[wpaudio url="http://the-scientist.com/2011/01/01/book-excerpt-from-looking-for-a-few-good-males/erika-milam-3/" text="Listen to Erika Lorraine Milam read from her book, Looking for a Few Good Males: Female Choice in Evolutionary Biology" dl="0"]
Starting in the 1920s, three men—Ronald Aylmer Fisher, J. B. S. Haldane, and Sewall Wright—began to integrate genetics with natural selection, using mathematics to describe the evolution of a population. Only one of these mathematically inclined evolutionary theorists paid significant attention to female choice: Ronald Fisher. After Fisher was rejected for fighting duty in the First World War, because of his terrible eyesight, he decided he could best serve his country by becoming a farmer. In 1917, Fisher and his new bride, along with her older sister (a long- time friend of Fisher), moved to a former gamekeeper’s cottage in Bradford, England. They were soon to be joined by several pigs, at least one calf, and children. Fisher sought to exemplify a eugenic life through subsistence farming, and it was only after the war that financial constraints, along with the continued exhortations of Charles Darwin’s fourth son and eighth child, Leonard Darwin, to give up farming, led Fisher to accept a post as a statistician at Rothamsted Experimental Station. The early years of his professional career exemplify the passions that would last throughout his life: eugenics, theoretical population biology, and statistical analyses.
Fisher’s interest in female choice was part and parcel of his more general explication of sexual selection and the evolution of humans in The Genetical Theory of Natural Selection, published in 1930. In Genetical Theory, Fisher used sexual selection to argue that female choice could explain the evolution of apparently nonadaptive traits in humans, such as self-sacrifice (heroism) and beauty. These two traits presented a problem for any evolutionary theory based solely on natural selection, he believed, as neither could be explained as enhancing the survival of individuals. Fisher’s concern with the physical fitness and vigor of the next generation also drove his interest in sexual selection. Far from trying to remove the taint of “vigor” from theories of natural selection, Fisher intended his theories of natural selection and sexual selection to demonstrate the importance of eugenic concerns to the physical and intellectual prowess of the next generation. Fisher’s commitment to female choice and positive eugenics was explicit in his early publications in the Eugenics Review (for which he also acted as book review editor for many years), especially “Some Hopes of a Eugenicist” (1914), “The Evolution of Sex Preference” (1915), and “Positive Eugenics” (1917). His later elaboration of sexual selection described the process of evolution as based on differential reproduction, occurring within a single population, and resulting in either progressive development or degradation of the population.
Fisher’s formulation of sexual selection and female choice in Genetical Theory emerged from both his genetic and evolutionary interests in human progress. His interest in eugenics began early in his education, and as an undergraduate he was elected the first chairman of the Undergraduate Committee for the Cambridge Eugenics Society. Fisher, like Darwin, believed that females compared males and chose the one they preferred. The belief that female choice was a comparative, choice-based evolutionary mechanism lay at the heart of Fisher’s conviction that sexual selection was more important for the improvement of humanity’s biological future than it was for animal evolution.
In his short 1914 paper, “Some Hopes of a Eugenicist,” Fisher set forth Darwinian evolution as vital to the future of humanity. “From the moment that we grasp, firmly and completely, Darwin’s theory of evolution, we begin to realise that we have obtained not merely a description of the past, or an explanation of the present, but a veritable key of the future.” Selection influenced the physical body of man as well as his mental and emotional capabilities. “All the refinements of beauty, all the delicacy of our sense of beauty, our moral instincts of obedience and compassion, pity or indignation, our moments of religious awe, or mystical penetration,” were the result of evolution in action.
Fisher identified at least two facets of the eugenic problem: the quality and the quantity of off spring in the next generation. In choosing with whom to reproduce, humans’ marriage choice determined the quality of children in the next generation. The number of babies born to families of high and low quality determined the proportion of high- and low- quality adults in the next generation. In 1915, Fisher addressed the first of these aspects, quality of off spring, by linking the past and future evolution of humans to mate choice in “The Evolution of Sexual Preference.” In this article, Fisher contrasted the effects of Darwin’s theory of natural selection with the effects of sexual selection. Natural selection, he argued, could explain the evolution of the organization and physical structures of animal and human bodies. The evolution of human ethics, aesthetics, beauty, and morality he reserved as the special jurisdiction of sexual selection. “In the sexual selection of mankind, therefore, beauty and character provide standards of universal currency. Everywhere we see the power of beauty of form, colour, voice, expression and grace of movement; everywhere also the charms and merits of character dominate our judgments.” Further, human capacity to perceive all the “elusive traits of human excellence” was at its most acute under the influence of burgeoning love. Only two years later, in “Positive Eugenics,” Fisher addressed the second issue—quantity of off spring. He argued adamantly that upstanding professional families needed to produce more children. “To increase the birth- rate in the professional classes and among the highly skilled artisans would be to solve the great eugenic problem of the present generation and to lay a broad foundation for every kind of social advance.” Fisher’s vision of eugenic evolution in human society, then, included both the quality and quantity of the off spring who would form the next generation.
