Sex-role reversal in vertebrates: behavioural and endocrinological accounts
Introduction
Since Darwin (1871) proposed the concept of sexual selection to explain the evolution of sex differences, there have been impressive empirical and theoretical advances in this field (Andersson, 1994, Bateman, 1948, Clutton-Brock and Parker, 1992, Emlen and Oring, 1977, Trivers, 1972). Although some degree of competition for mates is common in both sexes of most species, the predominant pattern in animals is that of males competing more intensely for mates than females (Andersson, 1994). In many animals, males also develop secondary sexual characters such as conspicuous colours, exaggerated ornaments, or menacing weapons. In general, female reproductive success is limited by gamete production, whereas male success is limited by mate availability (Bateman, 1948). Hence, males are under strong selection to acquire mates. In some animals, nevertheless, females compete more intensely than males for access to mates. Such species are typically described as sex-role reversed (Trivers, 1972, Williams, 1966, Williams, 1975) and they provide critical tests of the generality of theories pertaining to the strength of sexual selection (Andersson, 1994, Jones et al., 2000, Okuda, 1999, Vincent et al., 1992). In these species with mainly paternal care, the sex differences in parental roles can apparently override the effects of anisogamy and lead to a reversal of other aspects of sex roles and sexual dimorphism (Andersson, 1994). As we will see later, current parental investment theory asserts that regardless of whether males or females provide parental care, the sex with the higher potential reproductive rate will compete more strongly for mates (Clutton-Brock and Vincent, 1991).
Although studies of reproductive patterns have historically neglected female behaviour and focused instead on the more common phenomenon of male–male competition for access to females or on male secondary sexual characteristics, there has recently been a surge of interest on female sexual behaviour and on female–female competition (Ahnesjö et al., 1993, Berglund et al., 1993, Okuda, 1999, Swenson, 1997, Vincent et al., 1992). Since Darwin (1871) and Williams (1966) drew attention to sex-role reversed behaviour, an increasing number of examples has come to light (Trivers, 1985, Andersson, 1994). Sex-role reversal has now been documented or suggested in insects, fish, amphibians, and birds.
During the last three decades, numerous papers have proposed various determinants of sexual selection. Trivers' concept of parental investment (PI) was a major advance in sexual selection theory that helps to explain sex differences in mating competition and to predict which sex would compete more intensely for mates (Trivers, 1972). The sex that invests less in offspring should compete more for mates because that sex reproduces more often, leading to scarcity of sexually active members of the opposite sex. Trivers' PI theory has subsequently been revised by many researchers who have suggested that it is the operational sex ratio (OSR), rather than the relative PI, that is the causal factor in the evolution of sex roles (see Owens and Thompson, 1994). Emlen and Oring (1977) introduced the concept of the OSR (defined as the ratio of fertilizable females to sexually active males in a population at a given time) as an empirical measure of the sex bias in reproductive animals. Emlen and Oring were the first to suggest that sex roles were determined by the relative abundance of each sex and they argued that the more abundant sex should be the more competitive one. Because PI and OSR can be difficult to measure in nature, the potential reproductive rate (PRR), i.e. the maximum number of independent offspring that each parent can produce per unit of time, has been proposed as an empirical measure for predicting the direction of mating competition (Clutton-Brock and Vincent, 1991). They predicted that the mating competition would be more intense among the sex with higher PRR. Recently, additional theoretical work has suggested that courtship roles are determined by a combination of OSR, PI and the relative time involved in reproductive tasks (‘time out’) versus the amount of time each sex is available to mate (‘time in’; Parker and Simmons, 1996; see also Kvarnemo and Ahnesjö, 1996). Another determinant of mating competition is mate quality: where the PRR is similar in the two sexes, the relative benefits of acquiring qualitatively superior mates, rather than the OSR, may determine the comparative intensity of mating competition in the two sexes (Clutton-Brock and Vincent, 1991, Owens and Thompson, 1994, Petrie, 1983).
Whatever the reasons for sex-role reversal (e.g. PRR, OSR, differences in mate quality or parental investment), when it occurs, theory predicts: (1) stronger female than male competition for mates; (2) more critical choice of mate by males; (3) higher variance in female than male mating success; and (4) more pronounced female secondary sex traits and mate-attracting displays (Andersson, 1994, Trivers, 1985).
In this paper, we survey the occurrence of sex-role reversal in vertebrates. We focus on behavioural aspects of sex-role reversal and we examine possible hormonal correlates of this phenomenon.
Section snippets
Fishes
Although male care of offspring is the dominant parental care pattern in teleost fish, males are also generally the predominant competitors for mates and evidence for sex-role reversal is rare (Vincent, 1992, Vincent et al., 1992). This is probably because the most common forms of paternal care do not usually depress male PRRs below that of females: egg guarding, nest building and fanning do not prevent males from caring simultaneously or in quick succession for several clutches (Clutton-Brock
Discussion
In this paper, we surveyed the occurrence of sex-role reversal in vertebrates, focusing in particular on behavioural aspects of sex-role reversal and on endocrinological correlates of this phenomenon. We did not pay attention to the reasons for sex-role reversal in the animals mentioned which are still obscure and debated (Andersson, 1994).
As mentioned earlier, the OSR is central in predicting the intensity of mating competition and which sex is competing for which (Kvarnemo and Ahnesjö, 1996).
Acknowledgements
We thank three anonymous referees for their comments which improved the paper. This study was supported by the Research Council of the University of Antwerp (NOI BOF UA 1997) and a FWO Research Project (G.0075.98). Marcel Eens is a Research Associate of the F.W.O. — Flanders.
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2020, Advances in the Study of BehaviorCitation Excerpt :Empirical evidence for the role of OSR in determining sex roles comes from rare cases where interactions between ecology and reproduction cause a reversal in sex roles (Kokko & Jennions, 2008; Williams, 1966). Sex role reversal is characterized by choosy males and aggressive, competitive, and polygamous females (Andersson, 1994; Eens & Pinxten, 2000). The primary ecological driver of sex role reversal is a shift in the OSR in favor of females; this happens when males become the reproductively limiting resource, usually as a result of increased male reproductive investment, causing in turn a decrease in male PRR (Eens & Pinxten, 2000; Gwynne, 1991; Parker & Simmons, 1996).