Mate Choice: The Evolution of Sexual Decision Making from Microbes to Humans

by Gil Rosenthal

Overview

A major new look at the evolution of mating decisions in organisms from protozoans to humans 

The popular consensus on mate choice has long been that females select mates likely to pass good genes to offspring. In Mate Choice, Gil Rosenthal overturns much of this conventional wisdom. Providing the first synthesis of the topic in more than three decades, and drawing from a wide range of fields, including animal behavior, evolutionary biology, social psychology, neuroscience, and economics, Rosenthal argues that "good genes" play a relatively minor role in shaping mate choice decisions and demonstrates how mate choice is influenced by genetic factors, environmental effects, and social interactions.

Looking at diverse organisms, from protozoans to humans, Rosenthal explores how factors beyond the hunt for good genes combine to produce an endless array of preferences among species and individuals. He explains how mating decisions originate from structural constraints on perception and from nonsexual functions, and how single organisms benefit or lose from their choices. Both the origin of species and their fusion through hybridization are strongly influenced by direct selection on preferences in sexual and nonsexual contexts. Rosenthal broadens the traditional scope of mate choice research to encompass not just animal behavior and behavioral ecology but also neurobiology, the social sciences, and other areas.

Focusing on mate choice mechanisms, rather than the traits they target, Mate Choice offers a groundbreaking perspective on the proximate and ultimate forces determining the evolutionary fate of species and populations.

Product Details

ISBN-13:	9780691150673
Publisher:	Princeton University Press
Publication date:	07/18/2017
Pages:	648
Product dimensions:	6.40(w) x 9.20(h) x 1.80(d)

About the Author

Gil G. Rosenthal is professor of biology and of ecology and evolutionary biology at Texas A&M University. He is codirector of the CICHAZ field station in central Mexico.

Read an Excerpt

CHAPTER 1

Mate Choice and Mating Preferences

AN OVERVIEW

1.1 INTRODUCTION

Hiking in the eucalyptus woods of northern Australia, we might come upon an odd structure with a promenade of shells and bones leading up to a curving, symmetric arch. We might reasonably speculate that we have stumbled upon an indigenous ceremonial site, or perhaps a contemporary art installation (fig. 1.1a). Diving off Japan's Okinawa Prefecture, we come upon a similar structure — an "alien crop circle" in the popular media (fig. 1.1b). We are astonished when we discover that the architects were a male great bowerbird (Ptilonorhynchus nuchalis) and a male pufferfish (Torquigener sp.), and that these structures only function in the context of courtship and mating. As amazed as we are by the structures' builders, we should be awestruck by the aesthetics of the females they were built to impress. How intricate their aesthetics, how exacting their desires, must be in order to drive males to such cognitive and physical extremes? Why do females even bother to choose males on the basis of these structures, rather than simply mating at random?

Mating is an expensive, risky, and intimate interaction, and over an individual's lifetime one expends time and energy on facilitating some matings, and time and energy on avoiding others. Who a chooser mates with and who she pairs with will affect how long she lives and how many healthy children and grandchildren she has. Mate choice determines which sperm fuse with which eggs, and therefore ultimately shapes how lineages split apart or merge together. It can drive the evolution of elaborate traits that hinder critical tasks like finding food and avoiding predators, in direct opposition to natural selection. The role of mate choice in both reproductive isolation among species and in sexual selection made it a key concept in Darwin's Origin of Species (1859). There was widespread skepticism over his conjecture that mating preferences — a "taste for the beautiful," in Darwin's memorable phrasing — could explain the seeming paradox of so much exuberant scent, texture, and sound in nature. Accordingly, he devoted the bulk of his next major work, The Descent of Man, and Selection in Relation to Sex (1871), to making the case for the central evolutionary role of sexual selection, particularly via mate choice.

