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Beauty and the Beast

LOOKING FOR A FEW GOOD MALES: Female Choice in Evolutionary Biology. Erika Lorraine Milam. x + 236 pp. The Johns Hopkins University Press, 2010. $60.

Erika Milam’s Looking for a Few Good Males is a timely and welcome history of female choice and sexual selection. Sexual selection is the part of evolutionary biology that explains why male peacocks have fancy tails and male deer have large antlers; it also offers an evolutionary rationale for courtship behavior. Psychology and the general public have now widely assimilated sexual selection’s gendered narratives. Nonetheless, Milam demonstrates that sexual selection has been contentious and politically loaded ever since Charles Darwin first proposed it. And turbulent disputation about the meaning and truth of sexual selection continues today behind a papier mâché mask of seeming scientific consensus.

2010-11BREVRoughgardenFA.jpgClick to Enlarge ImageDarwin, as Milam explains, envisioned a psychological continuity between animals and humans and found it appropriate to suggest that females “choose” their mates. In 1859 in On the Origin of Species, and in much more detail in 1871 in The Descent of Man, Darwin argued that the cumulative effect of female choice caused the evolution of ornaments such as the peacock’s tail. In the latter book, he wrote that

in the same manner as man can give beauty, according to his standard of taste, to his male poultry . . . so it appears that in a state of nature female birds, by having long selected the more attractive males, have added to their beauty.

Thus, sexual selection—that is, the study of how secondary sexual characters evolve—has been coupled since Darwin with a claim about animal minds: namely, that animals (and female animals in particular) have the capacity for “choice” based on an innate sense of aesthetics.

Sexual selection is often mistakenly equated with female choice, but the two are distinct. Female choice is one mechanism for sexual selection. Darwin proposed another: competition between males (especially in the form of combat) for access to females. Thus the mechanisms of Darwin’s sexual selection are female choice and male–male competition, which cause the evolution, respectively, of male ornaments and of male armaments, such as antlers. Although they are distinct as mechanisms, Darwin thought them to be conveniently reinforcing. He viewed female choice as coincident with success in combat; it’s as though he thought that females want to bed the winners.

As Milam relates, the history of sexual selection is intertwined with alternative views about animal minds and with a varying emphasis on female choice versus male–male competition as the primary mechanism in sexual selection. Alfred Russel Wallace, in 1889 and later, notably disagreed with Darwin about sexual selection. Wallace had no difficulty with the overall idea of sexual selection by female choice, but he disputed the claim that animals had minds that permitted such choice. He argued instead that female peacocks were less ornamented than males because they were selected to be inconspicuous to predators so as not to endanger their young. Thus to Darwin, males had evolved to be colorful, and to Wallace, females had evolved to be drab.

But humans are another matter, because we have minds. Wallace argued that sexual selection in humans could lead to improvement of the species. As Milam summarizes,

Wallace suggested that when people were “free to follow their best impulses,” they would spontaneously create a “system of selection” that would “steadily tend to eliminate the lower and more degraded types of man, and thus continuously raise the average standard of the race.”

Wallace wrote that

when women are economically and socially free to choose, numbers of the worst men among all classes who now readily obtain wives will be almost universally rejected. . . . just as we advance in the reform of our present cruel and disastrous social system, we shall set free a power of selection in marriage that will steadily and certainly improve the character, as well as the strength and the beauty, of our race.

Sexual selection, by either of its mechanisms, has thus been viewed as a kinder and gentler form of eugenics, a reproductive eugenics to be contrasted with the survivalist eugenics of concentration camps. Even today, some proponents of sexual selection in animals feel ennobled by believing they are studying a natural system of eugenics in which female choice and male–male competition weed out bad genes, improving the “conservation value” of species.

Milam reviews the theories of mind for animals from the early to mid 1900s, mentioning Konrad Lorenz’s hydro-mechanical model of instinctual behavior, Danny Lehrman’s critique of ethological methodology and of the concept of instinct, and Niko Tinbergen’s notions of ritualization in courtship. During this period, “choice” was largely replaced by mechanical stimulus and response, which avoided attributing sophisticated minds to animals.

