Behavioural Processes 51 (2000) 135–147 www.elsevier.com/locate/behavproc Sex-role reversal in vertebrates: behavioural and endocrinological accounts Marcel Eens *, Rianne Pinxten Department of Biology, Uni6ersity of Antwerp, U.I.A., Uni6ersiteitsplein 1, B-2610 Wilrijk Belgium Received 23 December 1999; received in revised form 20 May 2000; accepted 23 May 2000 Abstract Sex-role reversal occurs when females compete more intensely than males for access to mates. 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 endocrinological correlates of this phenomenon. The best documented cases among vertebrates of sex-role reversal occur in fish and birds. In nearly all sex-role reversed species or populations, females have higher potential reproductive rates than males. Some species in which females were previously thought to be the predominant competitors for mates (for instance seahorses and a dendrobatid frog), appear not to be sex-role reversed according to recent studies. The endocrinology of sex-role reversal has been studied in only a few species and therefore remains poorly understood. In birds, which probably have been studied the most in this respect, steroid hormones appear to follow the typical ancestral conditions (for instance no reversal of testosterone levels) in sex-role reversed species, whereas prolactin, a principal regulator of the onset and maintenance of incubation, departs from the usual avian pattern in that it is higher in males than in females. The study of sex-role reversed behaviour offers unique opportunities not only to test sexual selection theory, but also to enhance our understanding of the neuroendocrine mechanisms mediating behavioural sex differences. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Aggression; Female–female competition; Parental investment; Sex-role reversal; Sexual selection; Testosterone 1. Introduction 1994; Bateman, 1948; Clutton-Brock and Parker, 1992; Emlen and Oring, 1977; Trivers, 1972). Al- Since Darwin (1871) proposed the concept of though some degree of competition for mates is sexual selection to explain the evolution of sex common in both sexes of most species, the pre- differences, there have been impressive empirical dominant pattern in animals is that of males and theoretical advances in this field (Andersson, competing more intensely for mates than females (Andersson, 1994). In many animals, males also develop secondary sexual characters such as con- * Corresponding author. Tel.: +32-3-8202284; fax: +32-3- spicuous colours, exaggerated ornaments, or men- 8202271. E-mail addresses: [email protected] (M. Eens), pin- acing weapons. In general, female reproductive [email protected] (R. Pinxten). success is limited by gamete production, whereas 0376-6357/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S0376-6357(00)00124-8 136 M. Eens, R. Pinxten / Beha6ioural Processes 51 (2000) 135–147 male success is limited by mate availability researchers who have suggested that it is the (Bateman, 1948). Hence, males are under strong operational sex ratio (OSR), rather than the rela- selection to acquire mates. In some animals, nev- tive PI, that is the causal factor in the evolution of ertheless, females compete more intensely than sex roles (see Owens and Thompson, 1994). Em- males for access to mates. Such species are typi- len and Oring (1977) introduced the concept of cally described as sex-role reversed (Trivers, 1972; the OSR (defined as the ratio of fertilizable fe- Williams, 1966, 1975) and they provide critical males to sexually active males in a population at a tests of the generality of theories pertaining to the given time) as an empirical measure of the sex strength of sexual selection (Andersson, 1994; bias in reproductive animals. Emlen and Oring Jones et al., 2000; Okuda, 1999; Vincent et al., were the first to suggest that sex roles were deter- 1992). In these species with mainly paternal care, mined by the relative abundance of each sex and the sex differences in parental roles can appar- they argued that the more abundant sex should be ently override the effects of anisogamy and lead the more competitive one. Because PI and OSR to a reversal of other aspects of sex roles and can be difficult to measure in nature, the potential sexual dimorphism (Andersson, 1994). As we will reproductive rate (PRR), i.e. the maximum num- see later, current parental investment theory as- ber of independent offspring that each parent can serts that regardless of whether males or females produce per unit of time, has been proposed as an provide parental care, the sex with the higher empirical measure for predicting the direction of potential reproductive rate will compete more mating competition (Clutton-Brock and Vincent, strongly for mates (Clutton-Brock and Vincent, 1991). They predicted that the mating competition would be more intense among the sex with higher 1991). PRR. Recently, additional theoretical work has Although studies of reproductive patterns have suggested