40 Years of Evolution: Darwin's Finches on Daphne Major Island

40 Years of Evolution

40 Years of Evolution

Peter R. Grant and B. Rosemary Grant

Princeton University Press

Princeton and Oxford

Copyright © 2014 by Princeton University Press

Published by Princeton University Press, 41 William Street, Princeton, New Jersey 08540

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Library of Congress Cataloging-in-Publication Data

Grant, Peter R., 1936–

Forty years of evolution : Darwin’s Finches on Daphne Major Island / Peter R. Grant and B. Rosemary Grant.

pages cm

Includes bibliographical references and index.

ISBN 978-0-691-16046-7 (hardback : alk. paper) 1. Ground finches—Evolution—Galapagos Islands. 2. Bird populations—Galapagos Islands. 3. Birds—Evolution—Galapagos Islands. I. Grant, B.

Rosemary. II. Title.

QL696.P246G7324 2014

598.072′32098665—dc23

2013018007

British Library Cataloging-in-Publication Data is available

This book has been composed in ITC Caslon 224

Printed on acid-free paper. ∞

Printed in the United States of America

2 4 6 8 10 9 7 5 3 1

To the next generation: Nicola and Thalia

And the next one: Rajul, Olivia, Anjali, and Devon

And succeeding ones

Daphne Major

She looms from the hyaline like some mutant barnacle—frond once a pillar of smoke, operculum blown off—that has assumed a couchant pose, waiting for the searchers with mist-nets and calipers to return each year who pit the caltrop against magnirostris and scratch protean generations from her flank, until she blows again or sounds and sinks back to Gondwanaland’s deep ocean drift

(Weston 2005, p. 49)

The sight of Daphne Major conveys something like this [passage of time] to us, even in the first glance over the water, or in the last, as it revolves like a wood chip in the wake of the boat. We know we are looking at a place that was here before we came and will remain when we are gone. The very island will sink someday, and another will rise when it is drowned.

(Weiner 1994, p. 303)

Contents

Illustrations

Tables

Boxes

Preface

DARWIN’S ORIGIN OF SPECIES (1859, p. 1) begins: When on board H.M.S. ‘Beagle,’ as naturalist, I was much struck with certain facts in the distribution of the inhabitants of South America, and the geological relations of the present to the past inhabitants of that continent. These facts seemed to me to throw some light on the origin of species—that mystery of mysteries, as it has been called by one of our greatest philosophers. We followed in his footsteps 138 years after his visit to the Galápagos, with the same quest in mind. Our book describes what we learned by studying Darwin’s finches (fig. P.1) for 40 years on Daphne Major (fig. P.2), a small island in the center of the Galápagos archipelago (fig. P.3).

Genetic variation is the raw material for evolution. Although much has been learned about genetic variation from theoretical and laboratory research, long-term field studies in natural environment have been relatively neglected. Knowledge of how genetic and phenotypic variation interacts with environmental variation is fundamentally important for understanding evolution in nature. It can be achieved by long-term field studies of evolution with well-chosen organisms in well-chosen environments when coupled with the benefits of laboratory science. This is what we have attempted to do. By taking a multidimensional approach to questions of evolution and speciation, carefully documenting genetic, ecological, and behavioral factors responsible for evolution of finches across 40 years, we have made discoveries about speciation far beyond our initial expectations. And although finches are the focal organisms of the study, the principles of their evolution apply broadly to all organisms.

These are exciting times to be an evolutionary biologist. Changes in technology are proceeding at an ever-increasing pace, giving us the tools for expanding our knowledge and understanding of how evolution occurs in the natural world. In view of this it is worth reflecting on the state of knowledge in 1973 (Mayr 1970, Dobzhansky 1970), on the methods and tools available for evolutionary investigations at that time, and the transformation that studies of speciation have undergone since then. Techniques we take for granted now did not exist. Electrophoresis (Hubby and Lewontin 1966) was only just becoming widely available as a method of detecting allozyme variation if the appropriate buffers could be worked out. It required a power source, which ruled it out for most studies on uninhabited islands. Cladistics (Hennig 1966) had yet to shake the foundations of phylogenetic reconstruction and interpretation. Personal computers had yet to be invented; we were the handmaidens of university mainframes. Statistical programs for the analysis of complex data had not been invented either, and the revolution in molecular biology, including evodevo, lay far off in the future. Whole genomes were conceivable, but their sequences were not. Now we do things we could not anticipate doing at the outset; for example, we study genes, their expression patterns and regulation, and we infer from molecular data the time when events took place in the past. Our account of evolution on Daphne reflects the expanding knowledge brought about by the development of new methods as the study progressed.

