Evolutionary Pathways in Nature

A Phylogenetic Approach

Reconstructing phylogenetic trees from DNA sequences has become a popular exercise in many branches of biology, and here the award-winning geneticist John Avise explains why. Molecular phylogenies provide a genealogical backdrop for interpreting the evolutionary histories of many other types of biological traits (anatomical, behavioral, ecological, physiological, biochemical, and even geographical). Guiding readers on a natural history tour along dozens of evolutionary pathways, the author describes how creatures ranging from microbes to elephants came to possess their current phenotypes. If you want to know how the toucan got its bill and the kangaroo its hop, then this is the book for you. This book also provides a definitive answer to the proverbial question: `which came first, the chicken or the egg?' This scientifically educational yet entertaining treatment of ecology, genetics and evolution is intended for college students, professional biologists, and anyone interested in natural history and biodiversity.

John C. Avise is a distinguished professor of Ecology and Evolutionary Biology at the University of California, Irvine.

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Evolutionary Pathways in Nature

A Phylogenetic Approach

JOHN C. AVISE
Department of Ecology and Evolutionary Biology
University of California

Illustrations by Trudy Nicholson

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CAMBRIDGE UNIVERSITY PRESS
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Cambridge University Press
The Edinburgh Building, Cambridge CB2 2RU, UK

Published in the United States of America by Cambridge University Press, New York

www.cambridge.org
Information on this title: www.cambridge.org/9780521857536

© John C. Avise 2006

This publication is in copyright. Subject to statutory exception
and to the provisions of relevant collective licensing agreements,
no reproduction of any part may take place without
the written permission of Cambridge University Press.

First published 2006

Printed in the United Kingdom at the University Press, Cambridge

A catalog record for this publication is available from the British Library

ISBN-13 978-0-521-85753-6 hardback
ISBN-10 0-521-85753-8 hardback
ISBN-13 978-0-521-67417-1 paperback
ISBN-10 0-521-67417-4 paperback

Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate.

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CONTENTS

		Preface	page ix
		Acknowledgments	xi
1		Introduction	1
		The meaning of phylogeny	1
		Phylogenetic metaphors	3
		Molecular appraisals of phylogeny	8
		Comparative phylogenetics	11
		Phylogenetic character mapping	15
2		Anatomical structures and morphologies	19
		Whence the toucan’s bill?	19
		The beak of the fish	22
		Snails’ shell shapes	25
		More on snails’ shell shapes	28
		Winged walkingsticks	30
		Hermits and kings	34
		True and false gharials	36
		Loss of limbs on the reptile tree	39
		Fishy origins of tetrapods	42
		Panda ponderings	44
		Fossil DNA and extinct eagles	47
		The Yeti’s abominable phylogeny	48
3		Body colorations	52
		Light and dark mice	52
		Sexual dichromatism	54
		Dabbling into duck plumages	58
		Specific avian color motifs	62
		The poisonous Pitohui	65
		Warning colorations in poison frogs	68
		Müllerian mimicry butterflies	71
		Caterpillar colors and cryptic species	73
4		Sexual features and reproductive lifestyles	77
		The chicken or the egg?	77
		The avian nest	80
		Egg dumping and foster parentage	84
		Egg laying and live bearing	87
		Piscine placentas	90
		Male pregnancy	93
		Living and reproducing by the sword	95
		Brood care in Jamaican land crabs	98
		Social parasitism of butterflies on ants	101
		Of monkeyflowers and hummingbirds	104
		Parthenogenetic lizards, geckos, and snakes	107
		Delayed implantation	110
5		More behaviors and ecologies	114
		The kangaroo’s bipedal hop	114
		Powered flight in winged mammals	118
		Magnetotaxis in bacteria	121
		Cetacean origins	122
		Feeding and echolocation in whales	124
		The phylogeny of thrush migration	129
		Pufferfish inflation	131
		Eusociality in shrimp	134
		Evolutionary reversals of salamander lifecycles	137
		Dichotomous life histories of marine larvae	140
		Adaptive radiations in island lizards	143
		Spiders’ web-building behaviors	145
		Lichen lifestyles	150
6		Cellular, physiological, and genetic traits	153
		Foregut fermentation	153
		Snake venoms	156
		Antifreeze proteins in anti-tropical fish	159
		Warm-bloodedness in fishes	162
		Electrical currents	166
		The Xs and Ys of sex determination	168
		The eyes have it	170
		Two types of body	174
		The phylogenomics of DNA repair	178
		Roving nucleic acids	180
		Host-to-parasite gene transfer	184
		Tracking the AIDS virus	187
7		Geographical distributions	190
		Afrotheria theory	190
		Aussie songbirds	193
		Madagascar’s chameleons	196
		The evolutionary cradle of humanity	200
		Coral conservation	204
		Sri Lanka, a cryptic biodiversity hotspot	207
		Overseas plant dispersal	210
		Phylogenetic bearings on Polar Bears	212
		Looking over overlooked elephants	215
		Bergmann’s rule	218
		Epilog	221
		Appendix: a primer on phylogenetic character mapping	223
		History of cladistic concepts and terminology	223
		Maximum parsimony	228
		Maximum likelihood	231
		Independent contrasts between pairs of quantitative traits	233
		Glossary	239
		References and further reading	253
		Index	279

