement, 47–61 and biogeographic cladistics, 27–28

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biographical information on, 19–21 and botanical cladistics, 21–25 “Endemism and Evolution in Macaronesia” paper, 20, 22, 102, 116 in evo-devo research field, 37, 42 honors awarded to, 21 and importance of taxonomy, 72 influence of, 28–29, 35–37 organizing “Modern Views of Kingdoms and Domains” conference, 219 as research student at the University of Reading, 35 root weight measure of, 49, 50, 51–56 Wallacea research of, 309, 310, 314, 316 Huxley, Julian, 181 Huxley’s Line, 306, 308 Hypotheses in taxonomy, 67–68, 70, 79, 82 of homology, 83 Ichthyodectiforms, 254 disparity of, 262, 263 phylogeny of, 255 Idea, 310 Idiogenes, 267, 268, 269, 281, 292 Inclusive hierarchy, 147, 149, 152, 161–162 Indo-West Pacific, areas of endemism in, 311, 312 Inferring Phylogenies (Felsenstein), 176, 177, 179–180 Instrumentalism, 157, 158, 161 Integrated Taxonomic Information System, 78 International Code of Botanical Nomenclature, 79 International Conference on Systematic and Evolutionary Biology, Third (1985), “Ontogeny and Systematics” symposium at, 37 International Union of Geological Sciences, 203 Intrinsic properties of organisms, 160, 161 Invasive species affecting island organisms, 92, 94, 96 Island Biology (Carlquist), 92 Islands as biodiversity hot spots, 91–92 potential impact of climate change on, 91–98 common characteristics of organisms from, 92–98 in Macaronesian region, flora of, 101–141 early British collectors and observers of, 125–141 endemism and evolution of, 101–117

Island syndrome, 92–98 Ismelia, 26 ITS data set on Eucalyptus, 270, 272–278, 279 combined with ETS data set, 278, 279, 281 parsimonious tree based on, 277 strict consensus tree based on, 276 Jacquin, Nicolaus, 138, 139 Jahn, F. F., 223, 224 Jahn, T. L., 223, 224 Jakobids, 232 Jamaica, visit of Sloane to, 128 James-Clark, H., 227 Jarvis, Charlie, 20, 36 Jensen, Richard, 169, 170 Johnson, L. A. S., 267 Jurassic period land-sea configuration in, 247, 248 teleost fish in, 248, 249, 251 vicariant events in, 255 Jussieu, Antoine Laurent de, 184 Kellert, S. R., 59 Kent, W. S., 222 Kew Gardens, Masson as official collector for, 135–136 Keys for identification, 82–83 Kingdoms in classification systems, 219–225 in five-kingdom system, 224 in four-kingdom system, 222–223 in nineteen-kingdom system, 224–225 in six-kingdom system, 223 in three-kingdom system, 221–222 in two-kingdom system, 219–221, 222 Kitching, I. J., 309 Kluge, A. G., 24–25 Koponen, Timo, 22 Kroenke, L. W., 315 Ladiges, P. Y., 28, 273 Lamarck, J.-B., 81, 181, 220 Lantern fish, 248 Lauraceae, 113 Laurisilva, 113 Lavandula, 82 Lavatera, 108 Least-inclusive taxonomic unit, 154–155 Leedale, G. F., 224–225 Leiserowitz, A. A., 59 L’Héritier, Charles-Louis, 139 Link, Johann, 139 Linnaean hierarchy, 148–152

