The nature of diversity an evolutionary voyage of discovery

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The Nature of Diversity

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The Nature of Diversity
An Evolutionary Voyage of Discovery

Daniel R. Brooks
Deborah A. McLennan

The University of Chicago Press
Chicago and London


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D A N I E L R . B R O O K S is professor in the Department of Zoology at the
University of Toronto. He is coauthor, with E. O. Wiley, of Evolution
as Entropy: Toward a Unified Theory of Biology, and, with Deborah A.
McLennan, of Phylogeny, Ecology, and Behavior: A Research Program in
Comparative Biology and Parascript: Parasites and the Language of Evolution.
D E B O R A H A . M C L E N N A N is associate professor in the Department of

Zoology at the University of Toronto. She is coauthor, with Daniel R.
Brooks, of Phylogeny, Ecology, and Behavior: A Research Program in
Comparative Biology and Parascript: Parasites and the Language of Evolution.
The University of Chicago Press, Chicago 60637
The University of Chicago Press, Ltd., London
᭧ 2002 by The University of Chicago
All rights reserved. Published 2002
Printed in the United States of America
11 10 09 08 07 06 05 04 03 02
1 2 3 4 5
ISBN: 0-226-07589-3 (cloth)
ISBN: 0-226-07590-7 (paper)
Library of Congress Cataloging-in-Publication-Data
Brooks, D. R. (Daniel R.), 1951–
The nature of diversity : an evolutionary voyage of discovery /
Daniel R. Brooks, Deborah A. McLennan.
p. cm.
Includes bibliographical references and index.
ISBN 0-226-07589-3 (cloth : alk. paper)—ISBN 0-226-07590-7
(pbk. : alk. paper)
1. Biological diversity. 2. Phylogeny. 3. Adaptation (Biology)
I. McLennan, Deborah A. II. Title.
QH541.15.B56 B76 2002
576.8Ј8—dc21
2001053860
The paper used in this publication meets the minimum requirements of
the American National Standard for Information Sciences—Permanence of
Paper for Printed Library Materials, ANSI Z39.48-1992.

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[T]here are two factors: namely, the nature of the organism and the
nature of the conditions. The former seems to be much more the important, for nearly similar variations sometimes arise under, as far as
we can judge, dissimilar conditions; and, on the other hand, dissimilar
variations arise under conditions which appear to be nearly uniform.
Darwin 1872:32



Contents

Preface
1. Voyage of Discovery
2. Tools for the Voyage

ix
1
23

3. Species: Exploring the Entities

100

4. Historical Biogeography: Exploring Space

173

5. Functions: Exploring Options

253

6. Evolutionary Radiations: Exploring Time

353

7. Community Evolution: Exploring the Space-Time
Continuum

417

8. Coevolution: Exploring Personal Relationships

465

9. Biodiversity: Exploring the Future

525

References

561

Index

661



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Preface

Scientists have odious manners unless you support their
theory; then you can borrow money off them.
Mark Twain

We wrote the predecessor to this book more than a decade
ago in an attempt to show people how the comparative phylogenetic
method could illuminate some of the dark corners of their research. At
that time, our biggest problem was finding enough studies to illustrate
all of the ideas. Over the past decade, interest in this approach has grown
tremendously. This time around we found ourselves in the enviable position of having too many studies from which to choose. Given such an
embarrassment of riches, we could not include everything we encountered during our voyage through the literature (which ended as an active
search on the eve of the new millennium). So, lest anyone feel that his
or her study or group of interest has been neglected, please understand
that our choice of examples is completely subjective and reflects our
own biases toward the organisms and questions we find interesting. We
have striven to include studies based on a wide variety of taxa published
by a geographically diverse group of researchers, but we do not claim
to have provided a true representation of either. The power of this approach is that it is infinitely malleable. All groups, all questions are
welcome!
Those of you who have read Phylogeny, Ecology, and Behavior will find
yourselves initially on familiar ground: an introduction, albeit updated,
to what is still a young but vigorously growing research program. There
are, however, several major differences between Phylogeny, Ecology, and
Behavior and “Voyager.” The first difference results from a change in perspective. A decade ago we emphasized the extent to which adding phylogenetic history to our explanations could simplify and clarify our work.
Believing that the message was complicated, not to mention controversial, enough, we seldom ventured beyond documenting general patterns
supporting the hypothesis that a substantial degree of order in the world
around us was due to phylogenetic history. The past ten years of research

has convinced us (more than ever) that Darwin’s metaphor of the tangled bank is the ultimate descriptor of biodiversity on this planet. We
now believe biologists (including ourselves) are ready to move beyond
ix

