Evolution's Wedge: Competition and the Origins of Diversity

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Overview

Evolutionary biology has long sought to explain how new traits and new species arise. Darwin maintained that competition is key to understanding this biodiversity and held that selection acting to minimize competition causes competitors to become increasingly different, thereby promoting new traits and new species. Despite Darwin’s emphasis, competition’s role in diversification remains controversial and largely underappreciated.


In their synthetic and provocative book, ...

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Evolution's Wedge: Competition and the Origins of Diversity

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Overview

Evolutionary biology has long sought to explain how new traits and new species arise. Darwin maintained that competition is key to understanding this biodiversity and held that selection acting to minimize competition causes competitors to become increasingly different, thereby promoting new traits and new species. Despite Darwin’s emphasis, competition’s role in diversification remains controversial and largely underappreciated.


In their synthetic and provocative book, evolutionary ecologists David and Karin Pfennig explore competition's role in generating and maintaining biodiversity. The authors discuss how selection can lessen resource competition or costly reproductive interactions by promoting trait evolution through a process known as character displacement. They further describe character displacement’s underlying genetic and developmental mechanisms. The authors then consider character displacement’s myriad downstream effects, ranging from shaping ecological communities to promoting new traits and new species and even fueling large-scale evolutionary trends. Drawing on numerous studies from natural populations, and written for a broad audience, Evolution’s Wedge seeks to inspire future research into character displacement’s many implications for ecology and evolution.

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Editorial Reviews

From the Publisher

"Fresh. . . . Well documented and easily accessible. . . . Highly recommended."--Choice
Choice - F. T. Kuserk
“Fresh. . . . Well documented and easily accessible. . . . Highly recommended.”
BioScience - Alexander Pigot
"Enjoyable to read. . . . [Evolution's Wedge is] a valuable resource for any student or established researcher with an interest in Earth’s biological diversity."
The Quarterly Review of Biology - Richard A. Richards
"A welcome addition to the discussion."
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Product Details

  • ISBN-13: 9780520274181
  • Publisher: University of California Press
  • Publication date: 10/25/2012
  • Series: Organisms and Environments Series
  • Pages: 320
  • Product dimensions: 7.20 (w) x 10.10 (h) x 2.90 (d)

Meet the Author

David W. Pfennig is Professor of Biology at the University of North Carolina.
Karin S. Pfennig is Associate Professor of Biology at the University of North Carolina.

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Read an Excerpt

Evolution's Wedge

Competition and the Origins of Diversity


By David W. Pfennig, Karin S. Pfennig

UNIVERSITY OF CALIFORNIA PRESS

Copyright © 2012 The Regents of the University of California
All rights reserved.
ISBN: 978-0-520-27418-1



CHAPTER 1

DISCOVERY OF A UNIFYING PRINCIPLE


In a frequently heard—and perhaps apocryphal—story, the evolutionary biologist J. B. S . Haldane, when asked to comment on what could be inferred about the Creator based on the creation, is reported to have said, "He must have had an inordinate fondness of beetles" (Farrell 1998). Why are there so many species of beetles (Figure 1.1A)? For that matter, why are there so many different kinds of living things generally?

As it turns out, living things are amazingly diverse. As one measure of this diversity, conservative estimates place the number of species alive today at 8 to 10 million (Stork 1993; Hamilton et al. 2010; Wilson 2010, p. x; Mora et al. 2011). Yet, as staggering as these numbers are, they vastly underestimate life's true diversity: all species consist of individual organisms that are themselves unique. Indeed, each species comprises a bewildering array of morphological, physiological, ecological, and behavioral traits (for example, see Figure 1.1B, C). In short, the total inherited variation of all organisms—"biodiversity," as coined by Wilson and Peter (1988)—is truly astounding.

Biodiversity demands explanation. Why are there so many different species? Why do species typically express different traits, especially when these traits influence resource acquisition or reproduction (for example, see Figure 1.1B)? Why do species harbor so much trait variation within them, which, in some cases, is as pronounced as the variation normally seen between different species (for example, see Figure 1.1C)? What factors trigger the formation of new traits and new species in the first place? Finally, once new species do arise, why do they sometimes coexist with other species and sometimes not?

