Discovering Evolutionary Ecology Bringing together ecology and evolution Peter J. Mayhew University of York, UK 1 3 Great Clarendon Street, Oxford OX2 6DP Oxford University Press is a department of the University of Oxford. It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide in Oxford New York Auckland Cape Town Dar es Salaam Hong Kong Karachi Kuala Lumpur Madrid Melbourne Mexico City Nairobi New Delhi Shanghai Taipei Toronto With offices in Argentina Austria Brazil Chile Czech Republic France Greece Guatemala Hungary Italy Japan Poland Portugal Singapore South Korea Switzerland Thailand Turkey Ukraine Vietnam Oxford is a registered trade mark of Oxford University Press in the UK and in certain other countries Published in the United States by Oxford University Press Inc., New York © Oxford University Press 2006 The moral rights of the author have been asserted Database right Oxford University Press (maker) First published 2006 All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, without the prior permission in writing of Oxford University Press, or as expressly permitted by law, or under terms agreed with the appropriate reprographics rights organization. Enquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above You must not circulate this book in any other binding or cover and you must impose the same condition on any acquirer British Library Cataloguing in Publication Data Data available Library of Congress Cataloging in Publication Data Data available Typeset by Newgen Imaging Systems (P) Ltd., Chennai, India Printed in Great Britain on acid-free paper by Biddles Ltd., King’s Lynn ISBN 0–19–857060–0 978–0–19–857060–8 ISBN 0–19–852528–1 (Pbk.) 978–0–19–852528–8 (Pbk.) 10987654321 Preface There’s more to this life than just living. Frank Borman, Apollo 8 astronaut The natural world is a place I escape to: a place that goes about its business regardless of everyday individual human concerns. It is a place of beauty, change, diversity, and endless fa scination. Like many who share these senti- ments, I was never content to just be in nature: I had to watch, name, learn, and understand. This book is about understanding how and why the natural world works, thereby to appreciate it more for what it really is. For me,that is one of the things that make life ‘more than just living’. For naturalists, two fields of science feel especially comfortable: ecology and evolution.Ecology is traditionally a science of the great outdoors, dealing with the interactions between organisms and their environment (including other organisms).Evolution is traditionally a science of museum specimens, dealing with how lineages of organisms arise, change, and eventually go extinct. Both ecologists and evolutionary biologists share a common goal: they want to understand the diversity of life; how it arises, how it is main- tained, and why sometimes it is not. They should have a lot to say to each other. The field where ecologists and evolutionary biologists meet is called evolutionary ecology and, despite having 150-year-old roots, it has only recently matured into something that can fill books. This book has one overriding aim: to synthesize the field of evolutionary ecology; that is, to explain what the field as a whole has discovered, rather than just all the little bits. Along the way there is some detail; the work of scientists.While the detail can exist without the synthesis,the synthesis gives the detail added value.While some of the detail may change,be lost, or added to, the synthesis I hope will remain. I have written primarily for the students of biology whom I meet at undergraduate level. In 1998, as a new lecturer at the University of York, my colleague Richard Law invited me to take over his lectures on evolutionary ecology. However, I found no books that dealt with the field in the way I needed and decided to write my own. I have written the book that I would have wanted as a student: using a short,informal style, so some people might get to the end. As a result this is not a compendium of evolutionary ecology knowledge. There is always more detail in the world, or indeed in any scientific field, than any one person can assimilate. From what little detail we do have, however, we mortals must formulate pictures of the world that we can apply to novel situations, of which the world is full. I hope this book has just enough to do that. The book may also be more widely accessible than I originally meant it to be. I hope that postgraduates and other researchers in the field, who tend to stay within the bounds of a single chapter, will find it useful to have an overall view that places their work in a broader context.The public at large should also have a fighting chance, and I have tried to make that more likely by including a glossary of the more technical terms. Terms included in the glossary appear in bold on first mention. The precise content of the book was shaped by three secondary desires. First, I did not want to write yet another behavioural ecology book. But, because most evolutionary ecologists study behaviour, if I had devoted space in proportion to the amount of work carried out in the various subdisciplines of the field, that is pretty much what would have happened. However, a behavioural ecology book would not have achieved my broader aims. Instead, I have tried to cover a wide range of topics to do justice to the breadth of the field in ways that previous books have not.Each chapter serves merely as an introduction to each topic, about which others have written entire books. For those