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CONTENTS
List of Contributors ix
Introduction to Human Mating Strategies 1
David M. Buss
Part I • Theoretical Perspectives
1. Writing Trivers’s 1972 Theory of Parental Investment and Sexual Selection 11
Robert Trivers
2. Sexual Selection and the Animal’s Mating Mind 16
Michael J. Ryan
3. The Interface of Sexual Selection, Conflict, and Evolutionary Psychology: Emerging Core Themes 33
Jennifer C. Perry and Tracey Chapman
4. Extensions of Sexual Strategies Theory across Peoples, Cultures, and Ecologies 66
David P. Schmitt
Part II • Attraction and Mate Selection
5. The Early Stages of Mate Selection 121
Norman P. Li and Bryan K. C. Choy
6. Computational Models of Mate Choice 154
Daniel Conroy-Beam
7. The Logic of Physical Attractiveness: What People Find Attractive, When, and Why 178
David M. G. Lewis, Kortnee C. Evans, and Laith Al-Shawaf
8. Incest Avoidance Adaptations: Evolved Function and Proximate Mechanisms 206
Debra Lieberman and Carlton Patrick
9. Parental Influence over Mate Choice 222
Menelaos Apostolou
10. Beyond Sex: Reproductive Strategies as a Function of Local Sex Ratio Variation 240
Ryan Schacht and Caroline Uggla
11. Mating Strategies in Sexually Egalitarian Cultures 262
Leif Edward Ottesen Kennair, Trond Viggo Grøntvedt, Andrea M. Kessler, Steven W. Gangestad, and Mons Bendixen
12. Mating Strategy Variation by Sexual Orientation 286
David A. Frederick, Jenna C. Alley, Scott Semenyna, and Justin R. Garcia
Part III • Mate Competition
13. Contest Competition for Mates and the Evolution of Human Males 317
David Puts, David Carrier, and Alan R. Rogers
14. An Evolutionary Review of Female Intrasexual Competition 378
Maryanne L. Fisher and Jaimie Arona Krems
15. Mate Competition between the Sexes: Evidence from Two Non-Western Cultures 404
Scott W. Semenyna, Francisco R. Gómez Jiménez, and Paul L. Vasey
Part IV • Pair-Bonded Relationship Dynamics
16. Evolving Connections: Attachment and Human Mating Strategies 427
Gurit E. Birnbaum
17. Archaeology of love: A Review of the Ethnographic Exploration of Love around the World 447
William Jankoviak and Alex J. Nelson
18. Marital and Sexual Satisfaction 466
Andrea L. Meltzer
19. Sex Differences in Jealousy: The State of the Theory 483
John E. Edlund, Brad J. Sagarin, and Kristyn M. Kinner
20. Mate Guarding 502
Valerie G. Starratt and Todd K. Shackelford
Part V • Sexual Conflict in Mating
21. Deception in Human Mating 515
Gayle Brewer
22. Marriage and Monogamy in Cross-Cultural Perspective 531
Brooke A. Scelza
23. Sperm Competition 555
Valerie G. Starratt and Todd K. Shackelford
24. Violent Mates 566
Joshua D. Duntley
25. The Dark Triad Traits and Mating Psychology 590
Peter K. Jonason and Vlad Burtaverde
26. Sexual Harassment 606
Kingsley R. Browne
27. Sexual Coercion 629
Joseph A. Camilleri
28. Women’s Avoidance of Sexual Assault 648
Rachel M. James, Melissa M. McDonald, and Viviana Weekes-Shackelford
Part VI • Mating and Endocrinology
29. Hormones and Human Mating 667
James R. Roney
30. Understanding Women’s Estrus and Extended Sexuality: The Dual Sexuality Framework 700
Steven W. Gangestad, Tran Dinh, Lauren Lesko, and Martie G. Haselton
31. Ovulatory Cycle Effects and Hormonal Influences on Women’s Mating Psychology 739
Julia Stern and Lars Penke
32. The Impact of Hormonal Contraceptives on Women’s Sexual and Mating Psychology 756
Katja Cunningham and Sarah E. Hill
Part VII • Mating in the Modern World
33. Mating in the Digital Age 777
Helen E. Fisher and Justin R. Garcia
34. Popular Culture and Human Mating: Artifacts of Desire 796
Catherine A. Salmon and Rebecca L. Burch
35. Evolutionary Mismatch and Human Mating: Understanding the Mating Mind in the Modern World 814
Cari D. Goetz
Index 833
LIST OF CONTRIBUTORS
Jenna C. Alley, Ph.D.
University of California, Los Angeles
Laith Al-Shawaf, Ph.D.
University of Colorado
Menelaos Apostolou, Ph.D.
University of Nicosia
Mons Bendixen, Ph.D.
Norwegian University of Science and Technology (NTNU)
Gurit E. Birnbaum, Ph.D.
Reichman University (IDC Herzliya)
Gayle Brewer, Ph.D., Ed.D.
University of Liverpool
Kingsley R. Browne, M.A., J.D.
Wayne State University
Rebecca L. Burch, Ph.D.
State University of New York at Oswego
Vlad Burtaverde, Ph.D.
University of Bucharest
David M. Buss, Ph.D.
University of Texas, Austin
Joseph A. Camilleri, Ph.D.
Westfield State University
David Carrier
University of Utah
Tracey Chapman, Ph.D.
University of East Anglia
Bryan K. C. Choy, M.Phil.
Singapore Management University
Daniel Conroy-Beam, Ph.D.
University of California, Santa
Barbara
Katja Cunningham, M.S.
Texas Christian University
Tran Dinh, M.A.
University of New Mexico
Joshua D. Duntley, Ph.D.