326 / INDEX

Linnaeus, Carl (elder), 60, 72, 81 on artificial and natural systems, 181, 182 kingdoms in classification system of, 219 Masson writing to, 137, 138 Linnaeus, Carl (younger), Masson writing to, 137, 138–139 Linnean Society, 21, 24, 29, 126, 138, 219 Longevity of island plants, 92, 97 Longistylis, 282 Lovelock, Jim, 56, 59 Lovelockian revolution, 58 Løvtrup, S., 37, 53 Lowe, Richard, 140, 141 Macaronesia flora, 101–141 biogeography of, 103, 110 early British collectors and observers of, 125–141 endemism and evolution of, 101–117 growth form of, 113–116, 117 intraregional radiation of, 103, 111–113 molecular phylogenetic studies of, 103, 104–107, 111 relationship with Mediterranean flora, 110, 117 Madagascar, 314–315, 316 Madeira, 101, 102, 125 Masson travel to, 136 Plukenet writings on flora of, 134 Sloane visiting, 127–128, 134, 135 Majer, J. D., 270 Malaysian region, 308 Mallet, J., 159 Martin, H., 282 Masson, Francis, 127, 135–139, 140 Maximum likelihood analysis, 243 May, Robert, 49, 56 Mayr, E., 173, 174, 175, 178 nondimensional species concept of, 158, 160 McNeilly, T., 96 Mediterranean flora, relationship with Macaronesian flora, 110, 117 Meiosis, 41 Melderis, Alexsandr, 19 Mesomycetozoa, 227 Mesopristes, 315 Metaphyta, 223 Metaspecies, 155 Metazoa, 223 Methods artificial and natural, 182 differentiated from systems, 182 Michaux, B., 309 Mickevich, M., 51 Micomeria herpyllomorpha, 131, 132

Microsporidia, 227–228 Migration of island organisms, 94, 95–96, 97 Mimicry, evolution of, 48 Ministeria, 227 Miocene Australian environment in, 284 Eucalyptus in, 282, 283, 292 Mishler, B. D., 154, 170 Mitochondria, classification systems based on, 225, 227 “Modern Views of Kingdoms and Domains” conference, 219 Molecular operational taxonomic unit, 155, 156 Molecular phylogenetics, 78 DNA sequence data in. See DNA sequence data of Macaronesian endemic plants, 103, 104–107, 111 Monera, 223, 224 Archigonic, 221 Neutral, 221 Vegetable, 222 Monographs artifacts and biases in, affecting stratigraphic distribution of brachiopods, 197–215 compared to floras, 80–82 Monophyletic groups, 151, 152–153, 244 of areas in biogeography, 312–313 asymmetry between tokogenetic systems and, 153, 154 hierarchy of, 151, 152, 153, 161–162, 173 kingdom system in classification of, 224–225 in Macaronesian region, 108 of teleost fish, 244 Moritz, C., 156 Morphology of Eucalyptus, 273, 274 importance of data on, 83 of teleost fish, rate of evolution, 259–262, 263 Morris, M. G., 48 Müller-Wille, S., 181 Mychota, 222, 223 Myctophiformes, 244 Myers, N., 91 Myrica faya, 131, 132 Myrtaceae, 282, 284 Myrtaceidites, 282 Myxomycetes, 223, 224

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Name lists, compared to descriptive taxonomy, 78–79, 81, 84 Narosa, 310 National Parks of the World, 48 Natural affinity, 183 Natural groups, 173, 179 Natural History Museum, 126, 128, 138 Humphries joining Botany Department at, 19, 36, 48 Natural System, Darwin on, 184 Natural system of classification, 81, 82, 173, 182–183, 188 differentiated from artificial method, 181, 182 Nelson, E. C., 291 Nelson, G. J., 27, 37, 73, 182, 184 Neogene, Australian environment in, 284 New Systematics, 178, 181, 187 Newton, Isaac, 72 Nixon, K. C., 154 Noble, I. R., 292 Nothofagus, 20, 28, 68 Numerical taxonomy, 24, 169–170, 171, 176–181 Numerical Taxonomy (Sneath and Sokal), 177, 178, 180 Nutrition, as basis of classification, 224 Olea europaea, 108 Olesen, J. M., 309 Oligocene Australian environment in, 283–284, 289 Eucalyptus in, 283, 292 Wallacea in, 313, 314 Olmstead, R. G., 155 Omland, K. E., 156 Ontogeny, 54 pollen and spore in, 38–42 predictive models in, 38, 42 and systematics, 37–42 Ontogeny and Systematics, 37–38, 40, 42 Opalinids, 231 Operation Wallacea, 316 Opisthokonta, 220, 226–228 Ordovician period brachiopods in, 203–204, 205, 206, 207, 210, 214 Great Biodiversification Event in, 204, 206 Ortiz, J. E., 113 Osmitopsis, 25 Osteoglossomorpha, 244, 262, 263 Outbreeding capacity of island organisms, 93 Out-group comparisons, 37 Owen, R., 72, 221