Almost a century and a half later, mate choice continues to present a unique problem in evolutionary theory. Like predators coevolving with their prey, or hosts with their parasites, those courting and those choosing form a feedback loop, where chooser decisions can select for particular courter behavior and vice versa. In the case of mate choice, however, the same genome influences the behavior of both actors, and the interests of both are partly aligned and partly in conflict (Arnqvist & Rowe 2005). This kind of dynamic can lead to rapid evolution of elaboration of signals and choices within a species, which can lead to marked diversity of such signals and choices between species. Such divergent mate-choice patterns are often a prerequisite for reproductive barriers among species. Both the formation of new species, and the blending together of species via hybridization, depend on individual mate-choice decisions.

The study of mate choice is both fueled and complicated by its importance to our everyday experience. Mate choice forms our human identity: we are who we are because of a chain of highly improbable reproductive decisions, and our lives are in no small part defined by the people we desire, those with whom we have sexual relationships, and those with whom we reproduce. Our decisions to do so are regulated, to varying degrees in different times and places, by families, communities, and governments; few things are more painful than having our choices thwarted or overridden. It is hard to imagine music, prose, and poetry without love, jealousy, or heartache. And when we court each other and choose each other by starlight, we do so to the soundtrack of crickets and frogs doing the same. Mate choice surrounds us.

It is easy to make the case that mate choice is important, but how it actually evolves and how it actually works remains essentially mysterious. We are at a loss to explain much of the beauty in the world, from birdsong to the palette of colors on a coral reef, because we know that these things arise from mate choice, but we are still striving to understand how. We don't understand why choosers pay attention to so many different things or how they integrate information into a unitary decision to mate. Perhaps most visibly, we still fail to agree on the importance of adaptive processes in mate choice. My first scholarly exposure to mate choice was in the fall of 1993, in a freshman seminar on "Sex and Evolution" led by Jae Choe. At the time, the field was consumed by a debate about the extent to which an individual's mate-choice decisions impact the "genetic quality" of her offspring. Two decades later, we remain mired in, and limited by, the argument of whether or not mate choice is optimally designed to pick mates bearing "good genes."

There are at least three reasons why the conversation hasn't changed much over a generation. The first reason is that work on mate choice is hard to do; the core of mate-choice research involves inferring and predicting mating decisions indirectly and/or over long timescales. This is because mate choice as a phenotype is inherently slippery; we're usually measuring behavioral decisions, which are inherently contingent on the stimuli presented, and can only be measured indirectly. We can readily measure the spectral reflectance of the components of a bower and calculate how they catch the sunlight over the course of a day, but it's much more challenging to measure how these components influence the likelihood that a female will mate with the male who produced it. The next chapter deals with the technical challenges of measuring mate choice.

The second reason is the Balkanization of our approaches to studying mate choice. Those who study humans are generally associated with entirely different disciplines (anthropology and social and evolutionary psychology) than the majority of their colleagues working on non-humans (biology and its subfields, as well as comparative psychology). Biologists, moreover, are further subdivided into quantitative geneticists, behavioral ecologists, ethologists, and behavioral neuroscientists. The massive literature on mate choice is a mixed blessing, since it makes it difficult for any individual to have in-depth knowledge of more than one of these areas. A major goal of this book is to bring these fields together toward a synthetic understanding of mate choice.

The third and perhaps principal reason for the field's slow progress is that we have always thought about mate choice primarily in terms of its functional consequences. Starting with Darwin (The Descent of Man, and Selection in Relation to Sex, 1871) and sexual psychologist Havelock Ellis (Sexual Selection in Man, 1905), and continuing on to the present (Andersson, Sexual Selection, 1994; Eberhard, Female Control: Sexual Selection by Female Choice, 1996; Arnqvist & Rowe, Sexual Conflict, 2005), the focus has not been on mate choice as an intricate psychological and behavioral process in its own right, but on mate choice as an agent of sexual selection. Evolutionary models sometimes rely on fanciful assumptions about mechanisms; conversely, empirical studies of mechanism frequently assume optimal design. Conversely, to the extent that those who study mate-choice mechanisms think about fitness consequences, they often assume these mechanisms are systems optimally designed to maximize the benefits of mate choice to choosers, rather than systems cobbled together from available genetic variation that sometimes lead choosers astray. It is tempting to think of choosers as actuaries, evaluating expected lifetime fitness, and taxonomists, recognizing conspecifics and heterospecifics, and executing each of these tasks both perfectly and separately. Yet relatively little attention is paid to how mate choice actually works, although this is crucial to understanding both how it evolves and how it imposes selection. How does a female bowerbird actually experience her choices (fig. 1.1c)? Our focus on courter traits, rather than chooser preferences, has produced some stumbling blocks for evolutionary theory: one important example is that the predictions of most sexual selection models depend entirely on whether the net direct benefits of mate choice are positive or negative, yet we seldom measure this directly. What is total selection on mate choice, and how does it affect the way preferences and sampling strategies evolve?