who feel like learning a bit more, I make a few recommendations for further reading at the end of each chapter. Some of the topics in the book are not normally considered to lie in evolutionary ecology, but more solidly in mainstream evolution or ecology. I have included them because I feel they should be here. Second, I am aware that most biologists express a greater enthusiasm for some organisms than others. They spend a lot of time trying to persuade each other that their study organisms are the most interesting. I believe that to appreciate evolutionary ecology to the full, you must be prepared to dis- card taxonomic and functional prejudice. This does not mean that you should not feel a special affection for some taxa; rather you should not feel disaffection for other taxa. The reader should be prepared for a good mix of the botanical, microbial and zoological, aquatic and terrestrial. To empha- size this even more I have occasionally employed positive discrimination in my choice of material. Third, I have not made a special effort to emphasize applied questions. Evolutionary ecology can help solve many problems that beset our planet and our species, but my desire here is to help people to love the subject, and not to plague them with worry or guilt. I have included applied questions simply where they provide a fascinating perspective that improves under- standing. As it turns out, there should be enough applied biology to keep enthusiasts happy. viii PREFACE PREFACE ix The chapters should preferably be read in sequence from start to finish since they build upon each other to provide the overall picture at the end. Because I still wanted this book to be scientific, factual statements are supported by citations from the primary scientific literature, though space and flow limited the extent to which I could do this. Space limitations also meant that I often had to reduce long complicated stories to a few salient points,leaving out alternative viewpoints. This makes it virtually certain that researchers in the field, and possibly other readers, will disagree with me at least once somewhere in the book. I hope that you all find such moments stimulating. Many people helped in the creation of this book. Biology students at York made comments on my teaching that shaped the way the book was written. Several people, mostly anonymously,reviewed the initial proposal, and I am grateful to all of them. I particularly thank Brian Husband, who convinced me that speciation mechanisms had to be included. I am grateful to the following persons for commenting on draft chapters: Peter Bennett, Calvin Dytham, Ian Hardy, Richard Law, Geoff Oxford, Ole Seehausen, Jeremy Searle, and Mark Williamson. Permission to reproduce photographs was generously provided by John Altringham, Craig Benkman, May Berenbaum, Didier Bouchon, Sarah Bush,David Conover,James Cook,Angela Douglas,Andrew Forbes, Richard Fortey, Niclas Fritzén, Leslie Gottlieb, Peter Grant, Angela Hodge, Greg Hurst,Mike Hutchings,Ian Hutton,Eric Imbert, Colleen Kelly, E.King,Hans Peter Koelewijn, Thomas Ledig, Mark Macnair, James Marden, Stephane Moniotte,Camille Parmesan,Olle Pelmyr,Thomas Ranius,Loren Rieseberg, Dolph Schluter, Ole Seehausen, Kim Steiner, Robert Vrijenhoek, Truman Young, Arthur Zangerl, and Gerd-Peter Zauke. I am grateful to the following for permission to reproduce various figures: The American Association for the Advancement of Science, The Royal Society of London, The Society for the Study of Evolution, and Springer Science and Business Media.Ian Sherman at Oxford University Press opened the door to what you are reading, gave valuable advice, displayed admirable patience, and was above all a friendly face. I am grateful to Alastair Fitter, for granting me the sabbatical term in which I made the majority of progress. I was also supported by my colleagues at York who bore the brunt of my ‘normal’ work while I was on sabbatical, particularly Calvin Dytham and Dale Taneyhill. Finally, thanks to my wife Emese and daughters Alice and Lara, the former for understanding my need to write the book and support- ing me in the struggle,and the latter for illustrating to me at first hand many of the interesting concepts mentioned in the book. Contents 1 Where two fields meet 1 2 Evolutionary cover-stories 13 3 Brave new worlds 25 4 Traits, invariants, and theories of everything 37 5 Sons, daughters, and distorters 51 6 Voyagers, residents, and sleepers 64 7 Doing adaptive things 75 8 Evolution and numbers 86 9 A world of specialists 97 10 The good, the bad, and the commensal 108 11 Evolving together 120 12 Birth of species 132 13 Death of species 145 14 Big evolution 158 15 Big ecology 170 16 Combining in diversity 180 REFERENCES 186 GLOSSARY 204 INDEX 209 1 Where two fields meet A teacher of mine once simplified his complex family history by saying that he, like all of us, originated from Olduvai Gorge in Tanzania (the ‘cradle of mankind’). Tropical Africa has been a cauldron of diversity not only for our own species. It is, to take one example, surprisingly fishy. The Great Lakes of East Africa (Figure 1.1), and surrounding rivers, contain a whopping 1500 species in just one fish family, the cichlids, familiar to freshwater aquarium enthusiasts. This makes cichlids the most species-rich family of vertebrates, beating such diverse and familiar groups as songbirds and mice. They are so diverse that many still await proper scientific description, and many more are doubtless completely undiscovered. Lakes Victoria and Malawi each con- tain about 500 