Much like Wallace, Fisher expressed skepticism that evidence of sexual selection in nonhuman animals would ever be found. He insisted that although the process of sexual selection in animals and humans was very similar, “among mankind the conditions are more favourable for the higher development of sexual selection…[because] the choice of a mate is of more importance among mankind than among most other animals.” Not all humans were equally good at judging mate quality, however; individuals of high intellectual development could best appreciate fine differences in the quality of potential mates. Fisher’s linkage of aesthetic sensibility and intelligence gives us a sense of how biologists used sexual selection to both explore the animalistic basis of human sexuality and simultaneously reserve for humans their highest expression.
These factors of mate quality, off spring quantity, and the importance of individual choice in directing human evolution came together in Fisher’s description of sexual selection in Genetical Theory. The book had twelve chapters. The first seven explored evolutionary theory in general; the last five dealt more specifically with humankind. In the preface, Fisher indicated that “the deductions respecting Man are strictly inseparable from the more general chapters.” The first chapters contained the mathematical and theoretical foundations of Fisher’s later arguments about social economic reform. He most clearly explored the connection between animals and humans (or, more generously, between the general theory and its specific application) in chapter 6, “Sexual Reproduction and Sexual Selection,” and chapter 11, “Social Selection of Fertility.”
From a historical perspective, Fisher at first seems to be a bit of a renegade within the biological community because he argued, against the wisdom of contemporary zoologists such as Kellogg, that sexual selection could work in animals. Yet, like his contemporaries, Fisher emphasized the power of sexual selection and female choice to enact evolutionary change in human societies rather than in animals. In his chapter on sexual selection in Genetical Theory, Fisher outlined a process in which female preference for a trait (say, long tails in birds) could cause such a trait to spread in a population, even if it had no survival value for the males or, even worse, hurt the males’ chance of survival. Fisher called this process “runaway sexual selection.” Today, biologists interested in animal behavior and evolutionary theory look back on Fisher’s work as seminal to the development of their field, but his formulation of runaway sexual selection failed to attract much attention among biologists until the 1960s.
For Fisher, the power of sexual selection rested in its ability to act in opposition to the selective effects of natural selection. For female preferences to become ingrained in a population, Fisher posited, initially there must be some fitness advantage inherent to females’ choices. He suggested there were only two necessary conditions for directional evolution through sexual selection: first, that a sexual preference must exist in at least one sex, and second, that the preference must confer a reproductive advantage. Once heritable mate preferences were established in a population, they could begin to act as a mechanism for evolutionary change in their own right. Given these conditions and enough time, sexual selection could even help generate traits that were detrimental to individuals survival—hence, “runaway” sexual selection.
According to Fisher, runaway selection occurred when female preference for a male trait and the male trait itself began to evolve in lockstep. Fisher used the example of plumage development in birds to illustrate his point. As some males’ plumage became more beautiful and extravagant (think of a peacock’s tail), the effect of the average male’s plumage on females declined—the fancy males would produce many more off spring than the plainer males. The next generation would disproportionately exhibit longer and brighter tails. If females continued to choose to mate with males with the longest and brightest tail, their preference would become more intense as the male traits became more extravagant. Even if extravagant males were less likely to escape predators (natural selection), further development of male tails would proceed until the reproductive advantage was completely negated by the disadvantage incurred by natural selection. Thus, through female choice, populations would evolve in ways that carried no survival advantage (or even decreased individuals’ chances of survival) but increased the ability of females to discern and appreciate beauty.