The standard approach in the mate-choice literature is to begin by reviewing theoretical and conceptual models, then discussing empirical evidence in light of the theory. Inspired by Darwin's inductive approach in the Origin and the Descent, I have attempted to turn this approach upside down and interpret theory in light of what we know about how mate choice works. Accordingly, I focus this first section of the book on natural history — a broad description of the mechanisms, ontogeny, and phenotypic expression of mating preferences and mate choice. I have deliberately chosen my language to minimize a priori assumptions about any adaptive functions of choosing particular mates over others. In the second section, I use this perspective to address how mate choice evolves and acts as an agent of selection, and how it generates fitness consequences for individuals and evolutionary consequences for populations and species.

Part of the challenge of studying mate choice arises from the enormous scope of mate choice as a phenomenon. The contemporary literature on mate choice is immense. Choice can range from the simplicity of a single-celled protozoan exchanging genes only with another individual emitting a particular signaling molecule, through the protracted mutual courtship of humans and other vertebrates. What these vastly different mechanisms have in common is that they impose variation in the mating success of the individuals being chosen — courters. Preferred courters will, by definition, have an advantage over unpreferred ones (but see Long et al. 2009 for a counterexample).

By contrast, the magnitude and direction of mate choice's benefits to choosers is hugely variable, and while sophisticated mate-choice mechanisms offer more opportunity for nuanced evaluation and comparison, they also offer greater entry for subversion and deceit. Some of the mechanisms involved in mate choice, like the tuning of peripheral sensory receptors, are universal among organisms. Other mechanisms, such as selective attention to particular traits, are highly labile among species, within species, and even within individuals. A recurring theme of this book is the importance of the processes promoting and maintaining within-population variation in mate choice.

Like the mechanisms used for mate choice, the ecological theater of mate choice spans the full range of natural history. Mate choice occurs in everything from parrots that grow up with both parents, to parrotfish that are cast off into the plankton as fertilized eggs. There is mate choice among anglerfish in the deep ocean that encounter mates so rarely that when they do, males permanently attach to females, their circulatory systems fusing together; and there is mate choice among crickets in noisy choruses, surrounded by thousands of courters and choosers. Both the mechanisms constituting mate choice and the selective pressures shaping it are thus as variable as can be among taxa. The diversity of mate-choice mechanisms provides the potential for wonderful natural experiments, but these are again limited by the difficulties inherent in measuring choice. One person can easily go to museums and measure a morphological trait in a hundred species. An individual research lab working on mate choice can manage at most a handful of species with similar maintenance needs. Accordingly, taxonomic clustering adds to the intellectual Balkanization of mate choice. Social-context effects on mating (chapter 6) are one example. Nearly all studies of sexual reward come from one rodent species, and nearly all studies of mate-choice copying come from one fish family and one bird species. With different model systems come different constraints as to what we can measure, different traditions of what's important to think about, and different networks of researchers. This book attempts to bring these approaches together and survey mate choice across taxa (including humans), striving to avoid being too biased by my own inordinate fondness for livebearing fishes.