One hundred and fifty years ago, Charles Darwin (1859 [2009]) offered a scientific explanation for biodiversity—natural selection. Although natural selection is an evolutionary process, Darwin argued that at natural selection's core is an ecological process: competition. (Throughout this book, the term "competition" refers to any direct or indirect interaction between species or populations that reduces access to vital resources or successful reproductive opportunities and that is therefore deleterious — on average—to both parties; see Table 1.1.) According to Darwin (1859 [2009]), all organisms face recurring competition for scarce resources, and this competition favors individuals that are least like their competitors in resource use and associated traits. Consequently, groups of organisms that compete should become increasingly different over time. Selection driven by competition, Darwin held, is the primary engine of diversification.

This book explores how competitively mediated selection generates biodiversity. In particular, we examine how such selection—whether stemming from competition for resources or access to successful reproduction—can promote evolutionary diversification through a process known as "character displacement" (sensu Brown and Wilson 1956). Although evolutionary biologists have long recognized that numerous factors can act as agents of selection and thereby potentially promote diversification (these factors are reviewed in MacColl 2011), competition may be the most common of all selective agents (Vermeij 1987; Amarasekare 2009). Moreover, because competition (unlike, for example, predation) is uniquely mutually costly to both parties involved (Table 1.1), it is a particularly potent agent of divergent selection, which can serve as a wedge that drives competitors apart ecologically and phenotypically.

Our aim in this book is to evaluate character displacement's role in the origins, maintenance, abundance, and distribution of biodiversity. In this opening chapter, we summarize the history of the discovery of character displacement and describe how the process of character displacement is often conflated with the patterns that are predicted to arise from it. We also provide a formal definition of character displacement that avoids such confusion. We conclude the chapter with a discussion of how character displacement serves to unify evolutionary biology and ecology.


A BRIEF HISTORY

Divergence of character ... is of high importance on my theory, and explains, as I believe, several important facts.

(DARWIN 1859 [2009], p. 111)

Natural selection, also, leads to divergence of character; for more living beings can be supported on the same area the more they diverge in structure, habits, and constitution, of which we see proof by looking at the inhabitants of any small spot or at naturalised productions. Therefore during the modification of the descendants of any one species, and during the incessant struggle of all species to increase in numbers, the more diversified these descendants become, the better will be their chance of succeeding in the battle of life. Thus the small differences distinguishing varieties of the same species, will steadily tend to increase till they come to equal the greater differences between species of the same genus, or even of distinct genera.

(DARWIN 1859 [2009], pp. 127–128)

... it is the most closely-allied forms,—varieties of the same species, and species of the same genus or of related genera,—which, from having nearly the same structure, constitution, and habits, generally come into the severest competition with each other. Consequently, each new variety or species, during the progress of its formation, will generally press hardest on its nearest kindred, and tend to exterminate them.

(DARWIN 1859 [2009], p. 110)


With these words, Darwin first proposed that competition acts as a ubiquitous and potent agent of divergent selection. Darwin's ideas were groundbreaking: none of his predecessors had viewed interactions among organisms as being significant in evolution (Ridley 2005). The crux of Darwin's idea is that when organisms compete for scarce resources, natural selection should favor those individuals that are least like their competitors. Consequently, groups of organisms that compete should become more dissimilar over time.

Darwin considered this process, which he dubbed "divergence of character," to be "of high importance" for two reasons. First, he held that this process was crucial to the origin of species. According to Darwin, selection that minimizes competition between "varieties" could drive divergence between them until they became separate species (see the second quote above).

Second, Darwin maintained that his principle of divergence of character could explain why species tend to differ phenotypically and also—perhaps even more radically — why evolution has produced a distinctive "tree-like" typology (reviewed in Ridley 2005). Indeed, Darwin changed the way that we view the shape of evolution. Before Darwin, the image of evolution (attributed mostly to the early evolutionists Jean-Baptiste Lamarck and Geoffrey Saint-Hilaire) was that of a ladder, with ancient, simpler life forms at the base of the ladder and more complex life forms at the top (Gould 1989). In this system, lineages did not branch. Instead, evolutionary lineages persisted indefinitely, gradually accumulating changes over many generations, until they became new species (Figure 1.2A).

Darwin's view of evolution was entirely different. His imagery was that of a tree, in which ancestors and descendants split and coexisted. Moreover, according to Darwin, when evolutionary lineages split, they tended to produce two new lineages that diverged from one another, thereby accentuating the tree-like pattern (Figure 1.2B). Darwin held that evolution's divergent nature could be traced to the tendency for the strength of competition to decrease with increasing divergence between competitors (see the third quote above). Thus, according to Darwin, by continually eliminating intermediate forms, competitively mediated selection has caused species to differ and the history of life to resemble a tree, with numerous, diverging branches.