Paleocene Australian environment in, 283 Eucalyptus in, 282–283 Paleogene, Eucalyptus in, 282 Palynology, 36, 38–42 Pandora subregion, 315–316 Paraphyletic groups, 244 of Macaronesian flora, 103, 108, 110 of teleost fish, 244 Paraphyly, 184 Parenti, L. R., 24, 28, 309, 313 Parsimony, 22, 24–25, 83, 174 in Eucalyptus analysis, 273, 275, 277, 278, 279 Passifloraceae, 48 Passmore, John, 58 Pattern analysis, 147, 153 Patterson, C., 27, 28–29, 36, 153, 259 Pericallis, 113, 114 Permian period, brachiopods in, 204, 205, 206, 214–215 Permian-Triassic mass extinction, 205, 206 Petiver, James, 130, 131 Phenetics, 24, 54–55, 169–188 classification in, 176, 177–178, 179, 180 compared to cladistics, 171, 176 definition of, 171–174 similarity in, 171–174, 176, 177, 178 Phenograms, 71, 172, 173–174 Phenon, 173, 178 Phenotypic characters, unusual or distinctive, 42 Philosophia Botanica (Linnaeus), 81 The Philosophy of Inductive Sciences (Whewell), 182–183 Phyllis nobla, 131, 132 PhyloCode, 154 Phylogenetics, 73 classification in, 180 and descriptive taxonomy, 79 diversity in, 56, 57 measures of, 50, 53, 111 DNA sequence data in, 36, 78, 80 of Eucalyptus, 273–281 hierarchy in, 147, 151 of monophyletic taxa, 173 inferences on relationships in, 54 of Macaronesian endemic plants, 103, 104–107, 111 Phylogenetic systematics, 23–24, 28, 36, 48. See also Cladistics Phylogenetic Systematics (Hennig), 180 Phylogenetic trees, 71, 82, 83, 147, 243–244 cladograms used as, 243

328 / INDEX

Phylogeny number of characters in reconstruction of, 187–188 origin of term, 184 Phylogeographic groups, 156 Phytographia (Plukenet), 134 Pinus canariensis, 131, 132 Piqué, Herrera, 135 Plant kingdom, 219, 221, 222, 224, 228 Platnick, N. I., 27, 51, 182 Pleijel, F., 154, 155 Plesiomorphy, 23 Plesiospecies, 155 Plukenet, Leonard, 129, 134–135 Poaceae, 20 Poggio, Juan B., 130–131 Pollen and aperture positioning, 41–42 morphology and ultrastructure of, 36, 38–42 self-assembly model, 41 Pollination of island plants, 93, 96, 97 Polyphyletic groups of Macaronesian flora, 110 Popper, Karl, 68 Precinctiveness, 97 Predictive models all-or-nothing, 68 in ontogeny, 38, 42 Press, J. R., 82 Preuss, Daphne, 38 Primitiva, 268, 269, 282 Primitive traits, 37 woodiness of island plants as, 113 Principles of Numerical Taxonomy (Sokal and Sneath), 176, 177–178 Prokaryotes, 222, 224, 225 Proteaceae, 284 Protista, 221–222, 223, 224 Protoctista, 221, 222, 223, 224 Protozoa classification of, 221, 222, 223 introduction of term, 221 Pryor, L. D., 267 qrt mutations, 41 in Arabidopsis, 38, 39, 40 Q values in root weight measure, 51, 52 Radiation of brachiopods, 198, 203, 213 monographic artifacts affecting interpretation of, 197–215 of island organisms, 94 in Macaronesian region, 103, 111–113, 117 of teleost fish, 254–255