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x Preface

the initial stance of “history ϭ simplicity” to “evolution has been so
historically contingent and complex that we need a phylogenetic framework if we are ever to have a hope of disentangling that complexity.”
The second difference is reflected in our sense that this phylogenetic
framework, although necessary, is never sufficient to explain that complexity. We have found ourselves drawn more and more to research integrating phylogenetic and experimental studies in an attempt to detect
the imprint of the past in the shape of extant biodiversity. Third, we
believe that the research program we present in this book can benefit
from connections with other independent and progressive research programs in evolutionary biology. We have attempted to highlight those
connections in “Frontiers” sections at the end of each chapter. Fourth,
we revisit continuously in this book the caveat that nothing should be
eliminated from the “scope of the possible” unless there is strong biological evidence to the contrary. In other words, we do not believe that any
person on this planet has a pipeline to God (or any other words you
choose to associate with a sense of “truth”). Eliminating irritating data
because they do not conform with what one “knows” to be the “correct”
answer is simply not acceptable within the logic of scientific investigation. Another manifestation of this sentiment is our belief that virtual
reality does not take precedence over empirical data. If models do not
agree with the empirical data, chances are the models, not the data,
should be re-evaluated. This is not an antimodel stance. A mutually reinforcing and mutually modifying dialogue between models and empirical
discovery enhances progress. We are naturalists (one of us is a field biologist and the other is an experimental ethologist); therefore, our best contributions come from the accumulation of empirical knowledge about
the world, which can be used both to evaluate predictions of existing
models and to suggest new models.
Finally, we passionately believe that the biodiversity crisis is upon us

and as such should be a real and pressing concern for all biologists. We
owe a special debt of gratitude to Harry Greene and Kelly Zamudio, who
(over a memorable California lunch) urged us to emphasize biodiversity
science in this book. The special debt also extends, with love and gratitude, to Dan Janzen and Winnie Hallwachs, as well as the staff of the
Area de Conservacio´n Guanacaste (a World Heritage site in northwestern
Costa Rica), who operate at ground zero of the biodiversity crisis every
day. They have provided a living platform for integrating many of the
ideas and ideals of historical ecology into biodiversity science, as well as
a world standard of dedication and self-sacrifice in the dual pursuit of
saving biodiversity and promoting socioeconomic development. With-


Preface xi

out the substantial intellectual input of these biologists, as well as their
friendship and constant reminder of what human beings can be at their
very best, one of us at least would have been tempted to give up the
struggle and write murder mysteries.
A book of this scope could not have happened without the input of
many people who generously helped us by discussing ideas, suggesting
novel interpretations, and sharing publications. First and foremost
among those are the many zoology faculty and students at Stockholm
University. For nearly a decade we have been fortunate enough to lecture
to undergraduates at Stockholm and to attend the annual Blod Bad conference at Tovetorp Field Station, where we have had the opportunity to
air our views and to be encouraged and corrected (politely, gently, but
firmly) by researchers at one of the world’s foremost centers for comparative evolutionary studies. Of this large group of people, we especially
¨ rn, Sven Jakobsson (who also introduced
wish to thank Anders Angerbjo
us to the tourist moose), Niklas Janz, Ole Leimar, Patrick Lindenfors,
¨ ren Nylin, Hans Temrin, Birgitta Tullberg, Hans-Erik Wanntorp, Lars

So
Werdelin, Nina Weddell, and Christer Wiklund. Tack, gode va¨nner. Also
first in our hearts are Eric and Margaret Hoberg (U.S. National Parasite
Collection and Johns Hopkins), who have shared ideas about the great
evolutionary drama over good wine and good jazz for over two decades
now (and still invite us back). We also thank the unwavering support
and input of Diedel Kornet, Rino Zandee, Marco Van Veller, and Hubert
Turner at Leiden University, Netherlands (a town of contented cats),
Howard and Irene Burton, who have constantly turned our ideas upside
down by questioning our basic assumptions about the origins of “life,
the universe, and everything,” and Rick Winterbottom, who knows
more about fish (and phylogenetics) than is decent for one modest man
(even if they are marine fish).
We are eternally grateful for our time spent with Douglas Causey
(over too many lunches to remember), Harvard University; Michael
Ryan (whose passion for those terrestrial fish we call frogs is infectious),
David Hillis, James Bull, and Michael Singer, University of Texas; Gerardo Pe´rez Ponce de Leo´n and Virginia Leo´n-Re`gagnon, Universidad
Nacional Auto´noma de Me´xico (who both braved a Toronto winter for
the mutual love of parasitos); Dalton da Souza Amorim, Universidade
de Sa˜o Paulo, Martin Lindsay Christoffersen, Universidade do Joao Pes¨ rs
soa, and Walter Boeger, Universidade do Rio Grande do Sul, Brazil; Eo
Szathma´ry, Institute for Advanced Study, Budapest; Serge Morand,
Universite´ de Perpignan; Philippe Grandcolas and Louise DesutterGrandcolas, Muse´um National d’Histoire Natural, Paris (with particular