Fig. P.1 The four species of finches. Upper left: Small Ground Finch, G. fuliginosa. Upper right: Medium Ground Finch, G. fortis. Lower left: Large Ground Finch, G. magnirostris. Lower right: Cactus Finch, G. scandens. From Grant and Grant 2008a).

Fig. P.2 The two Daphnes. Left: Daphne Major, with Daphne Minor (Chica) in the background (D. Parer and E. Parer-Cook). Right: Daphne Minor, 1976. Daphne Minor has been climbed once, with ropes. Two immature fortis banded on Daphne Major were seen at the top (Grant et al. 1980).

Fig. P.3 Map of Galápagos. From Grant and Grant 2008a.

Fig. P.4 Phenotypic variation in the G. fortis population on Daphne.

In the absence of fossils, answers to questions about speciation in the past have to be sought with living organisms by looking backward in time. Typically this is done by using information on contemporary populations to test the assumptions of historical hypotheses: a retrospective analysis. We followed this path with a combination of field studies of short duration on many islands and a decade-long study on Genovesa. We concentrated almost entirely on the six ground finch species in the genus Geospiza because they are distributed widely in the archipelago, generally abundant, and easy to observe (Lack 1947). We wrote three books on our findings: two on the total finch radiation (Grant 1986 [1999], Grant and Grant 2008a) and one on the finch populations on Genovesa (Grant and Grant 1989a).

Here we describe what we have found by adopting a different approach to questions of speciation: studying populations through time, a prospective analysis. This provides insights into the process of speciation even if the progress we observe toward complete reproductive isolation is small. The present volume completes our program of converting research results into more accessible and synthetic book form, with new and unanticipated insights into Darwin’s question on the origin of species.

Fig. P.5 Phenotypic variation in the G. scandens population on Daphne.

We have designed this book for students, educators, and others to read for enjoyment and inspiration. Throughout we have tried to express our views in jargon-free language, with technical terms given only where necessary. We have adopted a few conventions. First, we have given numerical results of statistical tests only when not given before in the original papers we cite. Second, we have supplied details of methods of study and analysis in boxes and not in the main text. Third, we have used appendixes for some background information and discussion of topics that are relevant to the material in chapters but not central to it. In some cases these discussions have been supplemented with numbers in tables and figures.

Acknowledgements. Our research has been supported financially by the National Science and Engineering Research Council (Canada), National Science Foundation (USA), and McGill and Princeton Universities (Class of 1877 Fund), and logistically by the Charles Darwin Foundation and the Galápagos National Parks Service. More than twenty assistants helped us in fieldwork. Foremost among them were Ian and Lynette Abbott as postdoctoral fellows, and Peter Boag, Laurene Ratcliffe, Trevor Price, and Lisle Gibbs as PhD graduate students. They and we were helped by Phillip de Maynadier, James Gibbs, Lukas Keller, Greg Keys, Steve Latta, Irby Lovette, David McCullough, Stephen Millington, David Moore, Ken Petit, Ken Petren, Bob Podolsky, Wally Rendell, Gerry Retzlaf, Uli Reyer, Dan Rosenberg, Keith Tarvin, Ayse Unal, Carlos Valle, Jonathan Weiland, David Wiggins, and our two daughters, Nicola and Thalia. We thank Lisle Gibbs for reading chapter 7, and Trevor Price, Dolph Schluter, and an anonymous reviewer for reading previous drafts and offering numerous suggestions for improvement. They helped us write a significantly better book. For transforming the potential into the realized book we thank the editorial staff at Princeton University Press: Alison Kalett and Quinn Fusting for guidance in the early stages, Mark Bellis for shepherding it through production, and Dimitri Karetnikov for giving us the benefit of his artistic skills.