Attempts to fit mate choice between two covers are, perhaps sensibly, few and far between. Since Bateson's (1983) eponymous edited volume on mate choice, we have gained considerable ground in understanding sensory, perceptual, and cognitive mechanisms, and in understanding the evolutionary causes and consequences of choice. Across fields, the literature on mate choice has exploded. The aim of this book is to present a conceptually unified approach to thinking about what Darwin termed the "taste for the beautiful." It is not intended to be an exhaustive review of the literature, particularly since any such effort would be both redundant with the Internet and obsolete by the time of publication. I have attempted to synthesize the work of hundreds of people, but the papers I cite are probably biased by my taxonomic and geographic parochialism (Wong & Kokko 2005). I have tried to abide by the late Stephen Jay Gould's (1994, p. 164) maxim that erroneous ideas are useful, since they can invigorate science by stimulating new avenues of thought, while misleading facts are corrosive. Therefore, I have endeavored to be meticulous in terms of characterizing my sources, but have allowed myself some qualified speculation in the hopes of generating new conversations about mate choice. Nevertheless, I am a tourist to many of the subdisciplines involved, and although I have made an effort to have each chapter read by at least one expert colleague, the book surely retains mistakes and misconceptions that are entirely my own.

In this chapter, I begin by describing a basic framework for thinking about mate choice and mate preferences, and then provide an outline for how the book attempts to address key questions about how they work, how they evolve, and how they act simultaneously as targets and agents of selection.

1.2 WHAT IS MATE CHOICE?

It is possible therefore that the emotional reactions aroused by different individuals of the opposite sex will, as in man, be not all alike, and at the least that individuals of either sex will be less easily induced to pair with some partners than with others. With plants an analogous means of discrimination seems to exist in the differential growth rate of different kinds of pollen in penetrating the same style.

— Fisher (1930, p. 143)

One of the challenges of learning cell biology or neuroanatomy is the sheer amount of new vocabulary it entails. Students are overwhelmed by trying to keep the anterior cingulate cortex straight from the torus semicircularis. Animal behavior, by contrast, tends to assign specialized meaning to ordinary terms: while this makes them more accessible to a broad audience, it can lead to semantic confusion and anthropomorphism. Further, different authors use myriad terms to describe comparable processes. Edward (2015) provides a comprehensive review of the terminology surrounding mate choice and mating preferences. This book is biased toward multicellular animals with neurally mediated behavior, to which some authors prefer to restrict the term "choice." But neither sensory perception nor neural processing are required for a mechanism that discriminates among potential mates. Most contemporary scientists (Edward 2015; Kokko et al. 2003; Servedio & Bürger 2014) use variations on Halliday's (1983, p. 4) definition, which extends mate choice to a broad range of mechanisms in even the simplest creatures:

Mate choice can be operationally defined as any pattern of behavior, shown by members of one sex, that leads to their being more likely to mate with certain members of the opposite sex than with others.

(Continues…)

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Table of Contents

Preface xi

PART 1. MECHANISMS

Chapter 1. Mate Choice and Mating Preferences:

An Overview

1.1 Introduction 3

1.2. What is mate choice? 10

1.3. Choosers and courters, not females and males 11

1.4. Mate choice is distinct from sexual selection 12

1.5. Preference and antipathy underlie realized mate choices 13

1.6. Preference functions 15

1.7. Stages of mate choice 23

1.8. Mate choice as a problem in animal communication 26

1.9. Prospectus 29

1.10. Additional reading 30

Chapter 2. Measuring Preferences and Choices

2.1. Introduction 31

2.2. Measuring mate choice using mating outcomes 33

2.3. Empirical assays of preference: where to begin 35

2.4. Measures of preference 35

2.5. Stimuli used in preference assays 41

2.6. Repeatability of preferences 47

2.7. Sequential versus simultaneous assays 48

2.8. Other concerns with study design and interpretation 51

2.9. Synthesis: measuring mate choice and mating preferences in the twenty-first century 53

2.10. Additional reading 56

Chapter 3. The First Steps in Mate Choice: Preference Functions and Sensory Transduction

3.1. Introduction 57

3.2. Common features of sensory systems 63

3.3. Chemoreception 75

3.4. Vision 78

3.5. Hearing 80

3.6. Other modalities 83

3.7. Sensory constraints on mating preferences 85

3.8. Synthesis 89

3.9. Additional reading 89

Chapter 4. Beyond the Periphery: Perception, Cognition, and Multivariate Preferences