xii Preface

¨ rkgratitude for a memorable lunch during a warm day in Paris); Mats Bjo
lund, Ka˚re Bremer, and Fredrik Ronquist, Uppsala University; William
Wright, Colorado State University; Richard Mayden, St. Louis University

(who also knows more about fish, phylogenetics, and conservation than
an ordinary mortal); George Lauder, Harvard University; Bruce Lieberman and Edward Wiley, University of Kansas; Vicki Funk, U.S. National
Museum of Natural History, Smithsonian Institution; Wouter Holleman,
Rhodes University, Francis Thackeray, Pretoria, and Louise Coetzee,
Bloemfontein, South Africa; James Dale and Susan Smith (now blissfully
in Arizona, telescope and all) and Bill Presch, California State UniversityFullerton; Brian Maurer, Michigan State University; John Lynch, Universidad Nacional de Colombia; John Wenzel, Ohio State University;
and Geoffrey Scudder, Cyril Finnegan, and Jack Maze, University of British Columbia.
Closer to home, we greatly appreciate the support and input over numerous cups of coffee from our colleagues Doug Currie, Chris Darling,
Ellen Larsen, Robert Murphy (composer of and player in the famous
phylogenetic rock opera, Rommie), Robert Reisz, Hans-Dieter Sues, Malcolm Telford, and Polly Winsor of the University of Toronto and Royal
Ontario Museum. We also thank the more than 500 University of Toronto undergraduate students who have taken our course based on Phylogeny, Ecology, and Behavior during the past decade (and appear, on the
whole, to have enjoyed it), as well as a decade of outstanding graduate
students at the University of Toronto, notably Jingzhong Fu, Hugh Griffiths, Gregory Klassen, Michelle Mattern (cofounder of the XWP lab),
Randy Mooi, Brian Moore, Mark Siddall, Jon Stone, and David Zamparo.
Their feedback has helped us immensely.
We have taught and spoken at numerous places during the past ten
years, and we thank the organizers and participants for all those activities, as well as the Natural Sciences and Engineering Research Council
(NSERC) of Canada for continuing support of our respective research
programs. Finally, we burn metaphysical oxen to Athena Pronaia for inspiration while reading the first complete draft of this book—sequestered in our room at the Acropole Hotel, gazing down over a sea of olive
trees to the Gulf of Itea and the beginning of the Sacred Way up to
Delphi.
None of these words of gratitude, thanks, and love would have been
possible without the encouragement, the belief, the fathomless capacity
for understanding, the clarity, insight, intuition, and the treasured
friendship of Susan Abrams. Mille grazie speciale amica!
This is an introductory book, providing a set of directions for how to
begin a lifelong voyage of discovery. In the midst of striving to be clear


Preface xiii

about the basics, we may occasionally give the impression that this research is easy. It is not. Everyone on this voyage will encounter their
own personal storms and sea monsters. This the price you pay for the
sheer joy and wonder of discovery. To those of you who believe the voyage should be easy, cheap, and quick, we say, Put this book aside now.
To those of you who understand that the voyage never ends, precisely
because your passion will draw you ever onward, welcome aboard.