Stockton University
John E. Edlund, Ph.D.
Rochester Institute of Technology
Kortnee C. Evans, B.Sc.
Murdoch University
Helen E. Fisher, Ph.D.
The Kinsey Institute
Maryanne L. Fisher, Ph.D.
Saint Mary’s University
David A. Frederick, Ph.D.
Chapman University
Steven W. Gangestad, Ph.D.
University of New Mexico, Albuquerque
Justin R. Garcia, Ph.D.
Indiana University
Cari D. Goetz, Ph.D.
California State University San Bernardino
Francisco R. Gómez Jiménez, Ph.D.
University of Toronto Mississauga
Trond Viggo Grøntvedt, Ph.D.
Norwegian University of Science and Technology (NTNU)
Martie G. Haselton, Ph.D.
University of California, Los Angeles
Sarah E. Hill, Ph.D.
Texas Christian University
Rachel M. James, M.S.
Oakland University
William Jankowiak, Ph.D.
University of Nevada, Las Vegas
Peter K. Jonason, Ph.D.
University of Padua and Cardinal
Stefan Wyszynski University in Warsaw
Leif Edward Ottesen Kennair, Ph.D.
Norwegian University of Science and Technology (NTNU)
Andrea M. Kessler, M.Sc.
Norwegian University of Science and Technology (NTNU)
Kristyn M. Kinner, B.A.
Rochester Institute of Technology
Jaimie Arona Krems, Ph.D.
Oklahoma State University
Lauren Lesko
University of California, Los Angeles
David M. G. Lewis, Ph.D.
Murdoch University
Norman P. Li, Ph.D., M.B.A., M.A., B.A.
Singapore Management University
Debra Lieberman, Ph.D.
University of Miami
Melissa M. McDonald, Ph.D.
Oakland University
Andrea L. Meltzer, Ph.D.
Florida State University
Alex J. Nelson, Ph.D.
Appalachian State University
Carlton Patrick, J.D., Ph.D.
University of Central Florida
Lars Penke, Prof., Dr.
Georg August University Göettingen
Jennifer C. Perry, Ph.D., M.Sc., B.Sc.
University of East Anglia
David Puts, Ph.D.
Pennsylvania State University
Alan R. Rogers, Ph.D.
University of Utah
James R. Roney, Ph.D.
University of California, Santa
Barbara
Michael J. Ryan, Ph.D. University of Texas
Brad J. Sagarin, Ph.D.
Northern Illinois University
Catherine A. Salmon, Ph.D. University of Redlands
Brooke A. Scelza, Ph.D.
UCLA
Ryan Schacht, Ph.D.
East Carolina University
David P. Schmitt, Ph.D.
Brunel University London
Scott W. Semenyna, Ph.D.
Stetson University
Todd K. Shackelford, Ph.D.
Oakland University
Valerie G. Starratt, Ph.D.
Nova Southeastern University
Julia Stern, Ph.D.
University of Bremen
Caroline Uggla, Ph.D.
Stockholm University
Paul L. Vasey, Ph.D.
University of Lethbridge
Robert Trivers, Ph.D.
Rutgers University
Viviana Weekes-Shackelford, Ph.D.
Oakland University
Introduction to Human Mating Strategies
David M. Buss
Abstract
In sexually reproducing species, mating success is a non-negotiable requirement for evolutionary fitness. Consequently, selection has created a rich array of adaptations that are products of a long and unbroken line of human ancestors, each of whom succeeded in the complex game of mating. This Handbook showcases the current state of knowledge about those adaptations. These include mate preferences, tactics of attraction, forms of mate competition, tactics for dealing with sexual conflict, modes of mate retention, mate switching strategies, and many more. Chapters on the endocrinology of mating adaptations provide state-of-the-art knowledge about some of the key biological drivers. Chapters on mating in the modern world highlight key ways in which mating adaptations, forged over millions of years in environments long gone, get expressed in modern environments, sometimes creating evolutionary mismatches. This Handbook is not the final word on human mating strategies. Rather, it gives readers and researchers an impressive foundation of what is known and unknown, and importantly, a roadmap for future discoveries about what may be the most complex evolved psychology humans possess.
Key Words: human mating strategies, sexual selection, mate preferences, mate competition, evolutionary mismatches
The scientific study of human mating strategies is one of the major success stories of evolutionary psychology. The explosion of evolutionarily anchored theories and thousands of empirical studies of human mating is unique among the social sciences in at least two respects—the volume of hypothesis generation and the cumulative quality of the scientific empirical testing. This makes good theoretical sense. In all sexually reproducing species, evolutionary processes must all pass through the rigorous filters of successful mating. Survival is not enough. Each living human comes from a long and literally unbroken chain of ancestors, each of whom succeeded in selecting a mate, attracting a mate, being reciprocally chosen by that mate, navigating the complexities of sexual intercourse sufficient for conception, having a conceptus who survived the nine-month hurdles to be born, and after birth survived to reproductive age to begin the process anew.
Passing through these successive hurdles had to happen not just a dozen times but millions upon millions of iterations going back through the distant mists of human evolutionary history, our primate lineage, our mammalian lineage, and the origin of sexual reproduction itself more than a billion years ago. If any one of our ancestors had failed in any of these tasks, the chain would be irreparably broken and we would not be alive to read these pages. In this important sense, we are all evolutionary success stories. As descendants
of this unimaginably long line of forbears, each us carries with us the finely honed adaptations that led to our ancestors’ success. The current Handbook of Human Mating provides an up-to-date summary of the current state of the science of human mating—the modern theories, hypotheses, predictions, and empirical findings relevant to each.