4.1. Introduction 91

4.2. Mechanisms of perceptual integration 101

4.3. Categorical perception 107

4.4. Integration rules for complex preferences 110

4.5. Synthesis: complex preferences as integrated phenotypes 116

4.6. Additional reading 120

Chapter 5. Aesthetics and Evaluation in Mate Choice

5.1. Introduction: “A taste for the beautiful” 121

5.2. Universals of beauty? 123

5.3. Detection and evaluation as distinct components of mate choice 126

5.4. Mechanisms of evaluation 130

5.5. Evaluative mechanisms and perception are related: “beauty in the processing experience” 137

5.6. Plasticity and evolvability of evaluative mechanisms 137

5.7. Additional reading 138

Chapter 6. From Preferences to Choices: Mate Sampling and Mating Decisions

6.1. Introduction 139

6.2. The biological context of mate choice 142

6.3. Mate sampling algorithms in theory and practice 148

6.4. Sequential and static: fixed-threshold rules 148

6.5. Sequential and dynamic: adjustable thresholds 149

6.6. Simultaneous and static: comparative evaluation and (in)transitivity 158

6.7. Simultaneous and dynamic: best-of- n, comparative Bayes, and random walk 163

6.8. Sampling multiple traits 165

6.9. Recognition 166

6.10. Executing choices 167

6.11. The marginal cost of sampling and choice 169

6.12. Synthesis 171

6.13. Additional reading 173

Chapter 7. Mate Choice During and After Mating

7.1. Introduction 174

7.2. Remating and choice of multiple mates 177

7.3. Biasing fertilization 179

7.4. Resource allocation to offspring 191

7.5. Mate choice across stages: premating decisions and cryptic choice 194

7.6. Synthesis: what is different about cryptic choice? 196

7.7. Additional reading 200

Chapter 8. Mutual Mate Choice

8.1. Introduction 201

8.2. Reciprocal preferences 202

8.3. Social promiscuity and mutual mate choice 205

8.4. Pairing decisions: finding a social mate 213

8.5. Pair bonding 220

8.6. Mate choice in hermaphrodites 225

8.7. Synthesis 225

8.8. Additional reading 227

Chapter 9. Variation in Preferences and Choices: General Considerations

9.1. Overview 228

9.2. Scales of variation 231

9.3. Repeatability 232

9.4. Covariates of preference variation 251

9.5. Same-sex sexual behavior 260

9.6. Synthesis 261

9.7. Additional reading 262

Chapter 10. Variation I: Genetics

10.1. Overview 263

10.2. Interspecific genetic differences 265

10.3. Genetic mapping 268

10.4. Genetic variation in natural populations 270

10.5. The genetic architecture of mating preferences 279

10.6. Functional characterization of preference genes 284

10.7. Synthesis 286

10.8. Additional reading 287

Chapter 11. Variation II: Biotic and Abiotic Environment

11.1. Introduction 288

11.2. Context-sensitive effects 288

11.3. State-dependent preferences 290

11.4. Genotype-by-environment interactions 299

11.5. Synthesis 304

11.6. Additional reading 305

Chapter 12. Variation III: Social Environment and Epigenetics

12.1. Introduction 306

12.2. Social effects before birth: epigenetic and parental effects 307

12.3. Social status before and after maturity 312

12.4. Early learning: impacts on preferences 313

12.5. Mechanisms of early learning 318

12.6. Variation in early learning 324

12.7. Social experience after sexual maturity 327

12.8. Nonindependent mate choice and copying 328

12.9. Genotype by environment revisited: the instinct to learn 332

12.10. Synthesis 335

12.11. Additional reading 338

PART 2. ORIGINS, EVOLUTION, AND CONSEQUENCES

Chapter 13. Origins and Histories of Mating Preferences: Chooser Biases

13.1. Introduction 341

13.2. Preferences have histories 346

13.3. Perceptual biases 348

13.4. Biases from non-choice functions 350

13.5. Novel responses of preference mechanisms 352

13.6. Byproduct biases: novel biases shaped by current signals 353

13.7. Synthesis 354

13.8. Additional reading 357

Chapter 14. Selection on Mate Choice and Mating Preferences

14.1. Introduction 358

14.2. Selection on preferences for courter traits 359

14.3. Evolution of choosiness and mate-sampling strategies 372

14.4. When to choose: pre-versus postmating 378

14.5. Evolution of plastic preferences 381

14.6. Constraints on preference evolution 383