Chapter 1

Voyage of Discovery

“Why not go . . . and study . . . for yourself?”
Lord Dorwin raised his eyebrows and took a pinch of
snuff hurriedly. “Why, whatevah foah, my deah fellow?”
“To get the information firsthand, of course.”
“But wheah’s the necessity? It seems an uncommonly
woundabout and hopelessly wigmawolish method of getting
anywheahs. Look heah, now. I’ve got the wuhks of all the
old masters. . . . I wigh them against each othah—balance
the disagweements—analyze the conflicting statements—decide which is pwobably cowwect—and come to a conclusion.
That is the scientific method.”
Isaac Asimov, Foundation

Isaac Asimov’s Lord Dorwin is as far removed from Charles
Darwin as is possible to imagine. Although he is known today primarily
as a brilliant theoretician, Darwin was first and foremost a consummate
naturalist. His firsthand knowledge of biological diversity in many parts
of the world helped him “weigh the works of the great masters,” synthesizing information from each to formulate a conception beyond any one

person (Darwin 1859). With this new theory of evolution, Darwin himself became one of the great, if not the greatest, masters of all time in
biological sciences. Today, nearly a century and a half later, one might
think the task set out by Darwin complete, or at least that the finish line
was in sight. Nothing could be further from the truth. In fact, only about
10 percent of the basic units of evolution on this planet, species, have
been described and named. And we know the natural history for only a
fraction of that 10 percent. It would appear that there is still a place for
voyages of discovery. In this book, we will take you on one such voyage,
partly with the intent of convincing younger people that many such
voyages are possible and indeed necessary, and partly for the sheer joy
of the journey.
Nature is complex. As sentient beings, we have always sought explanations for the origin and maintenance of that complexity, hoping that
1


2 Chapter One

somewhere during the search we would discover answers to questions
about who we are and where we fit in the global biosphere. The search
for those answers has been conducted from many different perspectives,
from religion to sociology, art to science. Each perspective contributes a
valuable piece to the puzzle, a way of “seeing the world.” As biologists,
we can trace the roots of our way of seeing to the earliest paintings of
animals on cave walls and the emergence of myth making. All mythology is tied to an awareness of surrounding organisms and their natures.
We are connected to these myths, and thus to millennia of observing,
describing, and documenting the diversity of life, by our fascination
with the nature of the organism. That fascination entered the formal
realm of science when Darwin (building upon ideas from Lamarck and
Wallace) united that vast but loosely connected network of biological
information under one cohesive principle: the theory of evolution.

Darwin’s original conceptual framework included two components.
First, all organisms are connected by common genealogy:
[T]he characters which naturalists consider as showing true affinity
between any two or more species, are those which have been inherited from a common parent, all true classification being genealogical. (1872:346)

Second, the forms and functions of organisms are closely tied to the
environments in which they live:
[S]light modifications, which in any way favoured the individuals
of any species, by better adapting them to their altered conditions,
would tend to be preserved; and natural selection would have free
scope for the work of improvement. (1872:59)

Many specialized research programs emerged from these two postulates over the next 100 years. Every one of those budding disciplines
initially incorporated both genealogical (phylogenetic) and environmental (adaptational) factors into their explanations of evolutionary change.
However, the role of phylogeny was progressively diminished in some
fields, most notably in ecology, ethology, and the physiological sciences, while in other fields, most notably systematics, the role of the
environment was virtually eliminated from evolutionary explanations.
This, in turn, led to the emergence of markedly different worldviews
even within evolutionary biology. Gareth Nelson summarized two of
these perceptual differences in a discussion at a biogeography conference
at the American Museum of Natural History in 1979. He told an apocryphal story of two biologists, one an ecologist and the other a systematist,
who stepped into a large room together. Suspended from the ceiling by
a variety of supports were thousands of balls of many different colors


Voyage of Discovery 3

and sizes. All at once the supports were cut, and all the balls dropped
from the ceiling, hit the floor, and began bouncing around the room.
The ecologist exclaimed, “Look at the diversity!” whereupon the systematist said, “Hmm, 32 feet per second per second!”

The Darwinian revolution was founded on the concept that biological
diversity evolved through a combination of genealogical and environmental processes. Although in theory the majority of biologists adhere
to this proposition, until recently phylogenetic and ecological/behavioral studies have often been conducted quite independently. Is this a
problem? In order to answer this question let us consider the following
thought experiment. Suppose we were to pick, at random, any organism
from a designated tide pool and a crab from anywhere in the world. If
we then asked for a list of morphological, behavioral, and ecological
characteristics of the unknown organism from a given environment and
of the known organism (a crab) from an undetermined habitat, we
would expect that more of the predictions would be correct for the crab
than for the unknown tide-pool organism. At the same time, we would
not expect to be able to predict all the ecological and behavioral features
of our unknown crab without knowledge of the environment in which it
normally lives. So it appears that Darwin’s original intuition was correct:
evolutionary explanations require reference both to phylogeny and to
local environmental conditions. The answer to the preceding question
is thus, Yes, the sundering of phylogenetic and ecological/behavioral
studies is an important problem because the exclusion of either will
weaken our overall evolutionary explanations.
This answer leads us to two new questions: First, given the conceptual
framework proposed by Darwin, how did this dissociation come to be?
In order to answer this question we must examine the histories of three
disciplines: ethology, ecology, and evolutionary biology. This in itself has
formed the central theme for numerous papers, books, and book chapters,
so we will present only brief summaries.1 Second, how can communication between ecology/behavior and systematics in evolutionary biology
be reestablished? Answering this question requires the development of a
1. See, e.g., Kingsland 1985; McIntosh 1985, 1987; Lauder 1986; Hull 1988; McLennan
et al. 1988; Burghardt and Gittleman 1990; Funk and Brooks 1990; Ross and Allmon 1990;
Wanntorp et al. 1990; Brooks and McLennan 1991, 1993a,b; Harvey and Pagel 1991;
Maurer 1991; Behrensmeyer et al. 1992; Mayden 1992a,b; Zrzavy 1992; Miles and Dun˜ ez-Farfa´n and Cordero 1993; Ricklefs and Schluter 1993; Shettleworth