Ramsay, Marmaduke, 140 Range size rarity, 111 Ray, John, 71 Realism, scientific, 158 Real relationships, 183–184, 186–187, 188 Reciprocal illumination, 79–80, 83, 157 Reciprocal monophyly, 162n2 Regnum Primigenum, 221 Rensch, B., 307 Reproduction genetic hierarchy in, 152 of island plants, 93, 96, 97 Research funding, 69, 77 Reyes-Betancort, J. A., 111 Rhizaria, 220, 230, 232 Rhodophyta, 229 Rhynchonellida, stratigraphic distribution of, 207–215 authors of publications on, 208–215 Richardson, P. M., 23 Rieppel, Olivier, 53, 60 RNA, classification systems based on, 225 Root weight measure, 49, 50, 51–56 lability problem in, 54–56 Rosen, D. E., 27, 259 Ross, Herbert, 169, 176 Rouse, G. W., 154, 155 Rutherford, Ernest, 67 Sakai, A., 93 Salvages, 101, 102, 125 Sartenaer, P., 209–213 Savolainen, V., 156 Schaefer, H., 113 Schilder, Franz, 310–312, 314, 315, 316 Schilder, Maria, 310–312, 314, 315, 316 Schlee, Dieter, 180 Schuh, R. T., 309 Scientific realism, 158 Scotland, R. W., 83 Self-incompatibility of island plants, 93, 97 Semele androgyna, 131, 132 Sepkoski Curve, 204, 206, 208 Sideritis, 113, 115 Similarity in appearance, 186 hierarchy of, 149 measures of, 187 in phenetics, 171–174, 176, 177, 178 and real relationships, 186–187 Simmons, Thomas, 127, 129, 135 Simpson, A. G. B., 233 Simpson, G. G., 307, 309 Sister group relations, 28, 51–52 of Macaronesian endemic plants, 104–107, 110–111, 114–116 Skvarla, John, 36

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Sloane, Hans, 130, 134 Horti Sicci collection of, 126, 128, 130, 131, 132 visit to Madeira (1687), 127–128, 134, 135 Sloane Manuscript Collection of the British Library, 128, 131 Smith, A. B., 256 Sneath, P. H. A., 24, 170, 172–173, 176, 177, 178, 179, 182 Sokal, R. R., 24, 172–173, 176, 177, 178, 179, 182 Solanaceae Source, 78 Solander, Daniel, 140 Sonchus, 102, 111, 113 Sparrman, Anders, 138 Spatial hierarchy, 150 Speciation events, 159 Species in cladistics, 153–160 definitions of, 153, 154, 161 discovery and description of, 69, 77–78 DNA barcoding in identification of, 69–70, 155–157, 158–160 evolution of, 154, 161 extinction of, 70, 71. See also Extinction inequality in conservation of, 50–51, 56 inflation of, 157 intrinsic properties of, 160 nondimensional concept of Mayr, 158, 160 in philosophy of biology, 157, 158 as theoretical term, 157–158, 161 type specimen of, 159 Sponges, classification of, 221, 223, 227 Steel, M., 176 Stonedahl, G. M., 309 Stramenopiles, 220, 229, 230–231 Stratigraphic distribution of brachiopods, 203–208 monographic artifacts affecting, 197–215 of teleost fish, ghost lineages in, 256–259 Strophomenida, stratigraphic distribution of, 206 Symphyomyrtus, 270 Symplesiomorphy, 55 Synapomorphy, 23, 55, 154, 155, 180 Synthetic systematics, 22 System, differentiated from method, 182 Systematics classification in, 180 missions of, 77–78 New Systematics, 178, 181, 187 and ontogeny, 37–42

phylogenetic, 23–24, 28, 36, 48. See also Cladistics synthetic, 22 and taxonomy, 77. See also Taxonomy Systematics Agenda 2000, 78 Systematics and Biogeography (Nelson and Platnick), 182, 188 Systematics Association, 21, 24, 25, 181 Taxon journal, 24, 28, 29 Taxonomy descriptive, 69, 77–84 distinctness in, 52 index of, 51 and DNA barcoding, 69–70 equivalence or equal rank in, 52 in floral monographs, 80–82 funding of research on, 69, 77 hypotheses in, 67–68, 70, 79, 82 of homology, 83 importance of, 67–73, 77–84 missions of, 77–78 and name lists, 78–79, 81 numerical, 24, 169–170, 171, 176–181 and systematics, 77. See also Systematics Taylor, F. J. R., 225 Teleost fish, 243–264 ghost lineages of, 256–259, 260 morphological evolution of, 259–262, 263 taxic evolution of, 255–259 Teline stenopetala, 132 Terminal taxa, 51–52, 53 Tethys Ocean, 247, 248, 252 map of, 253 Texas, brachiopods in, 214–215 Thatcher, Margaret, 49, 56 Theoretical term compared to observation term, 157 species as, 157–158, 161 Thunberg, Carl Peter, 138 Tickell, Crispin, 49 Tokogenetic system, 152, 153, 154 Tolpis, 93, 103 Tradescant, John (elder), 130 Tradescant, John (younger), 130 Treatise on Invertebrate Paleontology (Williams), data on brachiopod distribution from, 197–215 automated extraction of, with XML-tagging, 199–201 standardization of, 201–203 Turner, Billie, 25 Type specimen of species, 159