species, and about 250 species are found in Lake Tanganyika. Diversity of this sort is what makes our planet such an interesting place, and of course, we have to find out what caused it. The cichlid species of the East African lakes have not each immigrated there from the surrounding habitat; they were born there, and in most cases they are endemics, being found in just one of the lakes (Fryer and Iles 1972). They are a ‘radiation’ of species. This radiation is all the more remarkable when the ages of the lakes are considered. Lake Tanganyika is the oldest (but has fewest species) at about 10 million years. Lake Malawi, the second oldest is a mere 1–2 million years old. Lake Victoria, amazingly, may have been completely dry around 14,500 years ago, the end of the last ice age. Since then, 500 cichlid species have been born. If species arose in a clockwork linear fashion, that would mean one new species of fish every 29 years! The varied lifestyles of the fish are equally impressive. In Lake Victoria, for example, have been found cichlids with the following diets: adult fish, fish larvae, fish scales, fish parasites, freshwater snails, insect and other invertebrate larvae, plant and animal plankton, algae growing on rocks, and vascular plants, all with specialized jaws to match (Figure 1.2). The most impressive radiations have occurred among the ‘haplochromine’ cichlids living on rocky shores in Lakes Victoria and Malawi (Kocher 2004). Clearly, we need to know how so many species could have formed in such a short time span, why it happened here, why cichlids, and why haplochromines most of all? At stake is our understanding of species richness itself. 1.1 Alternative mechanisms First, let us think briefly about how species are supposed to form. The standard dogma is that this happens through geographic separation and subsequent differentiation. One lineage splits into two distinct ones because a spatial separation occurs, either through a dispersal event to an isolated 2 DISCOVERING EVOLUTIONARY ECOLOGY Fig. 1.1 Seen from space, the Great Lakes of the East African Rift Valley are major landscape features. The two largest ones here are Lake Victoria (right) and Lake Tanganyika (bottom)—Lake Malawi is off the bottom of the picture. Lake Victoria is about 300 km across and its northern tip is on the equator. Photo from the NASA Visible Earth image archive. Black lines indicate national boundaries. new region, or through fragmentation of an existing one (vicariance). The lineages evolve in isolation,through natural selection or other processes,and eventually become distinct enough to be called new species. The differences between related, but geographically isolated species are what gave Darwin and Wallace many clues to their theory of evolution. Could such processes be at work in the fastest vertebrate radiation? Geographic separation and natural selection have undoubtedly contributed, and a number of observations on geographic distribution and morpholo- gical divergence among species are consistent with the process.For example, closely related sister species in Lake Victoria sometimes have widely sep- arated geographic ranges (Seehausen and van Alphen 1999); and different populations of the same species have distinct jaw morphologies that match local diets, suggesting local adaptation (Bouton et al. 1999). But there remains a dearth of special explanation: why here and why haplochromines? A growing weight of evidence suggests a role for additional mechanisms and in particular in haplochromines. WHERE TWO FIELDS MEET 3 Fig. 1.2 The diversity of jaw morphology of Lake Victoria cichlids. Clockwise from top left they eat, snails, fish, fish larvae, algae on rocks, invertebrates on rocks, insect larvae. What additional mechanisms might be important? Can speciation, for example, occur without geographic isolation? There are two problems that need to be overcome. First, there has to be ecological divergence: the two incipient species have to occupy different niches to prevent them from competing and allow stable coexistence.Second,there has to be reproductive divergence, so that interbreeding does not occur. Getting these events to occur without geographic isolation is a conceptual challenge that has long occupied evolutionary biologists. In the 1990s, this question was bothering cichlid enthusiast, Ole Seehausen. Ole’s hunch was that species could diverge in situ into reproductively isolated populations by assortative mating based on male coloration. Over time, mate selection by different females for different coloured males would produce two reproductively isolated species living in the same ecological niche but differing in male coloration.Once sep- arated like this,the way would be open for natural selection to allow niche dif- ferentiation. The process could then repeat itself. The power of this mechanism is its potential speed. Initial ecological differentiation need only be small, and the constant disruptive power of female choice would drive populations rapidly apart.It was a process that seemed capable of giving rise to a multitude of species in a very short time. What evidence supported this hypothesis? One source is patterns of geographic overlap between species. If speciation has occurred in the absence of geographic separation, there should also be groups of closely related species that overlap in range a lot. In fact, there are many such cases in Lake Victoria (Seehausen and van Alphen 1999). What about sexual selection? In the field, sympatric sister species tended to be opposite colours more commonly