Fisher used his illustration of runaway sexual selection in birds to elucidate the evolution of apparently nonadaptive traits in humans, such as heroism. Heroism, for Fisher, described the tendency of people (especially men) to sacrifice their lives in battle for the good of the group (tribe) to which they belonged. Fisher found it difficult to explain such altruistic tendencies solely in terms of natural selection, which he thought should act to cull such phenomena from a population very quickly. He compared the phenomenon of heroism in humans with the presence of bitter- tasting chemicals in some insects—the evolutionary benefit of both traits was conferred on the group to which such individuals belonged. Just as the bitter-tasting butterfly earned no personal fitness advantage (no increase in number of offspring) when eaten by a predator that subsequently learned to avoid eating similar-looking butterflies, the warrior’s sacrifice of his life for the safety of the group also connoted no personal advantage. Fisher argued that both of these traits were maintained evolutionarily by the reproductive advantage gained by the relatives of the sacrificed individual—a form of what biologists now call “kin selection.”
In one major aspect, however, the evolution of bad- tasting insects and heroic humans differed for Fisher—sexual selection. The effects of female choice and sexual selection complicated explanations of human heroism, because women preferred to mate with heroic men. If the hero did not die but returned home safely, his exploits would surely make him the focus of many women’s attentions. Fisher hoped that proper female choice in this context would correct the dysgenic effects of war. When his son died in combat in 1943, Fisher searched in vain for evidence of an unreported grandchild, hoping that his son’s genetic heritage would not be lost. Part of Fisher’s concern over the loss of his son was a specific instantiation of a much more widespread concern about the impact of the Great War on the United Kingdom’s population: war eliminated countless thousands of the bravest young men from the breeding population. Female choice for heroes ensured the eugenic quality of the next generation, but only if those heroes produced off spring.
Sexual selection could also enhance the effects of natural selection, and it served both as a viable method of eugenic improvement and as a cautionary tale about the inevitable effects of the fertility trends of modern society. As long as the preeminent members of society were more fertile than less desirable members, and women continued to choose their husbands well, then society would become more intelligent and more beautiful. If, however, the relationship between social and sexual selection for heroes and fertility were reversed, sexual selection would act to decrease the number of heroes in the population, and the numbers of less valuable members of society would increase. “Sexual selection must be judged to intensify the speed of whichever process, constructive or degenerative, is in action. The intensity of this influence must, however, be much diminished in the later stages of civilized societies, with the decay of the appreciation of personal differences.” Fisher argued that as the educated elite gave birth to fewer children than the masses, the connection between fertility and eugenic quality was becoming decoupled. He feared that in the future, women would lose the ability to choose well, and ill-advised female choice would speed social destruction.
Outspoken eugenicist William J. Robinson, who provided an extreme example of the evolutionary ladder of aesthetic appreciation and intelligence, expressed similar concerns about the lack of eugenic mate choice in civilized society. In his immensely successful Woman: Her Sex and Love Life, Robinson distinguished between the sexual drive to mate, which intercourse with any member of the opposite sex can satisfy, and feelings of true love for one individual above all others. “Real love, true love, is a new feeling, a comparatively modern feeling, absent in the lower races and reaching its highest development only in people of high civilization, culture, and education.” Robinson contended that only civilized people could exhibit true love and rational female choice; members of the lower races, just like animals, failed to differentiate their sexual interests. Similarly, in a 1937 article on teaching women proper mate choice, prolific American social hygienist Paul Popenoe admonished educated women to follow their evolutionary past in attracting a mate, by acting “seductive and alluring rather than aggressive” so as to elicit male courtship rituals. To behave otherwise, Popenoe suggested, was as dangerous to marital bliss as were insufficiently aggressive husbands. Through rational analysis and change of behavior, Popenoe contended, women could become more attractive mates and better wives.
Whereas books by Robinson and Popenoe sold thousands of copies, Fisher’s Genetical Theory attracted far less popular and scientific attention. After publication of the book, Fisher was dismayed that few reviewers commented on the application of his general theory to the problem of human evolution. In a letter to geneticist J. B. S. Haldane, Fisher wrote of his work that “the main practical point is to combat the idea that racial decay, or the differential birth- rate, or any other social phenomenon which we judge undesirable, is to be accepted fatalistically as the ‘Will of Allah,’ rather than tackled scientifically like rabies.” Fisher had hoped that the practical application of his theories to social policy would attract more attention. In a similar letter to geneticist Hermann J. Muller, Fisher lamented that “I feel on rather strong ground about Man, apart from the fact that one cannot make any innocent statement about that confounded animal without people thinking you are attacking their political or religious opinions.” He continued by pointing out that his first chapters on humans, “Chapters VIII to XI [,] are an attempt to build up one coherent argument analogous to sexual selection, or mimicry theory (I mention this because the best critic whose opinion I have yet heard, has missed just this point).”