330 / INDEX

University of Reading Compositae symposium of 1975 at, 25, 35 “Current concepts in Plant Taxonomy” presented at, 36 Humphries as research student at, 35 Upson, T., 82 Ursinia, 25 Vane-Wright, Richard I., 21, 28, 29, 36, 48, 49, 52, 58, 98, 111 Van Leeuwenhoek, Antony, 221 Van Welzen, P. C., 309 Vari, R. P., 315 Vicariance, 27–28, 117, 254–255 in Eucalyptus, 267–299 Vinctifer, 249 Viridiplantae, 228 Viruses, classification of, 223, 224 Visnea mocanera, 131, 132 Von Baer, K. E., 37 Von Buch, Christian Leopold, 140 Von Humboldt, Alexander, 127, 139–140 Von Siebold, C. T. E., 221 Wadiglossa, 200 Wagner, W. H., Jr., 22, 24 Wallace, Alfred Russel, 305, 307, 313, 316 Wallacea region, 305–317 instability of, 307 Wallace’s Line, 305, 306, 308, 309, 317n1 Wanntorp, Hans-Erik, 23, 24, 28

Weber’s Line, 306, 308, 309 Wheeler, Q. D., 154, 157 Whewell, William, 182–183 Whittaker, R. H., 53, 224 Will, K. W., 70 Williams, A., 199 Williams, D. M., 148 Williams, P. A. , 148, 149, 151, 152, 161, 162 Williams, Paul, 21, 49 Willi Hennig Society, 21, 24 Willmott, K., 159 Wills, M. A., 261 Winsor, Polly, 178–179 Wisdom, four cornerstones of, 60 Woltereck, R., 307 Woodger, J.. H., 148, 149, 150, 151, 152 Woodiness of island plants, 92, 97 as derived trait, 114, 115 in Macaronesian region, 101, 103, 113–116, 117 as primitive trait, 113 WORLDMAP, 111 World Wide Fund for Nature, 98 Wortley, A. H., 83 XML tagging of data on brachiopods, 199–201 Zaragüeta-Bagils, R., 251 “Zwischengebiet,” 307, 317n2

About the Editors

David Williams is a research diatomist at the Natural History Museum, London. His primary research interests are the taxonomy, systematics and biogeography of diatoms (Bacillariophyta) and the history, philosophy, and theory underlying systematics and biogeography. He has published over 150 papers, including three taxonomic monographs and five books. His most recent book is The Foundations of Systematics and Biogeography (with palaeontologist Malte Ebach) published in 2007. Sandra Knapp obtained her bachelor of arts degree in botany from Pomona College, in Claremont, California and her PhD in 1986 from Cornell University, Ithaca, New York. She is a specialist on the taxonomy of the nightshade family, Solanaceae, and has spent much time in the field in Central and South America collecting plants. She came to the Natural History Museum, London, in 1992 to manage the international project Flora Mesoamericana—a synoptic inventory of the approximately eighteen thousand species of plants of southern Mexico and the isthmus of Central America. She is also the author of several popular books on the history of science and botanical exploration, including the award-winning Potted Histories (2004). Her current projects include Flora Mesoamericana, a worldwide taxonomic monograph of the megadiverse genus Solanum (Solanaceae), collaborative research in phylogenetics and genomic evolution of Solanaceae, and the production of field guides for use in biodiversity monitoring in South and Central America.

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Species and Systematics

species: a history of the idea John S. Wilkins www.ucpress.edu/9780520260856 comparative biogeography: discovering and classifying biogeographical patterns of a dynamic earth Lynne R. Parenti and Malte C. Ebach www.ucpress.edu/9780520259454 beyond cladistics Edited by David M. Williams and Sandra Knapp www.ucpress.edu/9780520267725

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