Data used in constructing the figures have been deposited in Dryad (doi:10.5061/dryad.g6g3h). Two educational films illustrate features of the book. One, made by the Howard Hughes Medical Institute for high schools, illustrates natural selection on Daphne. It is entitled The Origin of Species: The Beak of the Finch (www.biointeractive.org). We are preparing another that is designed to illustrate all the main topics of the book.

February 2013

PART 1

Early Problems, Early Solutions

1

Speciation, Adaptive Radiation, and Evolution

I should like to take some one family to study thoroughly, principally with a view to the theory of the origin of species. By that means I am strongly of opinion that some definite results might be arrived at.

(Wallace 1847, letter to H. W. Bates)

Those forms which possess in some considerable degree the character of species, but which are so closely similar to some other forms, or are so closely linked to them by intermediate gradations, that naturalists do not like to rank them as distinct species, are in several respects the most important to us.

(Darwin 1859, p. 47)

Introduction

MANY OF US ARE FASCINATED by the biological world around us. We marvel at the diversity of color, pattern, form, shape, size, ferocity, tameness, speed, and ingenious things that animals and plants do to find food and mates and avoid being eaten. Some of us have peered into microscopes that have opened up a new and wonderfully diverse world. Others have had the same thrilling experience in diving off coral reefs and being dazzled by the variety of fish. Yet others have been simultaneously bewildered and stimulated by the overwhelming diversity of a tropical rain forest. All this is so enthralling that some of us not only want to know why the world is the way it is; we also want to explore, examine, and test ideas about it in order to make our own discoveries. We are evolutionary biologists.

As evolutionary biologists we ask, how do species form? If we can answer that question we have taken a large stride toward understanding the biological richness of the world. The question is old but remains unresolved because rarely is it possible to witness even a part of the process. It must generally be inferred from indirect evidence, and yet we have had the good fortune to be witnesses. In this book we describe what we have learned about speciation by tracking populations and measuring evolutionary changes across 40 years in contemporary time.

Our starting point is Darwin’s Origin of Species by Means of Natural Selection. This is a manifesto of cardinal evolutionary principles. It laid out a theory of common descent of all organisms, represented evolutionary diversification as a branching pattern, and invoked the principle of natural selection as the driving agency that caused the divergence. Darwin argued that species formed by diverging in separate locations and then, when they came together, competed with each other for food and space, and diverged yet further. By this means, repeated, complex communities built up from simpler ones. Darwin had little hope of seeing evolution occur, but he did write that young radiations of species might provide windows through which we could view the steps involved in speciation. By an indirect pathway this led us to the Galápagos Islands, to Daphne Major in particular, to the finches named after him, to a fascination with them that lasted 40 years, and even to the origin of a new species.

Adaptive Radiation of Darwin’s Finches

Finches on the Galápagos are a young radiation of ecologically diverse species that have evolved from a common ancestor (Lack 1947, Grant 1986). Other radiations of plants and animals are more spectacular in terms of both numbers of species and their diversity (e.g., Schluter 2000, Grant 2013), yet Darwin’s finches have several advantages for the study of biological diversity (box 1.1). Many populations live in pristine environments, no species has become extinct as a result of human activities, and evolution can be studied as a contemporary process.

Box 1.1. The Choice of Darwin’s Finches

When we began our Galápagos research, the best-known radiations of animals were the numerous species of cichlid fish in several of the African Great Lakes (Fryer and Iles 1972), Anolis lizards of the Caribbean (Williams 1972), Drosophila (Carson et al. 1967) and honeycreepers (Amadon 1950, Warner 1968) of Hawaii, and Darwin’s finches (Lack 1945, 1947). The major features of morphological diversity were understood as feeding adaptations caused by natural selection in spatially segregated populations, and color and pattern variation as a result of sexual selection. Deepening this understanding required two things: a better estimation of phylogenies, which only became possible much later with the development of molecular genetic markers (Wagner and Funk 1996, Givnish and Sytsma 1997), and an analysis of contemporary populations to investigate the genetic basis and ecological causes of evolutionary change. This is where Darwin’s finches had some advantages over the others. The subject was ripe for ecological analysis, and finches seemed suitable subjects because they could provide the missing focus on population biology.