In fact, the entire Genetical Theory failed to achieve much critical acclaim among biologists until the second edition appeared in 1958. One explanation is that the mathematics associated with the population dynamics of the early chapters was quite difficult; as a result, perhaps very few readers made it to the later chapters of the book. Another explanation could be that readers shied away from the book because of its explicit political agenda. In either case, biologists’ failure at the time to cite Fisher’s runaway selection model of female choice was probably not due to their lack of interest in female choice or behavior as an evolutionary mechanism in animals, but simply a reaction to the book as a whole.
The lukewarm reception of Genetical Theory did not signal the end of Fisher’s interest and research in human evolution. To be sure, he became frustrated with the decreasing importance of research in the Eugenics Education Society, and he ended his association with the group. His continued interest in the questions of human evolution and genetics is evidenced by his serological work in the 1930s and 1940s. Through an analysis of blood groups (ABO) and the rhesus (Rh) factor, Fisher hoped to elucidate the relationship between racial blood types and susceptibility to particular diseases. Despite his continued interest in racial evolution and genetics, Fisher never returned to the issue of female choice or sexual selection in his published research.
Fisher’s subsequent lack of publications on female choice also seems to have stemmed from his conviction that he had solved the problem of mate choice in humans. His reaction to a 1948 paper, “Intra-sexual Selection in Drosophila,” speaks volumes about his later attitude to research on female choice and sexual selection in animals. Fisher knew of the author, Angus John Bateman, because Bateman worked at the John Innes Horticultural Institute, under the direction of cytologist Cyril Darlington. Darlington and Fisher were long-time friends, cofounding (in 1947) and coediting the journal Heredity. Bateman’s paper, published in the second volume of Heredity, proposed that proper mate choice was more important to females than males, because females invested more resources in each young and mated far less frequently than did males. If a female made one poor mate choice, Bateman theorized, it could affect her entire reproductive contribution to the next generation; if a male made one poor mate choice, it affected his reproductive success far less, because his choice was only one among many in his lifetime. On reading the manuscript, Fisher made an off-hand remark to Darlington, who passed the comment along to Bateman. In response, Bateman wrote to Fisher protesting that he had not, in fact, plagiarized Darwin and insisting that his work represented a new framework within which to analyze the importance of female choice and sexual selection—namely, reproductive investment. Fisher immediately attempted to clear up the misunderstanding.
I am sure Darlington misunderstood me if he suggested that I thought you guilty of plagiarism. Of course that would be nonsense. I certainly had supposed it was obvious, and had been taken as obvious by writers on the subject, that the reproductive capacity of females being more limited than that of males, it was inevitable that they rather than the other sex should exercise selection and that the males should be more conspicuously modified by sexual selection…However, I do not think all this matters; at least your paper makes sure that future writers will be able to find the general principle clearly stated.
How reassuring, and yet how dismissive! For Fisher, the crux of female choice and sexual selection was human evolution. Working through the dynamics of female choice as it related to animals was trivial and missed the point. Through the lens of human mate choice and eugenics, it seemed obvious to Fisher that the differential investment of the sexes in reproduction and childcare meant that women should consider only a subset of men to be worthy mates, while men could afford to be significantly more profligate in their sexual tastes. For Bateman, looking only at animals, the connection was new and subtle.
In Fisher’s view, evolution was a directional process, potentially progressive or degenerative, taking humans closer to or farther from animality, and acting on a single population. Female choice in marriage partners led to differential reproduction, in which some males more than others contributed to the genetic composition of the next generation. Such differential reproduction acted as an evolutionary accelerant, either improving the eugenic worth of a single breeding population or hastening the population’s demise through genetic deterioration. Fisher appears to be a biological renegade in promoting female choice and sexual selection as valid biological concepts only if we ignore the human context of his evolutionary theorizing….
Milam, Erika Lorraine. Looking for a Few Good Males: Female Choice in Evolutionary Biology. pp. 43-51. © 2010 The Johns Hopkins University Press. Reprinted with permission of The Johns Hopkins University Press. Read "Appealing Choice," an essay on Lorraine's book.