Milam next reviews experimental population-genetic research with Drosophila during the 1950s and 1960s, drawing attention to the studies of Claudine Petit and Lee Ehrman on the “rare male” mating advantage. Their experiments demonstrated that male flies with eye-color and eye-shape mutations sired more offspring when they were surrounded by male flies with the wild-type eye color and shape. This advantage in mating of being rare counteracts the tendency of natural selection to eliminate these mutant genes from the gene pool and is thus a mechanism that promotes genetic diversity. Petit construed these studies as demonstrating selection sexuelle, and indeed they might be understood as showing that female flies can, in some sense, choose the males they mate with. This terminology illustrates the frequent synonymous substitution of sexual selection for female choice in the literature. Petit and Ehrman’s studies do not address the causes of secondary sexual characters in Drosophila and arguably are not studies of sexual selection per se.

From the 1940s through the 1960s, Mendel’s laws and mathematical population genetics were brought to bear on evolutionary studies, including those focusing on anatomy, paleontology, taxonomy and systematics, in what is known as the Modern Synthesis. Milam shows that the interest in female choice of Modern Synthesis architects such as Ernst Mayr and others was primarily in relation to speciation. Mating behavior, including female choice in particular, was of interest as an “isolating mechanism” preventing hybridization between the gene pools of geographically separated species. Female choice was also of interest as a possible cause of speciation without the need for geographical separation—so-called sympatric speciation, in which a single gene pool splits into two pools because females for some reason evolve into two groups, each of which chooses a different type of male to mate with. Again, female choice does not equate to sexual selection, and the Modern Synthesis architects paid little attention to sexual selection. Indeed, Mayr’s 1963 landmark book, Animal Species and Evolution, contains no discussion of sexual selection; nor is there an entry for the phrase “sexual selection” in its index. A lack of interest in sexual selection is evident even today in critiques of neo-Darwinism, which focus on difficulties at the genotype-phenotype interface and seldom mention sexual selection.

The theory of sexual selection, having lain dormant since Darwin and Wallace’s day, suddenly sprang to life in the 1970s, resuscitated by the writings of William Hamilton, John Maynard Smith, George Williams, Robert Trivers, Geoff Parker and Richard Dawkins, among others, all of whom were young Turks relative to the architects of the Modern Synthesis. Milam observes that most historians of biology refer to the long period during which the subject was neglected as the “eclipse narrative” of the history of sexual selection, and she notes that this “became the standard story of sexual selection.” Milam disputes the eclipse-narrative version of events, pointing out at some length that research on female choice was present throughout the dark age between the 1870s and the 1970s. I’m not persuaded though. The research during the eclipse may indeed have been in some way about animal minds, and it may have included the possibility of female choice. However, it was not concerned with explaining either the secondary sexual characters Darwin noted or the dynamics of courtship behavior that he envisioned as causing the evolution of those characters. Only in the 1970s did secondary sexual characters and courtship, rather than the animal mind, reemerge as the central issues of interest. Thus, the eclipse narrative of the history of sexual selection seems accurate to me.

Milam ends with an account of the research papers Robert Trivers published in the early 1970s and includes notes from her 2004 interview with him. The retrospective she offers would lead one to believe that sexual selection is now settled science. One day a sequel to Milam’s book will reveal, however, that the subject is now as much in flux as when Darwin and Wallace were in disagreement 150 years ago. What is at issue now is not the mental capacity of animals but the rationale for their choices. The sequel will document a remarkable rancor between those who believe that the accumulated exceptions and theoretical difficulties with sexual selection’s explanation for secondary sexual characters are a call to patch up a fruitful framework and those who feel that the weight of evidence and internal inconsistencies are so great that sexual selection should be abandoned and the matters it attempted to solve rethought from the ground up.

But for now, Erika Milam’s book is an accessible and important contribution to the history of an active topic of biological research today, and it should be read by evolutionary biologists as well as by historians and philosophers of biology.

Joan Roughgarden is a professor of biological sciences and of geophysics at Stanford University. She is the author of, among other books, The Genial Gene: Deconstructing Darwinian Selfishness (2009) and Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People (2004), both from University of California Press.

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