Sexual Selection Theory
Sexual selection theory (Darwin, 1871) provides the most important theoretical framework for understanding the mating adaptations of sexually reproducing species (e.g., Andersson, 2019). Sexual selection centers on the evolution of adaptations not due to survival success but rather due to mating success. Darwin identified two causal processes by which mating success could be attained—intrasexual competition and preferential mate choice. The classic example of intrasexual competition is two male stags locking horns in combat. Winners in these physical contests gained preferential sexual access to females, and so passed on genes for attributes that led to their success such as greater strength, agility, speed, and perhaps fearlessness and bellicosity. The attributes of losers bit the evolutionary dust because they failed in this brutal game of mating. Contest competition turns out to have been an extremely important sexually selective process in humans (Puts et al., this volume).
The second process of sexual selection articulated by Darwin identified the evolution of mating success through preferential mate choice. If members of one sex preferred certain qualities in the other sex in mating contexts, then those who possessed the desired qualities were more frequently chosen. Over evolutionary time, if there exists some degree of consensus about the qualities desired and those qualities are partly heritable, then the desired qualities evolve or increase in frequency.
Although Darwin envisioned intrasexual competition as pertaining primarily to males and preferential mate choice pertaining primarily to females, when it comes to humans, both processes apply to both sexes, as the chapters in this Handbook document. Moreover, the modes of intrasexual competition in humans involve not just physical contests, although it’s clear that these have been important. Rather, arenas of intrasexual competition include tactics for navigating status hierarchies and the use of language to influence social perceptions of one’s own mating desirability and to impugn the reputation of intrasexual rivals (Buss & Dedden, 1990; Fisher & Krems, this volume).
Sexual selection theory itself has witnessed important theoretical developments since Darwin’s 1871 articulation of it (see Ryan, this volume). Trivers (1972), for example, furnished a major theoretical advance by identifying the relative parental investment of each sex as a key determinant of which sex does the competing and which sex does the choosing (see Trivers, this volume, on the personal context in which he developed his theory). Sexual selection theory has also expanded to include processes such as sperm competition (Starratt & Shackelford, this volume) and sexual coercion (see Camilleri, this volume).
The chapters in this volume showcase the “state of the art” of sexually selected human mating strategies and the underlying psychological adaptations that give rise to them.
Sexual Conflict Theory
Another critical theoretical development since Darwin’s time has been sexual conflict theory (Parker, 2006; Perry & Chapman, this volume). When the genetic interests of females and males diverge, sexual conflict will ensue. There exist many domains of sexual conflict in humans, zones in which the optimal mating strategy from a female perspective differs from the optimal mating strategy from a male perspective. It is sometimes in a male’s best interest to initiate sex sooner, or with less investment, compared to the optimal interests of the female. These differing fitness interests create sexually antagonistic arms races very much analogous to those that occur between predators and prey. Each sex evolves adaptations to influence the other to be closer to its own optimum, which creates counteradaptations or defenses in the other to resist that influence and to manipulate the other sex to closer to its own optimum. This form of sexually antagonist evolution is often perpetual.
The many chapters on sexual conflict in this volume highlight the theoretical utility of sexual conflict theory in guiding researchers to discoveries that were entirely unknown prior to this theoretical development. These include predictable forms of deception in mating (Brewer, this volume), infidelity and jealousy (Scelza, this volume), adaptations for sperm competition (Starratt & Shackelford, this volume), intimate partner violence (Duntley, this volume), various forms of sexual coercion (Brown, this volume; Camilleri, this volume) as well as women’s defenses against sexual coercion (James et al., this volume).
Sexual Strategies Theory
Social scientists, including psychologists, typically receive no training in evolutionary biology. Consequently, most were unaware of these key theoretical developments in evolutionary theory and their potential applicability to human mating. In the last half of the 1980s and early 1990s, this started to change. Cunningham (1986) launched experimental tests of the evolution of female beauty from an evolutionary perspective. Kenrick et al. published a paper documenting that social dominance increased the attractiveness of men as mates but did not increase the attractiveness of women (Sadalla et al., 1987). And Buss (1989) published the first large-scale cross-cultural tests of evolutionary hypotheses about sex differences in human mate preferences.
The first major attempt to develop a more comprehensive evolution-based psychological theory of human mating strategies came under the rubric “sexual strategies theory” (Buss & Schmitt, 1993). This theory, containing nine key premises and twenty-two empirical predictions, proposed that humans have evolved a menu of mating strategies, not a single mating strategy. It provided a task analysis of the different adaptive problems that women and men recurrently face in mating, cross-cut with the temporal dimension of short-term mating (e.g., casual sex and brief affairs) and long-term mating (e.g., marriage and other temporally enduring mating relationships). It proposed that women as well as men engage in short-term mating, but the adaptive challenges they face when pursuing this strategy
differ profoundly. The reproductive benefits to men of pursuing a short-term mating strategy are fairly straightforward, since men’s reproductive success is most heavily limited by the number of fertile sex partners they can attract. Consequently, sexual strategies theory predicted that men would desire a larger number of partners than women do, let less time elapse before seeking sexual intercourse, and possess a host of other psychological design features that would promote the success of a short-term mating strategy (e.g., the male sexual overperception bias, first predicted by Buss, 1994).
Although women generally cannot (and never could) increase their direct reproductive success through short-term mating since adding additional sex partners would rarely have resulted in more offspring, they could use short-term mating to obtain key adaptive benefits. According to sexual strategies theory, these might include (1) immediate access to resources, (2) assessing several men through trial runs to determine which would be a good long- term mate, (3) cultivating a backup mate for insurance should something go wrong with her long-term relationship, (4) using short-term mating as a tactic for “trading up” to a higher mate value partner, and perhaps (5) obtaining higher-quality genes (e.g., genes for good health) from an affair partner than she could obtain from her regular partner. In the intervening years since the publication of sexual strategies theory in 1993, a tremendous volume of research has focused on testing hypotheses and predictions based on these theoretical benefits (e.g., Greiling & Buss, 2000, on women’s perceptions of the benefits of short-term mating; Buss et al., 2017 on the mate-switching hypothesis; Gangestad et al., this volume, on the good genes hypothesis).
