Sex roles, ornaments, and evolutionary explanation.

M are competitive, sexually indiscriminate, and pushy, whereas females are passive, choosy, and coy. This familiar generalization about the sexual behavior of animals and humans is grossly overstated and potentially misleading, yet has its roots in empirical observation of at least some species. One of the triumphs of modern sociobiology (1, 2) is that evolutionary theory can explain why the sexes differ in their behavior along these lines in so many cases. To state the generalization more accurately, it is frequently, if not usually, the case that for every receptive female in the mating pool of a population, there is more than one male ready to inseminate her. This typical imbalance in the operational sex ratio (OSR; ref. 3) in turn stems from the basic facts of reproductive physiology: sperm are small and cheap, whereas the time and energy burdens of egg production, gestation, and parental care typically fall more heavily on females with the result that fewer females than males are available in the mating pool at any given time (4). Consequently, competing inter alia often benefits males most strongly, whereas being discriminating in mate choice often benefits females most strongly, leading to an evolutionary process of sexual selection expected to result in the evolution of secondary sexual traits in males: weapons that help them win in competition with one another and ornaments that help them win the attentions of females. The appeal of this evolutionary explanation lies in part with its simple scientific validity, but in part with its consistency with long-standing, deep-seated cultural stereotypes about the roles of men and women. Most likely, our cultural stereotypes about human gender roles stem from the same biological bases that shape sex roles in other species. This cultural bias, in turn, and the very human tendency to see the world in terms of stereotypes, has tended to distort and obscure our view of the full richness of the conceptual framework explaining the evolution of sexual behavior and secondary sexual characters (5). A paper by Trond Amundsen and Elisabet Forsgren in this issue of PNAS (6) makes a significant contribution toward a more complete perspective on sex roles and their consequences for sexual selection. Their work with two-spotted gobies (Gobiusculus flavescens) shows that males can be discriminating in mate choice and implies that this discrimination may lead to the evolution of ornamentation in females. Overly simplistic notions of stereotypical or ‘‘normal’’ sex roles for males and females and attendant patterns of morphological dimorphism have been refined on a number of fronts in recent years. Studies of cryptic female choice (7), especially in insects, dispel the notion that females are passive recipients of the sperm of competing males. Instead, females of a number of species have been shown to be capable of discriminating among the sperm of different males once inseminated, allowing active mate choice to occur even if females are unable to exercise preferences before mating. Studies of fully role-reversed species provide exceptions that prove the rule for sex role theory more generally. In pipefishes, for example, biological constraints limit the reproductive capabilities of males relative to females so that the OSR becomes femalerather than male-biased (8, 9). In such role-reversed species, females are competitive, more highly ornamented (Fig. 1), and actively court males, whereas males are choosy in mate choice. The theory, then, can be extended to predict both ‘‘normal’’ and reversed sex roles from prevailing OSR, rather than focusing explanations on male-competitive, femalechoosy sex roles (although this may be the more common occurrence). A further lack of generality in sex role theory lies in the common but unnecessary assumption that either females choose and males compete (most commonly) or males choose and females compete (less commonly) and that therefore either males or females evolve ornaments and weapons. As a result, male mate choice is rarely studied in species in which females show strong mating preferences based on conspicuous ornaments of males. Guppies (Poecilia reticulata; Fig. 2), for example, have been the subject of intensive studies of color pattern evolution in males and mate choice evolution in females (10), but work on mate choice by males in this species, which is easily observable, has lagged far behind. A more complete view of sex roles and sexual selection is to realize that either sex may be expected to exercise discrimination in mating given that the potential for mating repeatedly is not unlimited, that females vary in quality, and thus that the relative degree of mating competition and mating discrimination in each sex will affect the evolutionary outcome with regard to sex roles and the evolution of secondary sexual characteristics (11–14). In most cases, however, male mate choice appears to be based on variation in female fecundity or reproductive state and is easily explained. Amundsen and Forsgren’s work illustrates the broader concept of sex roles and sexual selection far more dramatically by demonstrating male mate choice based on a seemingly ornamental characteristic of females in a species that does not seem to have behavioral role reversal. Two-spotted gobies appear at first to fit sex role stereotypes as usually conceived quite well. Males are larger than females,