Detailed population studies appeared to be feasible because some populations are small, the finches can be marked for individual recognition, and they are conspicuous and approachable, so their fates can be determined accurately. Ecological influences on their fates can be identified because the climate fluctuates strongly and the extremes are markedly different. In some years there is little or no rain (La Niña); in others there is an abundance of rain (El Niño). The change from one extreme to the other is caused by reversals in the gradient of atmospheric pressure and sea-surface temperature across the Pacific basin. It is known as the El Niño–Southern Oscillation or ENSO phenomenon. The climatic extremes occur somewhat predictably at approximately three-to seven-year intervals on average (Philander 1990, Chen et al. 2004), with multidecadal oscillations in amplitude (Schlesinger and Ramankutty 1994). Superimposed upon a normal annual cycle of hot-wet (January to April) and cool-dry (May to December) seasons, the interannual fluctuations create profound changes in both marine and terrestrial productivity. As we discovered, the swings from plenty to scarcity reveal the ecological forces that finches are subjected to, and the evolutionary consequences. These in turn help us to interpret the radiation because it is still in a natural state: no species is known to have become extinct through human agency, and several of the islands have scarcely or never been affected by human occupation or exploitation.

Once thought to be members of the passerine family Emberizidae (buntings and finches), Darwin’s finches are now classified as tanagers (Thraupinae) (Burns 1997). This Neotropical family comprises about 400 species (Isler and Isler 1999) that evolved in the last 12 million years (Cracraft and Barker 2009). The drab-colored Darwin’s finches are thus a small part of a much larger radiation of varied and often colorful birds. According to current understanding at least 13 species of finches evolved on the Galápagos in the last two to three million years, and another evolved on Cocos Island (Grant and Grant 2008a). The species are distinctive in morphology (box 1.2), especially in the size and shape of their beaks, as well as in their diets. How is all the variation to be explained?

Box 1.2. What Makes a Darwin’s Finch Species?

Lack (1945), following Swarth (1931) and earlier taxonomists, classified species by their size, proportions, and to a lesser extent plumage. For example, four species of ground finches can be recognized morphologically by their differences on any one island and the consistency of the differences across islands. The Small Ground Finch (fuliginosa), Medium Ground Finch (fortis), and Large Ground Finch (magnirostris) differ principally in average size (fig. B.1.2, appendix 1.2, fig. P.1). As size increases from one species to the next, beak size becomes both larger and more blunt. We refer to them as the granivore group because they all feed extensively on seeds. The fourth species, the Cactus Ground Finch (scandens), is about the size of the Medium Ground Finch but has a proportionately longer and narrower beak than any of the other three. As the name implies, it is a cactus (Opuntia) specialist. In other respects the species are identical. As young birds they are brown and streaked. With successive molts the males, but not females, acquire partly black then completely black plumage (Salvin 1876, Grant 1986). The remaining 10 species of Darwin’s finches, similarly recognized by morphology, have minor relevance to this book (they are briefly described in appendix 1.3). Lack confirmed the biological reality of species identified by morphology in the breeding season of 1938–39 on San Cristóbal and Santa Cruz islands. Without having the benefit of measurements of individuals, he observed members of each morphological group (aka species) pairing up and breeding with each other and not with members of another group. Later in the book (chapter 9) we discuss the additional relevance of song to the question of what constitutes a species.

Fig. B.1.2 Morphological variation among four species of Darwin’s ground finches (males) on several islands. Data are taken from Grant et al. 1985.

Lack (1945, 1947) made the first attempt to answer this question after studying Darwin’s finches in the field. His explanation laid stress on three factors; natural selection, diversification on separate islands, and competition between species for food. Truly Darwinian! According to the Darwinian view, splitting of a species on Galápagos is initiated allopatrically when individuals disperse from one island to another and establish a new population. This is easy to visualize (fig. 1.1) because the archipelago has many islands. Colonists encounter new conditions, many die, and those surviving pass on to their offspring the heritable characteristics that contributed to their survival. In this way the population evolves by natural selection and becomes adapted to the new environment. There may be additional elements of randomness in how they evolve, if, for example, the founders are few in number or are not a representative sample