ham 1993; Nu´n
1993; Skelton 1993a; Allmon 1994; Eggleton and Vane-Wright 1994; Grandcolas et al.
1994; Grande and Rieppel 1994; Hall 1994; Wainwright and Reilly 1994; Brooks et al.
1995; Harvey, Brown, and Smith 1995; Wagner and Funk 1995; Harvey 1996; Jablonski et
al. 1996; Martins 1996; Rose and Lauder 1996; Sanderson and Hufford 1996; Begun et al.
1997; Kendrick and Crane 1997; Pe´rez Ponce de Leo´n 1997; Pe´rez Ponce de Leo´n et al.
1997; Grandcolas 1998; and Hernandez et al. 2000.


4 Chapter One

research program that will allow us to integrate ecological, behavioral, and
historical information to produce a more complete picture of evolution.
The remainder of this book delineates the conceptual, methodological,
and empirical foundations for one such research program.
LOSING TIME IN EVOLUTIONARY BIOLOGY
The Eclipse of History in Ethology

Ethology, as a science, was founded upon a tradition of investigating
behavior within an explicitly phylogenetic framework. Darwin started
the ball rolling when he compared, among other things, the behavior of
two species of ants within the genus Formica in an attempt to trace the
evolution of slave making in ants. Following this example, the “founding fathers” of ethology, Oskar Heinroth and Charles O. Whitman, proposed that there were discrete behavioral patterns which, like morphological features, could be used as indicators of common ancestry.
Whitman’s (1899) views mirrored Darwin’s: “Instinct and structure are
to be studied from the common viewpoint of phyletic descent”(262).
This perspective served as the focal point for a plethora of studies in the
early twentieth century. Behavioral data were examined with an eye to
their phylogenetic significance for birds, including anatids (ducks and
their relatives) (Heinroth 1911; Herrick 1911), weaver birds (Chapin
1917), cowbirds (Friedmann 1929), and birds of paradise (Stonor 1936);

and for insects and spiders, including wasps of the family Vespidae
(Ducke 1913), bumblebees (Plath 1934), caddisfly larvae (Milne and
Milne 1939), termites (Emerson 1938), social insects in general (Wheeler
1919), and spiders (Petrunkevitch 1926). Wheeler reiterated Darwin’s
and Whitman’s perspective and reaffirmed the basis of ethological studies at the time: “Of late there has been considerable discussion . . . as to
the precise relation of biology to history . . . and what most of us older
investigators have long known seems now to be acceded, namely that
biology in the broad sense and including anthropology and psychology
is peculiar in being both a natural science and a department of history
(phylogeny)” (1928:20).
Comparative behavioral studies flourished under the direction of Konrad Lorenz and Niko Tinbergen during the 1940s and 1950s. Both of
these ethologists repeatedly emphasized two distinct but related points:
behavioral patterns are as useful as morphology in assessing phylogenetic relationships, and behavior does not evolve independently of phylogeny. Lorenz stated that “all forms of life are, in a way, phylogenetic
attainments whose special objects would have to remain completely
obscure without the knowledge of their phylogenetic development”