As the above discussion indicates, the concept of divergence of character was crucial to Darwin's thinking on the origin and diversity of species. Indeed, Darwin devoted as much space in The Origin to discussing divergence of character as he did to discussing the idea for which he is most widely known—natural selection (Ridley 2005). Yet, despite the importance that Darwin attached to his principle of divergence of character, he failed to provide any actual examples of competitively mediated divergence in contemporary species. Moreover, although some have questioned whether Darwin's principle of divergence of character is actually synonymous with character displacement (this is reviewed in Pfennig and Pfennig 2010), Darwin's statements that "more living things can be supported on the same area the more they diverge" and that "each new variety or species ... will generally press hardest on its nearest kindred" suggest that he envisioned the modern process of character displacement, in which sympatric species diverge owing to the action of competitively mediated selection.

As it turns out, for Darwin to come up with examples of competitively mediated divergence in contemporary species would have been no trivial exercise. Indeed, competitively mediated divergence can be notoriously difficult to detect. On the one hand, if two species are phenotypically similar enough to compete, then they probably have not undergone much divergence. On the other hand, if two species have already undergone competitively mediated divergence, then they are probably no longer similar enough to experience much competition with each other for an investigator to detect.

Lack (1947) was the first to propose a way around this conundrum. Lack was strongly influenced by Gause's (1934) hypothesis that, because of competition, no two species could persist in the same locality without possessing ecological differences (we expand on Gause's hypothesis in chapter 2). From this idea, Lack (1947) developed a powerful approach for detecting competition's evolutionary signature in natural populations. In particular, he devised the method of comparing different populations of the same species—those in sympatry with a heterospecific versus those in allopatry—to test the evolutionary effects of interspecific competition. The logic behind this approach is clear: selection to lessen competition between a pair of species will act only in areas where the two species actually co-occur. Thus, if competition plays an important role in evolution, Lack reasoned we should observe a distinctive pattern in which species pairs are more dissimilar where they occur together than where each occurs alone (Figure 1.3).

In developing these ideas, Lack drew on his detailed studies of finches from the Galápagos Islands. This archipelago contains over a dozen endemic species of finches, many of which co-occur on some islands but not on other islands (Grant 1986; Grant and Grant 2008). Interestingly, Darwin visited the Galápagos Islands as a young man in 1835, and these same finches—now referred to as "Darwin's finches" (Lack 1947)—were crucial in sparking Darwin's thinking about evolution and natural selection (Browne 1995). Indeed, according to Sulloway, Darwin was convinced that competitively mediated selection could explain why these species differ in the size and shape of their beaks. However, Darwin lacked evidence demonstrating that different beak morphologies were effective at reducing competition (Sulloway 1982).

Unlike Darwin, Lack was able to demonstrate that competition likely explained the observed differences between species in beak morphology. Specifically, he described several cases in which different species of finches differed in beak morphology more where they were sympatric with each other than where they were allopatric (Figure 1.4). He argued that such divergence between sympatric populations was a signature of past selection that had minimized resource competition. Specifically, Lack stated:

The significance of these marked beak differences between species otherwise similar has excited speculation from all who have discussed Darwin's finches.... If two species of birds occur together in the same habitat in the same region, eat the same types of food and have the same other ecological requirements, then they should compete with each other, and since the chance of their being equally well adapted is negligible, one of them should eliminate the other completely.... There must be some factor which prevents these species from effectively competing.... I consider that the marked difference in the size of their beaks is an adaptation for taking food of different size ... to enable [different species] to live in the same habitat without effectively competing. (Lack 1947, pp. 61 – 64)


Although Lack made a convincing case for competition having played a role in the adaptive radiation of finches on the Galápagos Islands, an important question remained: how general was this phenomenon (Mayr 1947)? The answer to this question awaited publication of a landmark paper by Brown and Wilson (1956). This paper was important for three reasons.

First, Brown and Wilson established that Galápagos finches were not unique. They sifted through the literature and applied the method of comparing sympatric and allopatric populations to taxa as diverse as insects, crabs, fish, amphibians, and birds. They presented several compelling cases in which species pairs were recognizably different in sympatry but not in allopatry, which suggested that competition may play a general role in promoting divergence between species.