than allopatric pairs of species. This is consistent with the origination of new species via selection on coloration in situ. These patterns have also recently been demonstrated in Lake Malawi cichlids (Allender et al. 2003). In the laboratory, females from red species behaved preferentially towards red males, as did females of blue species towards blue males. When exposed to monochromatic light that hid the males’ bright nuptial hues, females would no longer show a mate preference (Seehausen and van Alphen 1998). This was indeed assortative mating based on colour. But why should female mate choice be disruptive? One possible answer is percep- tual bias: the colour-sensitive cone cells of haplochromines are particularly sensitive to red and blue parts of the spectrum, and these different sensi- tivities could lead females to perceive red or blue males preferentially (Seehausen et al. 1997). However, other possible mechanisms could be at work. What ever the mechanism, female haplochromines agree with Winston Churchill when he said: ‘I cannot pretend to feel impartial about colours. I rejoice with the brilliant ones and am genuinely sorry for the poor browns’. 4 DISCOVERING EVOLUTIONARY ECOLOGY [...]... ecology and evolution interact and how do they do so? A basic answer, and one that does not require much in-depth study, is that both fields are concerned with understanding similar characteristics For 10 DISCOVERING EVOLUTIONARY ECOLOGY example, both evolutionary biologists and ecologists would consider species richness as one of the key variables they want to understand Both too would want to understand... taught us? 1.3 Cichlids and evolutionary ecology The cichlid story illustrates many of the broader features of evolutionary ecology, the science that involves both ecological and evolutionary knowledge Evolutionary biology is the field concerned with understanding how biological lineages change through time (anagenesis), split (cladogenesis), and ultimately go extinct Ecology is concerned with the interaction... only one of WHERE TWO FIELDS MEET 11 Ecology Evolution Individuals Populations Anagenesis Communities Cladogenesis Ecosystems Fig 1.6 The interaction of ecology and evolution the parts of evolutionary ecology Hence evolution by natural selection affects ecology at the level of the individual The traits that evolve within species are often relevant to population and community processes For example,... understand the other The second major evolutionary process, cladogenesis is also important for an understanding of ecology To produce species-rich communities, such as in East African lakes, species have to be formed and not go extinct Both evolution within lineages and the origin and death of lineages are processes that might have contributed Thus evolution influences every level of the field of ecology. .. field addresses are mutually supportive, such that understanding of one aids understanding of others For example, we can understand the rates of speciation in cichlids from a knowledge of speciation and extinction mechanisms, and we can understand those from a knowledge of sexual selection and sex determination Ultimately 12 DISCOVERING EVOLUTIONARY ECOLOGY then, workers in one area will benefit from an... ecology and maybe key to understanding some of the basic ecological properties of our planet In the following chapters, we will explore the ways in which the two fields of ecology and evolution interact, see what we have learnt about the world as a result, and along the way build up a picture of how exactly these interactions occur However, the book will describe something else about evolutionary ecology. .. cichlids, that influence their mating success So ecology, through the medium of selection, causes anagenesis, evolution within lineages Ecology can also influence cladogenesis, the other big evolutionary process We saw this in the role that water clarity plays in speeding up or slowing down rates of cichlid speciation and extinction Evolution can also affect ecology, and this interaction occurs at several levels... coral reefs, kelp forests, and seagrass beds The open ocean is a comparative desert, but consists of pelagic phytoplankton, zooplankton, and macroscopic predators A benthic fauna consists of filter feeders, scavengers, and predators The biosphere’s energy comes, almost exclusively, from light captured by plants, and its carbon source is atmospheric 26 DISCOVERING EVOLUTIONARY ECOLOGY Ma 0 CENOZOIC MESOZOIC... transitions in ecology resulting from evolutionary novelty, and when they occurred carbon dioxide, which is eventually returned by (high energy-yielding) aerobic respiration Where, then, did all this come from and what evolutionary novelties helped it get there? Below I tentatively identify eleven major changes that take us from the origin of life to an ecologically modern planet (Figure 3.1) 3.1 Evolution. .. detectable and non-trivial (Farrell 1998) We have now arrived at an essentially modern ecology How and why did these changes occur and why have they been retained? Let’s look at an example, the evolution of flight in birds, insects, bats, and pterosaurs 3.2 The evolution of animal flight: understanding a major transition in ecology There is now little doubt among most biologists that birds derive from a . Discovering Evolutionary Ecology Bringing together ecology and evolution Peter J. Mayhew University of York,. but only one of 10 DISCOVERING EVOLUTIONARY ECOLOGY the parts of evolutionary ecology. Hence evolution by natural selection affects ecology at the level