Sexual strategies theory also provided a task analysis of the adaptive challenges each sex faces when pursuing a long-term mating strategy. Women, for example, were hypothesized to face challenges such as (1) identifying men who are able to invest in them and their offspring, (2) identifying men who are willing to invest in them and their offspring, (3) identifying men able and willing to protect them (e.g., from sexual aggression from other men), (4) assessing men who give cues to long-term commitment to them, and (5) assessing men who give cues to “good dad” qualities linked with parenting skills. Men, while facing some of these adaptive challenges in selecting their mates for long-term mating such as commitment and good parenting, also had to solve additional sex-differentiated ones: (1) choosing women likely to be sexually faithful, thus solving the problem of paternity uncertainty (stemming from the fact that fertilization occurs internally within women), and (2) identifying women of high reproductive value (i.e., future reproductive capacity).
Since the 1993 publication of sexual strategies theory, a large body of empirical evidence has accumulated that supports many of the specific predictions generated by it (see Buss & Schmitt, 2019, for a review). Moreover, sexual strategies theory has been extended in new directions to include testing hypotheses across peoples, cultures, and ecologies (see Schmitt, this volume).
In this Handbook, multiple chapters showcase important theoretical developments and novel empirical extensions of the scientific understanding of human mating strategies. In the section “Attraction and Mate Selection,’ Li and his colleagues outline the logic and evidence of strategies in the early stages of mate selection. Conroy-Beam provides a novel computational model of mate selection that yields a sophisticated way of viewing the multidimensional process of mate selection. Lewis and colleagues provide a “state of the science” summary of theory and research on physical attractiveness using a cuebased approach. Lieberman and Patrick discuss theory and research on incest avoidance adaptations. Apostolou presents arguments and evidence for the importance of parents in influencing, and in some cases selecting, the mates of their daughters and sons. Schacht and Uggla highlight the importance of sex ratio, which surely varied tremendously across cultures and over time, on the mating strategies people pursue.
Kennair and colleagues discuss mating strategies in sexually egalitarian cultures such as Norway. Although some theories, such as traditional sex role theory, predict that sex differences should diminish or vanish in sexually egalitarian cultures, the data do not support those predictions. Indeed, some sex differences become larger, not smaller, in sexually egalitarian cultures. The concluding chapter in this section, by Frederick and colleagues, summarizes what is known about mating strategies as a function of individual differences in sexual orientation such as gay men, lesbian women, and bisexual individuals.
Pair-Bonded Relationship Dynamics
Once mate selection and mate attraction processes have been successfully implemented, complex dynamics occur within those who form long-term pair-bonded mating relationships. Birnbaum examines the role of attachment within pair-bonds. Jankoviak and colleague articulate the importance of love as universal phenomenon within long-term mateships. Meltzer explores the determinants of marital and sexual satisfaction within relationships. Edlund and colleagues examine the importance of jealousy within mateships, which some have argued is as central as love in human mating (Symons, 1979). Jealousy is an emotion often tied to mate guarding, the subject of the final chapter in this section, written by Starratt and Shackelford.
The Endocrinology of Human Mating
All mammals have complex endocrine systems that influence, and are influenced by, mating, and humans are no exception. These are sex-differentiated to an important extent. Reproductive-age women who are not on hormonal contraceptives, for example, experience predictable endocrinological changes as they progress through their ovulatory cycle. Roney kicks off this section by providing a broad overview of the state of the science on hormones and human mating. However, there is currently scientific controversy about the effects of the ovulation cycle on women’s mating strategies. Gangestad and colleagues argue that women possess a “dual mating strategy,” suggesting that women have not “lost
estrus” as many have argued, and moreover show preference and other mating strategy shifts depending on whether the odds of impregnation are high or low. Sterns and Penke, in contrast, argue that the cycle-phase shifts are more ephemeral or absent, according to large-scale attempts at replication. Resolution of this ongoing debate must await further research within this vibrant and cutting-edge area of the evolution of human mating. Concluding this section is a lively chapter by Cunningham and Hill who summarize the evidence on the effects of modern hormonal contraceptives on women’s sexuality and mating psychology.
Mating in the Modern World
The final section of the Handbook explores mating in the modern world, which has changed dramatically from the environment in which humans spent 99 percent of their evolutionary history. Helen Fisher and Justin Garcia explore mate choice in the digital age, with the dramatic surge in online dating and mating. Salmon and Burch examine popular culture in the modern world, including pornography, romance novels, and literature. Concluding this section is a chapter by Goetz, who outlines a number of key “mismatches” between the mating environments in which humans evolved and those they now inhabit.
I hope this Handbook provides a key reference for researchers and budding scientists who devote their efforts to uncovering the complexities of human mating. Biologist Theodosius Dobzhansky famously noted that “nothing in biology makes sense except in light of evolution.” It may not be too far a stretch to say that “nothing in human behavior makes sense except in light of human mating.”
Acknowledgements
This Handbook owes a great debt to Patrick Durkee, who offered suggestions throughout its creation and provided valuable feedback on a handful of chapters. Thanks also go to Joan Bossert, the editor at Oxford University Press who believed in the importance of this Handbook, and to Martin Baum, editor at Oxford University Press, who helped marshall the Handbook to completion and publication. Mostly I wish to thank the several dozen authors who wrote sterling chapters for this Handbook
References
Andersson, M. (2019). Sexual selection. Princeton University Press. (Original work published 1994)
Buss, D. M. (1989). Sex differences in human mate preferences: Evolutionary hypotheses tested in 37 cultures. Behavioral and Brain Sciences, 12(1), 1–14.