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Voyage of Discovery 5

(1941:3), and “every time a biologist seeks to know why an organism looks
and acts as it does, he must resort to the comparative method” (1958:69;
see also Lorenz 1950). Tinbergen outlined the comparative method:
The naturalist . . . must resort to other methods. His main source
of inspiration is comparison. Through comparison he notices both
similarities between species and differences between them. Either
of these can be due to one of two sources. Similarity can be due to
affinity, to common descent; or it can be due to convergent evolution. It is the convergences which call his attention to functional
problems. . . . The differences between species can be due to lack of
affinity, or they can be found in closely related species. The student

of survival value concentrates on the latter differences, because
they must be due to recent adaptive radiation. (1964:421–422)

In other words, the phylogenetic relationships among species provide
the platform from which explanations of processes responsible for behavioral evolution within species must be derived.
Although the comparative approach to studying behavioral evolution
flourished during the 1950s and 1960s, skepticism mounted about Lorenz’s assertion that species-specific behavioral characters were valuable
systematic characters. By the centenary of the publication of Darwin’s
book, two widely divergent viewpoints had emerged:
To assume evolutionary relationships on the basis of behavior patterns is not justifiable when such findings clearly contradict morphological considerations. The methods of morphology will therefore remain the basis for the natural system [of classification].
(Starck 1959, cited in Eibl-Eibesfeldt 1975:223)
If there is a conflict between the evidence provided by morphological characters and that of behavior, the taxonomist is increasingly
inclined to give greater weight to the ethological evidence. (Mayr
1960:345)

This difference in opinion was founded, in part, upon continuing unresolved debates among ethologists. Two questions recurred: first, how
well can sequences of ancestral and derived traits be determined for attributes that left no fossil record; and second, how well can similarities due
to common ancestry (homology) be distinguished from similarities due
to convergent or parallel evolution (homoplasy)?2 The question of homology was problematical because homologous characters were defined
by their common origin and, at the same time, were used to reconstruct
phylogenetic relationships. The inherent circularity in such a method
bothered many biologists. Remane (1956) proposed a set of criteria for
2. Boyden 1947; Lorenz 1950; Tinbergen 1951, 1953; Schneirla 1952; and Michener
1953.

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6 Chapter One

testing hypotheses of common origin (homology) without a priori reference to phylogeny. These were (1) similarity of position in an organ system; (2) special quality (e.g., commonalities in fine structure or development); and (3) continuity through intermediate forms. Although
authors did not agree about the universal applicability of Remane’s criteria
to behavior, the majority accepted that the criterion of special quality,
studied at the level of muscle contractions (fixed action patterns), was
the fundamental tool for establishing behavioral homologies (Baerends
1958; Remane 1961; Wickler 1961; Albrecht 1966). Initial attempts to
homologize behavior in this way were admittedly vague and simplistic
when compared to the more quantitative methodology of comparative
morphology, but this reflected more the youth of the discipline than a
fundamental flaw in the behavioral traits themselves. Time and again,
phylogenies reconstructed using behavioral characters mirrored those
based solely on morphology. However, in a scathing review of the ethologists’ research program, Atz made only a cursory reference to these successes when he concluded,
The number of instances in which behavior has provided valuable
clues to systematic relationships has continued to grow but it
should be made clear that the establishment of detailed homologies was seldom, if ever, necessary to accomplish this. . . . Functional, and especially behavioral, characters usually do not involve
demonstrable homologies, but depend instead on resemblances
that may be detailed and specific but nevertheless cannot be traced,
except in a general way, to a common ancestor. . . . Until the time
that behavior, like more and more physiological functions, can be
critically associated with structure, the application of the idea of
homology to behavior is operationally unsound and fraught with
danger, since the history of the study of animal behavior shows
that to think of behavior as structure has led to the most pernicious
kind of oversimplification. (1970:67–69)

Lorenz had marked the beginning of the eclipse when he wrote, “I am
quite aware that biologists today (especially young ones) tend to think
of the comparative method as stuffy and old-fashioned—at best a
branch of research that has already yielded its treasures, and like a spent
gold mine no longer pays the working. I believe that this is untrue”

(1958:69). Atz’s review punctuated the eclipse. For nearly 20 years, only
a few intrepid souls maintained the belief that phylogenetically relevant
behavioral homologies existed, could be studied scientifically, and were
important to explanations of the evolution of behavior.3
3. For example, Dunford and Davis 1975; Radinsky 1975; Drummond 1981; Greene
1983, 1986a,b, 1988; Hunt et al. 1983; Lauder 1986; Arnold 1987; McLennan et al. 1988;
Miller 1988; and Shine 1988.


