Looking for a Few Good Males: Female Choice in Evolutionary Biology

Introduction

Introduction How does a hen decide whether she is in the mood for sex? How does a hen decide which is the best rooster? For a female chicken to “choose” a rooster, in the way we think of humans choosing partners, she would have to recognize differences between males, compare them based on that variation, and decide with which male(s) she should mate and invest her reproductive future. Such cognitive comparisons imply a level of rational thought and aesthetic appreciation that many biologists in the twentieth century were hesitant to ascribe to nonhuman animals. For these biologists, rational choice was reserved for humans, and to interpret the behavior of animals in choice-based terms could be described only as anthropomorphic. Yet, despite this criticism, other biologists have been fascinated by the idea that the mating behavior of animals could serve as an experimental entrée to the more complicated process of mate choice in humans. In both cases, the history of female choice in evolutionary biology reflects biologists’ careful negotiation of the implied aesthetics and rationality of choice-based behavior in humans and other animals. The touchstone for research on female mate choice continues to be Charles Darwin’s theory of sexual selection. In 1871, Darwin published Descent of Man and Selection in Relation to Sex, in which he elaborated his “second” theory. Sexual selection consisted of two mechanisms that together explained why males and females differed in appearance and behavior: one was female choice, the other was male-male competition. In female choice, females compared the mating displays of reproductively mature males and chose the most appealing male with which to mate. In male-male competition, males fought to determine which male would have access to the reproductively available female(s) in the area. Both mechanisms, Darwin argued, would result in exaggerated male traits. Over evolutionary time, female choice would lead to aesthetically pleasing male traits (long tails and brightly colored plumage), and male-male competition to armor or weapons (bony plates or antlers). Darwin contrasted sexual selection with his more widely known theory of natural 2 Looking for a Few Good Males selection; whereas natural selection depended on who survived, sexual selection depended on who reproduced. Natural selection would lead to utilitarian adaptations. Sexual selection through female choice provided Darwin with an explanation for a variety of aesthetic phenomena he could not explain through survival alone: the presence of beauty in animals, differences between males and females of the same species, and racial differences within a species. Thus, for late nineteenth-century biologists, female choice presupposed both a sense of aesthetic appreciation and an ability to choose rationally based on this aesthetic sensibility—mental attributes they were hesitant to ascribe to animal minds. In the animal-human cognitive divide , humans were capable of rational aesthetic choices, and animals were not. According to most historical accounts of sexual selection theories, it was not until the 1970s that organismal field biologists self-consciously returned to a Darwinian model of female choice as a mechanism for evolutionary change, one that emphasized the continuity of rationality and choice across the animal-human boundary. Historians and biologists alike typically identify female choice as the cause of the eclipse of interest in sexual selection, and they point to Robert Trivers’s monumental paper “Parental Investment and Sexual Selection,” published in 1972, as inaugurating new interest in the theory by providing a biological justification for female choice in nature. Certainly, his paper had been cited more than three thousand times by 2000 (and over fifteen hundred more times by 2008), a citation record that speaks to the remarkable interest in sexual selection as a topic of research in recent decades. The history of mate choice is distinct from the history of sexual selection as an explanation of beauty in the animal kingdom. Although biologists’ interest in sexual selection did wane for much of the twentieth century, interest in female choice remained strong. In the early decades of the twentieth century, biologists reframed female choice in the mechanistic language of “stimulation” rather than the aesthetic, cognitive language of “choice.” Apparent mate choice was really due to the differential stimulation provided by the courtship displays of potential suitors. When choice-based behaviors in animals were recast within a stimulatory framework, they survived; when “choice” implied cognitive comparison, as in the aesthetic evaluation of beauty, they did not. Inasmuch as female choice was an issue for biologists between Darwin and...