Buss, D. M. (2016). The evolution of desire: Strategies of human mating. Basic Books. (Original work published 1994)
Buss, D. M., & Dedden, L. A. (1990). Derogation of competitors. Journal of Social and Personal Relationships, 7(3), 395–422.
Buss, D. M., Goetz, C., Duntley, J. D., Asao, K., & Conroy-Beam, D. (2017). The mate switching hypothesis. Personality and Individual Differences, 104, 143–149.
Buss, D. M., & Schmitt, D. P. (1993). Sexual strategies theory: An evolutionary perspective on human mating. Psychological Review, 100(2), 204–232.
Buss, D. M., & Schmitt, D. P. (2019). Mate preferences and their behavioral manifestations. Annual review of psychology, 70, 77–110.
Cunningham, M. R. (1986). Measuring the physical in physical attractiveness: quasi-experiments on the sociobiology of female facial beauty. Journal of personality and social psychology, 50(5), 925–935.
Darwin, C. (1871). The descent of man and selection in relation to sex. Murray.
Greiling, H., & Buss, D. M. (2000). Women’s sexual strategies: The hidden dimension of extra-pair mating. Personality and individual Differences, 28(5), 929–963.
Parker, G. A. (2006). Sexual conflict over mating and fertilization: An overview. Philosophical Transactions of the Royal Society B: Biological Sciences, 361(1466), 235–259.
Sadalla, E. K., Kenrick, D. T., & Vershure, B. (1987). Dominance and heterosexual attraction. Journal of personality and social psychology, 52(4), 730–738.
Symons, D. (1979). The evolution of human sexuality. Oxford University Press.
Trivers, R. L. (1972). Parental investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man (pp. 136–179). Aldine. David M. Buss, August 9, 2021
Theoretical Perspectives
1 Writing Trivers’s 1972 Theory of Parental Investment and Sexual Selection
Robert Trivers
Abstract
A brief summary of the most wide-ranging paper of mine, covering the evolution of sex differences in all species. Especially novel is the application to differential mortality by sex, which varies widely across species and higher taxa. The paper provided a framework, anchored in sexual selection and parental investment, for discovering and explaining many sex differences in human mating strategies. The paper has become one of the most widely cited publications in evolutionary biology, accruing more than 17,000 scientific citations as of the year 2022. It is also one of the most widely cited papers in the mushrooming field of evolutionary psychology.
Key Words: Robert Trivers, parental investment, sexual selection, sex differences, mating
I have described in print and in detail (Trivers 2002) how I came to write this chapter so I will not go into great detail now. There were three parts: pigeon behavior (Drury), key logic (Mayr, Bateman, 1948), and also valuable sublogic (Williams). Were pigeon couples really monogamous with no internal conflict (ornithology); nonsense (Drury, personal communication, date); what was the underlying logic (parental investment (Bateman, 1948; Mayr) and sublogic (Williams, 1966).
The first was to see that the conflict-free monogamous bird family was a fantasy of bird scientists, supported by neither evidence nor logic. All you had to do was watch an actual bird couple—up close and personal—and you could see the truth. Why would a male force his partner (for life) into sleeping on the sloping roof every night instead of the gutter, where all the other pigeons slept including himself? Does it have anything to do with the fact that in the gutter next to her would be another “monogamous” male sitting close to his partner? It was Bill Drury who taught me this entire approach. And Bill did not joke around. When I invented a patently nonfunctional explanation for the function of a gull trait we were observing—side by side with binoculars—he told me “Never assume the animal you are studying is as stupid as the one studying him.” I was that stupid animal. Here is a more extensive description of Bill Drury and what he meant to me (Trivers 2002):
“Go Thou to the Pigeon”
After I had spent a year or so watching herring gulls and other sea birds with Bill Drury, I wanted to start a project on a species of my own, a species that I could study on land. I believe I suggested the lesser marsh wren, so to speak—that is, a species whose social behavior and ecology had not yet been studied, though something would be known about a closely related species. Drury immediately batted down that idea. He said it would take me eighteen months to find the species on a regular basis and another eighteen months to acclimate individuals sufficiently to me to permit detailed behavioral observations. That it had not yet been studied, he said, might better be taken as a warning than as an invitation. He suggested I go in the other direction—study the pigeon, he said. They were everywhere in Cambridge and too ugly (due in part to earlier domestication) and common to attract any ornithologist since a monograph by Whitman (1919). The variability in feather patterns that helped make them ugly also made individuals easy to identify, so behavioral observations of known individuals could begin right away without the need to capture and handle the birds. As it turned out, at the North Cambridge third-floor apartment where I was living, there were in fact pigeons that roosted on the roof of the house next door that could provide a steady stream of behavioral observations right through the night!
What soon became clear in this monogamous species was that males were sexually much more insecure than were females, and males acted to deprive their mates of what they would be perfectly happy to indulge in themselves, that is, an extra-pair copulation. For example, the group outside my window began with four pigeons—two mated couples. They slept next to each other in the gutter of the roof of the house next door. They often settled on the roof any time after four o’clock in the afternoon. When spending the night together as a foursome, the two males, although they were the more aggressive sex, always sat next to each other with each one’s mate on the outside. By sitting next to each other, the males could ensure that each one was sitting between his mate and the other male.