14.7. Coercion and choice 384

14.8. Synthesis 385

14.9. Additional reading 387

Chapter 15. Dynamic Evolution of Preferences, Strategies, and Traits

15.1. Introduction 388

15.2. Genetic covariance drives preference evolution: the Fisher-Lande-Kirkpatrick null model 389

15.3. Constraints on genetic covariance: (mis)alignment of preferences and traits 396

15.4. Adaptive coevolution 402

15.5. Mode of transmission and preference-trait coevolution 410

15.6. The limits of indirect selection 412

15.7. Mate choice in context: social and life history evolution 419

15.8. Compatibility and epistasis 424

15.9. Mate choice as an agent of trait evolution 426

15.10. Population-level consequences of mate choice 428

15.11. Coevolution of multiple traits and preferences 431

15.12. Synthesis: a unified view of preference evolution 434

15.13. Additional reading 437

Chapter 16. Mate Choice, Speciation, and Hybridization

16.1. Introduction 439

16.2. Divergence of preferences among isolated populations 440

16.3. Divergence of preferences with secondary contact 444

16.4. Reinforcement and speciation with gene flow 450

16.5. Conspecific mate preference and intraspecific mate choice 461

16.6. Mate choice and genetic exchange 462

16.7. Synthesis 471

16.8. Additional reading 472

Chapter 17. Mate Choice and Human Exceptionalism

17.1. Introduction 473

17.2. Social influences on human mating decisions 476

17.3. Variation in human mating preferences 478

17.4. Synthesis: integrating evolutionary and social-science approaches to human sexuality 480

17.5. Additional reading 481

Chapter 18. Conclusions: A Mate-Choice View of the World

18.1. The sweep of mate choice 482

18.2. From sexual selection to preference evolution 483

18.3. How we talk about mate choice 484

18.4. How we study mate choice 485

18.5. Four open questions about mate-choice mechanisms 486

18.6. Mate choice and total selection 488

18.7. Synthesis: mate choice and its consequences 492

Glossary 493

Literature Cited 505

Subject Index 617

Taxonomic Index 629

What People are Saying About This

From the Publisher

"This book is a marvelously insightful, thought-provoking, and stimulating synthesis of mate choice. Drawing on information from the fields of animal behavior, ecology, evolutionary genetics, and sensory physiology, it will be a source of information and inspiration for everyone interested in this fascinatingly complex topic."—Rosemary Grant, coauthor of 40 Years of Evolution: Darwin's Finches on Daphne Major Island

"At once encyclopedic, idiosyncratic, and illuminating—a wonderful book to dip into."—Monique Borgerhoff Mulder, coauthor of Conservation: Linking Ecology, Economics, and Culture

"This book takes an interesting and substantial look at mate choice and will become a new reference on the topic. With its exhaustive references, broad taxonomic coverage, and fresh direction, this important work is a major, significant contribution to the field."—Richard O. Prum, Yale University

"Taking on the enormous field of mate choice, Gil Rosenthal reviews and curates research from neurobiology and endocrinology through psychology and evolutionary genetics to produce a towering work. An indispensable resource for students of animal behavior and evolution, this comprehensive and thoughtful book will anchor the study of mate choice for decades to come."—Robert Brooks, University of New South Wales, Australia

Editorial Reviews

"Mate Choice represents an ambitious synthesis of our current understanding of sexual selection in a broad range of life forms. . . . The book provides a clear synthesis of the state of affairs in the study of mate choice and related fields."

Science

"Rosenthal does an admirable job refocusing decades of work mostly concerned with the effects of (primarily female) mate choice on (primarily male) behavior, physiology, and morphology."—-David A. Gray, Quarterly Review of Biology

From the Publisher

"Mate Choice represents an ambitious synthesis of our current understanding of sexual selection in a broad range of life forms. . . . The book provides a clear synthesis of the state of affairs in the study of mate choice and related fields."

Science