that courtship roles are determined by a historically neglected female behaviour and fo- combination of OSR, PI and the relative time cused instead on the more common phenomenon involved in reproductive tasks (‘time out’) versus of male–male competition for access to females or the amount of time each sex is available to mate on male secondary sexual characteristics, there (‘time in’; Parker and Simmons, 1996; see also has recently been a surge of interest on female Kvarnemo and Ahnesjo¨, 1996). Another determi- sexual behaviour and on female–female competi- nant of mating competition is mate quality: where tion (Ahnesjo¨ et al., 1993; Berglund et al., 1993; the PRR is similar in the two sexes, the relative Okuda, 1999; Swenson, 1997; Vincent et al., benefits of acquiring qualitatively superior mates, 1992). Since Darwin (1871) and Williams (1966) rather than the OSR, may determine the compar- drew attention to sex-role reversed behaviour, an ative intensity of mating competition in the two increasing number of examples has come to light sexes (Clutton-Brock and Vincent, 1991; Owens (Trivers, 1985; Andersson, 1994). Sex-role reversal and Thompson, 1994; Petrie, 1983). has now been documented or suggested in insects, Whatever the reasons for sex-role reversal (e.g. fish, amphibians, and birds. PRR, OSR, differences in mate quality or During the last three decades, numerous papers parental investment), when it occurs, theory pre- have proposed various determinants of sexual se- dicts: (1) stronger female than male competition lection. Trivers’ concept of parental investment for mates; (2) more critical choice of mate by (PI) was a major advance in sexual selection males; (3) higher variance in female than male theory that helps to explain sex differences in mating success; and (4) more pronounced female mating competition and to predict which sex secondary sex traits and mate-attracting displays would compete more intensely for mates (Trivers, (Andersson, 1994; Trivers, 1985). 1972). The sex that invests less in offspring should In this paper, we survey the occurrence of compete more for mates because that sex repro- sex-role reversal in vertebrates. We focus on be- duces more often, leading to scarcity of sexually havioural aspects of sex-role reversal and we ex- active members of the opposite sex. Trivers’ PI amine possible hormonal correlates of this theory has subsequently been revised by many phenomenon. M. Eens, R. Pinxten / Beha6ioural Processes 51 (2000) 135–147 137 2. Evidence for sex-role reversal in vertebrates ation (but see also Masonjones and Lewis, 2000). A classical example of sex-role reversal is found 2.1. Fishes in pipefishes (Vincent et al., 1992). Two species, Nerophis ophidion and Syngnathus typhle, have Although male care of offspring is the dominant been studied in great detail. In both species, fe- parental care pattern in teleost fish, males are also males produce more eggs than the male brood- generally the predominant competitors for mates pouches can accommodate (Berglund and and evidence for sex-role reversal is rare (Vincent, Rosenqvist, 1990; Berglund et al., 1989). This 1992; Vincent et al., 1992). This is probably be- reproductive inequality results in a female-biased cause the most common forms of paternal care do OSR, causing the above mentioned sex-role rever- not usually depress male PRRs below that of sal (Clutton-Brock and Parker, 1992). Observa- females: egg guarding, nest building and fanning tional and experimental evidence obtained in these do not prevent males from caring simultaneously two species is consistent with the predictions of or in quick succession for several clutches (Clut- the sexual selection theory. First, females are the ton-Brock and Vincent, 1991; Vincent, 1992). predominant competitors for access to mates, and Nonetheless, some forms of teleost paternal care competition is primarily indirect (Berglund, 1991; do not permit the male to care quickly for large Rosenqvist, 1990). Second, males are more selec- number of eggs, and recent theory predicts fe- tive than females in accepting mates (Berglund et males to compete more intensely for mates in al., 1986b; Rosenqvist, 1990). Males benefit di- those species in which females have higher PRRs rectly from being choosy by selecting larger fe- than males. Such sex-role reversal is most proba- males that provide more and larger eggs (Berglund ble in those species in which males bear eggs et al., 1986a,b), which give rise to heavier and and/or embryos on their body, and consequently higher quality offspring (Ahnesjo¨, 1992a,b). may be severely restricted in the time or space Third, females of both species appear to be most available for brooding eggs, and in species where modified by sexual selection. In N. ophidion, sex- males provide extraordinarily lengthy care or ual dimorphism is most pronounced: females are build specialized nests which limit brood size (Vin- larger, have a bright blue colouration along their cent, 1992).