Then, for a period of several days, a new male arrived and was regularly attacked by each of the two resident males and driven off. Finally, after four or five days of persistence, such a male might still be sleeping twenty yards down the gutter from the other four pigeons, and subject to attack without notice. The very day he arrived with his own mate, however, the distance to the other birds was cut in half, suggesting that male concern about male visitors might be associated with some sexual threat or increased chance that his mate would indulge in an extra-pair copulation. More striking still, when the third couple managed to join the other two, it was no longer possible for each male to sit between his own mate and all other males. What happened then was that the outermost males kept their mates on the outside, thus sitting between their mate and the other two males, but the innermost male forced his female onto the sloping roof in front of them, rather than allow her to sit between him and his neighbor to the right! The female was not happy with this situation and would return to the more comfortable (and warmer) gutter, only to be forced back onto the sloping roof. Sometimes she would wait for him to fall asleep and would slip down beside him unnoticed,
but I would soon hear roo-koo-kooing out my bathroom window and would rush to see her pushed back onto the roof. This, for me, was a surprising observation because it put the lie to the notion, so common in ornithology and evolutionary thinking at the time, that the monogamous relationship was one without internal conflict. Here was a male willing to force his own mate, mother of his offspring-to-be, up onto the sloping roof all night long because of his sexual insecurities. This suggested relatively strong selection pressures.
Whitman (1919) reported a sex difference in behavior upon viewing the partner in adultery that I thought was instructive along these same lines. Whitman said that when a male pigeon saw his female about to begin copulating with another male, he flew straight at the second male, attempting to knock him off her; that is, he interrupted the copulation as soon as possible. By contrast, a female seeing her own mate involved in the same behavior would not attempt to stop the copulation but would intervene immediately afterward, separate the couple, and act to keep the other female away from her mate. What was going on here? The obvious answer was suggested by the relative investment of the two sexes in the offspring, certainly at the time of copulation. The male’s investment at copulation is trivial, or relatively minor, but the female’s investment may be associated with a year’s worth of reproductive effort. Thus, males chosen as extra-pair partners by females enjoy the possibility of a large immediate benefit (paternity of offspring who will be reared by the female with the help of another male) and similarly inflict a large cost on the “cuckolded” or genetically displaced male. These large potential selective effects would explain both a male’s eagerness to indulge in such extra-pair copulations and his anxiety that his own mate might act similarly!”
“Bateman ’48 in Heredity”
Were it not for Ernst Mayr I would never have heard of “Bateman ’48 in Heredity.” I was taking a reading course from him on genetics and having done no reading on genetics I told him pigeon stories. “Have you read ‘Bateman ’48 in Heredity’?” (Never heard of it.) “Go read it; it has the key to what you are talking about.”
Three weeks later I returned and still not having done any work on genetics, I launched more pigeon stories at him, when he briskly cut me off: “Have you YET read ‘Bateman ’48 in Heredity’?’ No, I had not. “I will not continue this conversation until you have,” Mayr said, turning away from me. That was how Ernst Mayr made sure I read the key paper—Bateman 1948 in Heredity!
And read it I did. That evening I xeroxed the paper when Harvard did not charge a graduate student for doing so.
And Bateman was the key. It had variance in reproductive success as a function of differences in relative parental investment; the less investment in offspring, the higher variance in their number. The variance data were unambiguous: 4 percent of females had 0 reproductive success; the rest varied by their ability to produce eggs. Fully 21 percent of males had no surviving offspring. This was because of low male parental investment. The cost of sperm was trivial compared to the cost of eggs. So, males were in competition with
each other and some did better. They either outmuscled their brothers or they were more attractive to females.
It is interesting that no one, but no one, cited “Bateman ’48 in Heredity.” The paper was completely overlooked. Ironically, “Bateman ’49,” a trivial paper on Drosophila genetics, was cited numerous times. For me, “Bateman ’48 in Heredity” immediately opened up a brand-new world unexplored by others—the connection between variance in reproductive success and relative parental investment. The latter was defined by the tendency for parental investment to inhibit future parental investment. Eggs vs. sperm. All I had to do was fill in the details.
George Williams had a strong influence on my thinking, of which I became conscious only after I had finished writing the chapter. I was about to teach a course at Harvard in 1971 on natural selection and social behavior in the anthropology department under Irv DeVore. Since I was preparing for the course, I reread Williams (1966) and was astonished to see how much of my own chapter was borrowed from his book. Sex role reversed species. Very simple. Males invest more than females. So, there’s a sex role reversal based on sex reversal in parental investment. Differential mortality by sex. Which sex dies faster under what conditions? He did not solve the over-age-17 problem, but he raised it. There were other examples.
Citations
Parental investment and sexual selection has been cited more than 17,000 times. This is extremely high for a theoretical paper, one of the top 5 of 30 million. It is not a direct measure of importance or quality. For example, the most important paper published in all of 20th-century biology was Watson and Crick (1953), which gave the structure of DNA, the double helix. It has been cited half as often as reciprocal altruism which has been cited some 13,000 times. Sometimes I like to joke that of course Watson and Crick is less important than reciprocal altruism, but is it really less than half as important as reciprocal altruism, as the data would actually suggest?
Why is a paper cited so often? On the one hand, parental investment and sexual selection give you a general theory for the evolution of sex differences in all species. They therefore apply wherever there are two sexes. And they link together data from all different species.
Perhaps more important than a general theory of sex differences, parental investment and sexual selection defined parental investment. And it was different than parental care, it was different than cost of parental care. It was parental investment and an analogy between growth of populations and growth of money. You invest money to get back more money in the future. You invest in current offspring in order to get more offspring in the future. Once you define a variable, it is natural to get cited whenever it is first used.
The Writing of the Chapter
I wrote the chapter in several stages.