Voyage of Discovery 7

Lorenz cautioned, “The similarity of a series of forms, even if the series structure arises ever so clearly from a separation according to characters, must not be considered as establishing a series of developmental
stages” (1941:81). In his opinion, without reference to phylogenetic relationships, the criterion of similarity was, of itself, a dangerously misleading evolutionary marker. Unfortunately, the Gordian knot of behavioral homology drove ethologists toward a new methodology based, in
direct contrast to Lorenz’s warning, upon arranging behavioral characters as a “plausible series of adaptational changes that could easily follow
one after the other” (Alcock 1984:432). Although intuitively pleasing,
this method relies heavily on subjective, a priori assumptions concerning the temporal sequence of ethological modifications and dissociates
character evolution from underlying phylogenetic relationships. This
dissociation of history from behavioral evolution has had an important
impact on both the nature and direction of ethological research.4
The Eclipse of History in Ecology
Ecology is founded upon the search for an understanding of the interactions between an individual and its environment. This simple aim masks
a Herculean challenge, for the term “individual” can encompass practically all levels of biological organization, from the organism through the
species to the ecosystem. The complexity of this search prompted Moore,
in the opening paper of the first issue of Ecology, to call for an integration
of ecology with other sciences.
There have been three stages in the development of the biological
sciences: first, a period of general work, when Darwin, Agassiz and
others amassed and gave their knowledge of such natural phenomena as could be studied with the limited methods at hand; next,
men specialized in different branches, and gradually built up the
biological sciences which we know today; and now has begun the

third or synthetic stage. Since the biological field has been reconnoitered and divided into its logical parts, it becomes possible to
see the interrelations and to bring these related parts more closely
together. Many sciences have developed to the point where . . .
contact and cooperation with related sciences are essential to full
development. Ecology represents the third phase. (1920:3)

Over the next 30 years, the call for integration and cooperation was
answered by disciplines such as forestry and geology. Communication
4. Lauder 1986; McLennan et al. 1988; Brooks and McLennan 1991; Wenzel 1992; and
Greene 1994a. For a discussion of nonhistorical and historical perspectives on particular
topics, see Pearson et al. 1988; Mooi et al. 1989; Pearson 1990; Altaba 1991; and Vogler
and Kelley 1996, 1998.


8 Chapter One

between ecologists and systematists developed more slowly, however,
and this period saw only a handful of studies exploring ecological questions within a historical framework.5 Although numerically small, this
research foreshadowed the emergence of a phylogenetically based perspective in ecology at the same time that this theme was being developed in ethology. On one side of the Atlantic, Lorenz (1941), drawing
on his observations of ducks and their relatives, was emphasizing the
importance of phylogeny to studies of behavioral evolution. On the
other side of the ocean, Bragg and his coworkers were reaching a similar
conclusion from their extensive studies of the ecology and natural history of toads.
Since variations in ecological conditions (physical or biotic) markedly effect the lives of individual organisms, and through this, of
species, it follows that there is a broader line between the usual
ecological emphasis upon succession of communities to the climatic or edaphic climax of a given region, on the one hand, and
the taxonomic and geographic distributional emphasis of taxonomists and biogeographers on the other. The study of habits of animals, interpreted in the light of both ecology and taxonomy is,
thus, an aid—indeed an absolute essential—to a complete understanding by either group of workers of the peculiar problems of
either. (Bragg and Smith 1943:301)

The next 25 years were characterized by two significant changes: the
appearance of papers by systematists in ecological journals, echoing this
sentiment of cooperation, and a burst in the number of comparative
studies.6 The ascension of the comparative approach coincided with the
appearance of the “new” evolutionary ecological perspective developed
by Hutchinson and MacArthur. This research program was primarily
concerned with attempting to answer the general question, Why are
there so many species? and its corollary, How do these species manage
to coexist? Answers to these questions had traditionally been sought
within a comparative framework, an approach reinforced by MacArthur’s statement, “Ecological investigations of closely-related species
then are looked upon as enumerations of the diverse ways in which the
resources of a community can be partitioned” (1958:617). King empha5. See, e.g., Baker 1927; Rau 1929, 1931; Parker 1930; Talbot 1934, 1945, 1948; Park
1945; Park and Frank 1948; and Smith and Bragg 1949.
6. Papers by systematists include Sabrosky 1950; Davidson 1952; Constance 1953; and
McMillan 1954. Comparative studies include Pavan et al. 1950; Hairston 1951; Dobzhansky and da Cunha 1955; Carpenter 1956; MacArthur 1958; Kohn 1959; Cade 1963; Rand
1964; Schoener 1965, 1968a,b; Shoener and Gorman 1968; Brown 1971; Preston 1973;
Laerm 1974; Roughgarden 1974; and McClure and Price 1975.