Second, Brown and Wilson attached a name to the phenomenon. In their paper, they coined the term "character displacement" to describe the pattern of exaggerated divergence in sympatry. In particular, Brown and Wilson (1956, p. 63) defined character displacement as "the situation in which, when two species of animals overlap geographically, the differences between them are accentuated in the zone of sympatry and weakened or lost entirely in the parts of their ranges outside this zone."

Third, Brown and Wilson emphasized that a pattern of exaggerated divergence in sympatry may reflect selection to minimize both resource competition ("ecological" character displacement) and mismatings between species ("reproductive" character displacement). In an earlier version of his book, Lack (1945) too had actually suggested that differences in beak size in Galápagos finches also mediate species recognition signals and might thereby reduce reproductive interactions between species, a conclusion that has been confirmed subsequently by Ratcliffe and Grant (1983).

As a consequence of Brown and Wilson's paper, ecologists and evolutionary biologists became more aware of the phenomenon of character displacement. They also began to consider how both resource competition and reproductive interactions may impose selection favoring divergence between species. Indeed, in the half-century since the publication of Brown and Wilson's influential paper, numerous instances of exaggerated divergence between sympatric species—in characters associated with both resource use and reproduction (for example, see Figure 1.5)—have been documented in taxa ranging from plants and protozoa to snails and shrews (see reviews by Howard 1993; Schluter 2000; Dayan and Simberloff 2005). In the next section, we describe some of the approaches that have been used to detect character displacement.


DETECTING CHARACTER DISPLACEMENT

The most compelling evidence for the occurrence of character displacement is to observe it actually taking place. However, because an evolutionary response to selection often takes many generations, direct corroboration is uncommon. In one such direct demonstration of character displacement, Grant and Grant (2006) documented the evolution of character displacement in Galápagos finches (Figure 1.6). Moreover, an evolutionary response to competitors has been demonstrated in laboratory populations of organisms that have short generation times (Barrett and Bell 2006; Tyerman et al. 2008).

Such direct demonstrations of character displacement are not feasible in many species. Nevertheless, most systems can be used to test key predictions of the hypothesis that competitively mediated selection promotes divergence between species. These experiments are conducted within a single generation and focus on species for which prior observational evidence exists to suggest that they have undergone character displacement (we describe how such observational evidence is gathered later in this section). For example, experiments have been used to test a crucial prediction of character displacement theory: that those members of a focal species that are the most similar to a heterospecific competitor in resource use or reproductive traits suffer the most from competition with that heterospecific (for example, see Schluter 1994; Pfennig et al. 2007; Smith and Rausher 2008).


(Continues...)

Excerpted from Evolution's Wedge by David W. Pfennig, Karin S. Pfennig. Copyright © 2012 The Regents of the University of California. Excerpted by permission of UNIVERSITY OF CALIFORNIA PRESS.
All rights reserved. No part of this excerpt may be reproduced or reprinted without permission in writing from the publisher.
Excerpts are provided by Dial-A-Book Inc. solely for the personal use of visitors to this web site.

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Table of Contents

Preface

1. Discovery of a Unifying Principle

Introduction
A Brief History
Detecting Character Displacement
Phenomena Mistaken for Character Displacement
What Constitutes Character Displacement?
Conflation of Process and Pattern
Reproductive Character Displacement versus Reinforcement
Terminology
A Unifying Principle
Summary
Further Reading
Box 1.1: Alternative Manifestations of Character Displacement
Box 1.2: Suggestions for Future Research

2. Why Character Displacement Occurs

Introduction
Why Ecological Character Displacement Occurs
RESOURCE COMPETITION
COMPETITIVE EXCLUSION
SPECIES COEXISTENCE
RESOURCE PARTITIONING VIA CHARACTER DISPLACEMENT VS. SPECIES SORTING
Why Reproductive Character Displacement Occurs
REPRODUCTIVE COMPETITION
REPRODUCTIVE EXCLUSION
REPRODUCTIVE PARTITIONING VIA CHARACTER DISPLACEMENT VS. SPECIES SORTING
Summary
Further Reading
Box 2.1: Alternative Models of Species Coexistence
Box 2.2: Is Competitively
Induced Plasticity Character Displacement?
Box 2.3: Suggestions for Future Research