I began by rereading the entire literature start to finish. I had assembled about 70 articles over two or three years. Some principles became obvious when the whole literature was read, while only suspected from reading the literature one by one. I was supposed to be focused on amphibians and reptiles and decided to concentrate on differential mortality by sex as the only topic they might contribute to. Alas, data from nature were useless since they measured not adult sex ratio but ease of capture—males disperse more widely, so they encounter traps more frequently and are less timid so they enter them more often.
I therefore expanded my subject to include all organisms.
This stage took about seven months, reading the entire available literature and organizing it into subcategories.
I then decided to embed the entire literature simultaneously in my brain “without fear or favor” (e.g., bias due to time of acquisition). To do so, I mixed all the papers up at random and then spent the next three days speed-reading the whole lot.
At this point I was ready to write the paper. I spent about nine weeks writing the chapter itself. Emended and improved since then, but what you see is what you got.
References
Bateman, A. J. (1948). Intra-sexual selection in Drosophila. Heredity, 2(3), 349–368.
Trivers, R. L. (1971). The evolution of reciprocal altruism. Quarterly Review of Biology, 46(1), 35–57.
Trivers, R. L. (1972). Parental investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man (pp. 136–179). Aldine.
Trivers, R. (2002). Natural selection and social theory: Selected papers of Robert Trivers. Oxford University Press. Watson, J. D., & Crick, F. (1953). A structure for deoxyribose nucleic acid. Nature 171(3), 737–738.
Whitman, C. O. (1919). Posthumous works: The behaviour of pigeons. 3 vols. H. A. Carr, Ed. Carnegie Institution of Washington.
Williams, G. C. (1966). Adaptation and natural selection: A critique of some current evolutionary thought (Vol. 75). Princeton University Press.
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Michael J. Ryan
Sexual Selection and the Animal’s Mating Mind
Abstract
Moving from Darwin’s theory of natural selection, I briefly review his theory of sexual selection and focus on his idea of female mate choice and the sexual aesthetics that motivate it. I review some early hypotheses on the adaptive significance of mate choice. Going forward, I then introduce studies that attempt to uncover the underlying mechanisms that define a female’s sexual aesthetics. Much of evolutionary psychology has been derived from basic notions in evolutionary biology, especially in mate choice. Here, I turn the tables and review studies of animal mate preferences that have been inspired by studies of humans in the fields of psychophysics, behavioral economics, and neuroaesthetics.
Key Words: sexual selection, mate choice, psychophysics, sexual beauty, irrational choice
Sexual Selection Theory
It has been 150 years since the publication of The Descent of Man and Selection in Relation to Sex (Darwin 1871), and a bit longer since Charles Darwin exclaimed, “. . . the sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick!” (Darwin 1860). Darwin already had one important theory, natural selection, under his belt when he turned his attention to what initially seemed to be a contradictory theory, sexual selection.
Darwin had an aversive reaction to the peacock’s tail because the mere existence of this ornament seemed to run counter to predictions of natural selection, the evolution of traits that enhance survivorship. The peacock’s tail is not an isolated example. Elaborate traits that seem to compromise survivorship are found throughout the animal kingdom among most sexually reproducing taxa, and these ornaments are perceived in all sensory modalities. These types of traits include birdsong, cricket and frog calls, firefly flashes, brilliant colors of many fish, and the musty odors of many mammals. These traits share other attributes: they are involved in mating behavior and they are sexually dimorphic, often being more extensively developed in males than in females.
In retrospect, Darwin’s sexual selection hypothesis does not seem complex. Like natural selection, evolution by sexual selection requires variation, selection, and inheritance. The
difference is in the second step. Natural selection favors those variants with higher survivorship while sexual selection favors those variants with greater mating success. Darwin suggested that sexual selection favored two types of traits: those that enhanced an individual’s access to members of the other sex and traits that made courters more attractive to members of the opposite sex, the choosers; in short, armaments and ornaments. An important caveat is that there is substantial variation in the animal kingdom, and there are cases in which females exhibit the more elaborate courtship traits and other species, such as our own, in which males and females both exhibit these types of traits (Rosenthal 2017). Nevertheless, Darwin posited that in most animal mating systems, males are competing for either access to or the attention of females.
Male-male competition was not a controversial idea perhaps for several reasons (Richards 2017; Ryan 2021). Males battling for access to females did not seem all that different from activities favored by natural selection and conformed to Tennyson’s epitaph that nature was “red in tooth and claw.” The idea of mate choice, however, rankled many of Darwin’s supporters, especially Alfred Russel Wallace. Many of Darwin’s contemporaries had a hard time empowering female animals as the agents who decide who gets to mate, and they also found Darwin’s explanation of why females have these preferences, that they were grounded in the female’s sexual aesthetics, as rather wanting. Darwin’s theory laid mostly fallow for about a century (Richards 2017; Ryan 2021).
There was a resurgence of interest in sexual selection by mate choice one hundred years later that resulted in large part from Campbell’s edited book Sexual Selection and the Descent of Man, 1871-1971 (Campbell 1972), and especially Trivers’s (1972) chapter on parental investment and sexual selection. Trivers was influenced by the early work of Bateman (1948), who showed that in fruit flies the number of matings had a larger effect on male reproductive success than on female reproductive success. Trivers pointed out that this discrepancy arises from greater female investment in her gametes than male investment in his gametes. This gives rise to a sexual conflict of interest (Arnqvist and Rowe 2005) in which males should be under selection to mate often and females should be under selection to mate carefully. A point sometimes overlooked by critics in the social sciences is that this formulation firmly planted females in the driver’s seat; they were the deciders. But when Darwin moved on to discuss humans, he returned to a more Victorian view of the sexes (Richards 2017).