Voyage of Discovery 9

sized the importance of searching for competitive exclusion within a
closely related group of organisms in his critique of MacArthur’s broken
stick model of species abundance.
As realized by Darwin, the principle of competitive exclusion is
most applicable to closely related sympatric species (that is, to species of high taxonomic affinity) having similar but not identical
niches. This may be related to the MacArthur model since when
competitive exclusion has taken place, the species of high taxonomic affinity that remain may be expected to have niches which
are nonoverlapping but contiguous. Hairston suggests that tests of
these species should display better fits to the MacArthur model

than do tests of all species occurring in the habitat. That these predictions are valid was first indicated by the striking fits obtained
by Kohn when only members of the genus Conus were examined.
Subsequent investigations of fresh-water fishes . . . reveal that in
one collection from a single locality members of the class do not
fit well, but when members of the same family are considered the
fit is much better. (1964:723)

MacArthur set the tone for ecological studies of species coexistence
and the search for correlations between changes in a species’ ecology
and changes in the environment. However, although evolutionary ecologists were examining experimental data within a comparative framework, few researchers were incorporating phylogenetic information into
their evolutionary explanations (for a historical review, see Collins
1986). The difference between asking a question within a historical context and incorporating historical information into the answer is a critical
and, at first, counterintuitive one. Consider the following simple example. Suppose you are interested in the question of species coexistence.
As MacArthur noted, the best place to look for the factors involved in
species coexistence is among sympatric populations of congeners. The
assumption behind this recommendation is a historical one: members
of the same genus should theoretically share a number of ecological,
morphological, and behavioral characters in common because they are
all descended from a common ancestor. The recognition that the genealogical relationships among species may influence the outcome of an
experimental investigation is the first step in any evolutionary ecological
study. Having discovered an appropriate group of sympatric congeners,
you set about collecting a wealth of data concerning feeding behavior,
habitat preference, and breeding cycles, in order to identify the way(s)
in which the species are partitioning their environment. This second
step in your study is primarily nonhistorical because it requires that you
make assumptions about the evolutionary past of species’ interactions,


10 Chapter One

based upon characters and interactions observed in the present environment. What is missing here is information about the evolutionary origin
and elaboration of the characters and of the associations themselves. So,
when we talk about “incorporating phylogenetic data into an evolutionary explanation,” we are referring to the combination of both the history
of the species and the history of the traits that characterize interactions among
those species.
The number of historically based studies began to decrease within
the rapidly burgeoning field of ecology at about the same time that the
comparative method was waning in ethology.7 This trend continued
through the 1980s8 and, paradoxically, paralleled an increase in the
number of studies concerned with examining ecology within a specifically evolutionary context. We cannot offer any particular explanation
for this observation. Part of the answer may stem from the MacArthurian
perception that historical effects, though real, would confound ecological predictions (see, e.g., Facelli and Pickett 1990). Part of the answer
may simply be that the theoretical foundations for ecology were well
developed by the 1970s so more ecologists turned their attention toward
a rigorous examination of the assumptions underlying those theories.
Although painstaking, there is no other way to test assumptions than
by careful species-by-species examination. And still another part of the
answer may lie in an observation by Stenseth (1984) that ecology was
once the “hand-maiden” of taxonomy, but became a science on its own
in the 1960s. If many ecologists felt they had been under the yoke of
taxonomy, perhaps the break had more to do with desires for individual
identities. If so, it would be unfortunate, because many systematists
have felt the same way about the subordination of their discipline
within ecology. Thus, ironically, the perception of subordination by
members of each specialty has been based on mutual misapprehensions.
Whatever the reason, Ricklefs (1987) suggested that this “eclipse of
history” had a profound and adverse effect on the field of community
ecology. He argued that community ecology had relied mostly on localprocess theories for explanations of patterns that are strongly influenced
by regional processes. Local explanations rely on the action of competition, predation, and disease to explain patterns of species diversity in
small areas, from hectares to square kilometers. According to this perspective, the community is maintained at a saturated equilibrium by bi-

7. But see Fraser 1976; Huey and Webster 1976; Huey and Pianka 1977; May 1977;
Pitelka 1977; and Hubbell and Johnson 1978.
8. But see Hixon 1980; Hairston 1981; Keen 1982; Horton and Wise 1983; Kingsolver
1983; Davidson and Morton 1984; Schroder 1987; and Armbruster 1988.