3. When Character Displacement Occurs

Introduction
Facilitators of Character Displacement
STANDING VARIATION
STRONG SELECTION
ECOLOGICAL OPPORTUNITY
LACK OF ANTAGONISTIC GENETIC CORRELATIONS
GENE FLOW
INITIAL DIFFERENCES
Variation in the Expression of Character Displacement
How Ecological and Reproductive Character Displacement Facilitate Each Other
ECOLOGICAL DIVERGENCE AS A FACILITATOR OF REPRODUCTIVE DIVERGENCE
REPRODUCTIVE DIVERGENCE AS A FACILITATOR OF ECOLOGICAL DIVERGENCE
WHY ONE FORM IS NECESSARY TO FACILITATE THE OTHER
How Ecological and Reproductive Character Displacement Can Impede Each Other
Summary
Further Reading
Box 3.1: Suggestions for Future Research

4. How Character Displacement Unfolds

Introduction
Mechanisms of Divergence
GENETICALLY CANALIZED DIVERGENCE
ENVIRONMENTALLY INDUCED DIVERGENCE
Tempo and Mode of Character Displacement
HOW MECHANISMS DIFFER IN SPEED OF DIVERGENCE
THE PLASTICITY-FIRST HYPOTHESIS
EMPIRICAL TESTS OF THE PLASTICITY-FIRST HYPOTHESIS
Summary
Further Reading
Box 4.1: Suggestions for Future Research

5. Diversity and Novelty Within Species

Introduction
How
Intraspecific Character Displacement Works

Intraspecific Character Displacement: Observational Evidence

Intraspecific Character Displacement: Experimental Evidence
Evolution of Alternative Phenotypes
FREQUENCY-DEPENDENT DISRUPTIVE SELECTION AND THE EVOLUTION OF
ALTERNATIVE PHENOTYPES
EVOLUTION OF RESOURCE POLYMORPHISM
EVOLUTION OF MATING POLYMORPHISM

Intraspecific Character Displacement and Species Diversity
Character Displacement Within Versus Between Species
Summary
Further Reading
Box 5.1: Suggestions for Future Research

6. Ecological Consequences

Introduction
Evolution of the Niche
Partitioning of Resources and Reproduction: A Reprise
Community Organization
Character Displacement and Darwinian Extinction
Species Distributions and Geographic Mosaics
Character Displacement and Species Ranges
Summary
Further Reading
Box 6.1:
Individual Variation and the Coexistence of Species
Box 6.2: Suggestions for Future Research

7. Sexual Selection

Introduction
How Sexual Selection Works
How Character Displacement Affects Sexual Selection
EFFECTS OF PHENOTYPIC SHIFTS
EFFECTS OF HABITAT SHIFTS
Implications of Character Displacement’s Effects on Sexual Selection
How Sexual Selection Affects Character Displacement
A Cautionary Note: Process Versus Pattern
Summary
Further Reading
Box 7.1: Suggestions for Future Research

8. Speciation

Introduction
What are Species?
How are Species Boundaries Maintained?
Evolution of Isolating Mechanisms
Character Displacement’s Role in Speciation
HOW CHARACTER DISPLACEMENT FINALIZES SPECIATION
HOW CHARACTER DISPLACEMENT INITIATES SPECIATION
HOW INTRASPECIFIC CHARACTER DISPLACEMENT INITIATES SPECIATION
Summary
Further Reading
Box 8.1: Selection and the Evolution of Reproductive Isolation
Box 8.2: Suggestions for Future Research

9. Macroevolution

Introduction
Competition in the Fossil Record
Methods for Studying Macroevolution: Rewinding the Tape of Life
Adaptive Radiation
SPECIES PROLIFERATION
DIVERGENT EVOLUTION
Evolutionary Escalation
Macroevolution: Red Queen or Court Jester?
Summary
Further Reading
Box 9.1: Suggestions for Future Research

10. Major Themes and Unsolved Problems

Introduction
Major Themes of the Book
CHARACTER DISPLACEMENT IS A PROCESS, NOT A PATTERN
CHARACTER DISPLACEMENT CAN PRODUCE DIFFERENT FORMS OF TRAIT EVOLUTION
ECOLOGICAL AND REPRODUCTIVE CHARACTER DISPLACEMENT INTERACT
PHENOTYPIC PLASTICITY CAN MEDIATE CHARACTER DISPLACEMENT
CHARACTER DISPLACEMENT PROMOTES DIVERSIFICATION AT MULTIPLE LEVELS
CHARACTER DISPLACEMENT AND SEXUAL SELECTION INTERACT
CHARACTER DISPLACEMENT HAS MACROEVOLUTIONARY IMPLICATIONS
Some Unsolved Problems
Summary

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