Bateman’s principle, as it is now called, has been productively criticized on a number of fronts (Gowaty et al. 2012; Tang-Martínez 2016). A recent meta-analysis of a large number of mating systems, however, upheld Bateman’s and Trivers’s prediction of these sex differences in mating roles (Janicke et al, 2016). In addition, Borgerhoff Mulder and Ross (2019) critically and carefully applied Bateman’s principle to their analyses of twenty years of data on marriage systems of the Pimbwe in East Africa.
Darwin’s theory of sexual selection by mate choice has attracted more attention and consternation than his theory about male competition for access to females. It was much
easier to explain the evolution of armaments than ornaments. Post-Trivers, behavioral ecologists showed that in many cases female mate choice garnered resources that increased her reproductive success. But the question that seemed to most interest behavioral ecologists was what kind of information about the male’s genetic quality is communicated to the choosing females. The good gene’s hypothesis posits that males advertise genes that enhance survivorship, and females are under selection to choose these males because of the genetic benefits to their offspring (Hamilton and Zuk 1982; Rowe and Houle 1996; Zahavi 1975). Theory suggests this hypothesis is logical (Grafen 1990), but there is not overwhelming empirical support that it is biological. Surely, good genes selection occurs, but estimates of its relative effect in nature are relatively small (Achorn and Rosenthal 2020; Kirkpatrick and Barton 1997; Møller and Alatalo 1999; Rosenthal 2017).
More recently, research in the realm of sensory ecology, neuroethology, and neuroscience have shown how selection on sensory, neural, and cognitive systems in other domains can have important influences on what females find sexually beautiful. These studies are providing important insights into the scaffolding of an animal’s sexual aesthetics. This is the line of research I follow in the remainder of this chapter.
Sexual Selection and Evolutionary Psychology
Evolutionary biologists have long been interested in human biology, and especially human behavior. Darwin is a prime example (Darwin 1871, 1872). Much of the current interest in the evolutionary basis of human behavior probably has its roots in Sociobiology (Wilson 1975). That book, and especially the last chapter, “Man: From Sociobiology to Sociology,” both garnered the most criticism from the general audience and also provided the foundation for evolutionary psychology. Many of the subjects in evolutionary psychology (e.g., altruism, mutualism, war, and sex) address ideas that populated that chapter (Barkow et al. 1992; Buss 1994; Miller 2011). Thus it seems fair to say that evolutionary biology writ large has inspired much of what is going on today in evolutionary psychology.
I am going to turn the tables. I am going to review a number of recent avenues of interest in animal sexual selection and mate choice that are inspired by studies of humans, especially in the fields of psychophysics, behavioral economics, and neuroaesthetics.
Cognitive Aspects of Mate Choice
A number of researchers working parallel to or collaborating with behavioral ecologists have delved into the neural underpinnings of female preferences. What is it about the female’s brain that makes her perceive some traits as more attractive than others? In a variety of taxa and in all sensory modalities, researchers have uncovered neural biases at the sensory periphery and neural circuits in the brain that contribute to the female’s sexual aesthetics (e.g., Endler 1992; Gerhardt and Huber 2002; Greenfield 2002; Wilczynski and Ryan 2010).
Although these studies in neuroscience have provided unparalleled understanding of the neural scaffolding of the female’s sexual aesthetics, another set of questions concerns the cognitive aspects of mating decisions. By the animal’s cognitive processes we refer to Shettleworth (1998), who defines cognition as the acquisition and analysis of information in the environment that contributes to decision-making. I will review a number of studies, including several that we conducted with túngara frogs, that were inspired by studies of human behavior.
Weber’s Law
We know from the notion of the Umwelt by von Uexküll (1982; see also Caves et al. 2019) that different animals perceive the environment in different ways. This is obvious when we compare the sensory limitations of ourselves to other animals. For example, we cannot hear the ultrasonic echolocation calls of bats nor the infrasound of elephants; we cannot see in the ultraviolet as can bees, fish, and birds, nor can we sense infrared with the precision of a rattlesnake. We cannot share the olfactory experiences of man’s best friend and are unable to sense the signals of most electric fish.
Another limitation is how we compare stimuli within a range we can sense. Psychophysics is a field with a long and distinguished history that is concerned with how we translate stimuli into perception. Many studies show that humans, and other animals as well, do not compare stimulus intensities as they actually exist; our perceived difference between stimuli is often not based on absolute (linear) differences but on proportional ones. These studies are often done in the context of just noticeable differences (JNDs): the minimum difference between two stimuli for us to perceive them as different. Akre and Johnsen (2014) reviewed a number of studies in humans (as well as other animals) showing proportional comparisons in different sensory modalities: in hearing in terms of amplitude and frequency comparisons; in vision in terms of comparisons of area, intensity, and wavelength; in temporal duration in both auditory and visual domains; and in our number sense (see also Shepard 1987).
Although there are exceptions, many of these comparisons follows Weber’s law, which is ∆I = kI, where ∆I is the JND, the magnitude of the stimulus is I and k is a constant. What is clear from this equation is that as stimuli become larger in magnitude, their differences must be greater for us to be able to detect differences between them. In the context of animal behavior in the wild, we are more concerned with just meaningful difference (JMDs; Nelson and Marler 1990) than JNDs.
Mate choice is all about comparisons whether it is between two or more individuals or one individual and a neural template; it is of some importance that we understand how these comparisons are made. In 1984, Cohen (1984) asked if these female comparisons followed Weber’s law; it took more than twenty-five years to get an answer.
Túngara frogs have become a useful system for asking questions about sexual selection and communication. As I refer to this system several times, it is worthwhile to summarize