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PREFACE

Many biologists now incorporate molecular phylogenetic analyses into their explorations of nature. Using sophisticated laboratory techniques, they uncover “DNA markers” or “genetic tags” that uniquely identify each creature. Furthermore, details in the submicroscopic structures of these natural labels offer tantalizing clues to how living organisms were genealogically linked through bygone ancestors. Thus, lengthy DNA sequences housed in the cells of all organisms carry not only the necessary molecular genetic instructions for life, but also extensive records of phylogeny, i.e. of evolutionary ancestry and descent.

   During the replication and transmission of DNA from one generation to the next, mutations continually arise. Many of these spread through populations (via natural selection, or sometimes by chance genetic drift), thereby cumulatively altering particular molecular passages in each species’ hereditary script. In recent years, scientists have learned how to read and interpret the genealogical content of these evolutionary diaries – these “genomic autobiographies” – of nature. Results are summarized as phylogenetic diagrams that depict how particular forms of extant life are connected to one another via various historical branches in the Tree of Life.

   Phylogenetic analysis has become a wildly popular exercise in many areas of biology, but phylogenies estimated from DNA sequences are seldom the ultimate objects of scientific interest. The primary value of each molecular phylogeny lies instead in its utility as historical backdrop for deciphering the evolutionary histories of other kinds of biological traits such as morphologies, physiologies, behaviors, lifestyles, or geographical distributions. By mapping such organismal features onto species’ phylogenies estimated from molecular data, biologists can address fascinating questions of the following sort. Did the bipedal hop arise once or multiple times in kangaroo evolution? From what type of ancestor did toucan birds evolve their banana-like bills? How often during evolution have reptiles lost their limbs? Are the antifreeze proteins in Arctic and Antarctic fishes functionally similar by virtue of shared ancestry or convergent evolution? By what evolutionary routes have some fishes evolved powerful electrical discharges? Did Jamaican land crabs derive their peculiar forms of offspring care from a common ancestor? Did walkingstick insects evolve from flyingsticks or vice versa, and how often? How have certain bacteria acquired their magnetic compasses? On how many occasions have distinct algal and fungal lineages joined forces in lichen symbioses? Where on the planet have phylogenetic appraisals uncovered cryptic species and conservation-relevant hotspots of global biodiversity? Can the ancient breakup of the supercontinent Gondwanaland account for the modern distributions of particular lineages of birds and mammals in the Southern Hemisphere? Where and when did the viruses responsible for the AIDS epidemic enter the human species? And, which came first: the chicken or the egg?

   By highlighting studies that have provided scientific answers to these and many additional questions, I intend to illustrate the power (and also some limitations) of comparative phylogenetic perspectives in biological research. Several available textbooks describe, in depth, how molecular data are gathered in the laboratory and analyzed at the computer. My approach here will not be to recount the many operational details of molecular phylogenetics (although introductory background is provided). Rather, my intent is to serve as a naturalist guide on a biological expedition into the remarkable world of nature, as viewed through the evolutionary prism of molecular phylogeny. In each of 67 essays arranged into six topical chapters, I describe how a DNA-estimated phylogeny provided historical framework for interpreting a puzzling ecological feature or evolutionary process in organisms with unusual anatomies or lifestyles, or in creatures with special significance to one or another biological field such as ethology, natural history, biogeography, conservation, biochemistry, physiology, epidemiology, or medicine.

   Through this case-history approach, I hope to provide a fun yet educational introduction – for amateur naturalists and students to professional biologists – to how comparative phylogenetic analyses have helped to solve some of nature’s most intriguing mysteries. Another goal is to encourage a deeper appreciation of the many intellectual and aesthetic treasures of the biological world. As more and more people become educated about nature’s ways, perhaps societies will learn to cherish life’s variety and strive harder to preserve what remains. Tragically, through human actions, populations and species today are being driven to extinction at rates seldom experienced in the planet’s long history. To terminate any lineage now is to lose forever a genetic wisdom that was honed along an epic evolutionary journey lasting nearly four billion years. Paradoxically, life is both fragile and tenacious. Extinction continually threatens, and once realized can never be undone. However, having withstood and adapted to countless environmental challenges over the geological eons, each extant lineage is also a hardy and proven survivor, surely deserving of our deepest respect and admiration.

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ACKNOWLEDGMENTS

Doug Futuyma, Blair Hedges, David Hillis, Kirk Jensen, Judith Mank, Axel Meyer, David Reznick, DeEtte Walker, John Ware, and several anonymous reviewers provided helpful comments on various portions of the text. I am especially grateful to Trudy Nicholson for producing the beautiful plant and animal drawings that grace this book.