Elsevier

Behavioural Processes

Volume 51, Issues 1–3, 5 October 2000, Pages 135-147
Behavioural Processes

Sex-role reversal in vertebrates: behavioural and endocrinological accounts

https://doi.org/10.1016/S0376-6357(00)00124-8Get rights and content

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.

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.

References (90)

  • C. Kvarnemo et al.

    The dynamics of operational sex ratios and competition for mates

    Trends Ecol. Evol.

    (1996)
  • H.D. Masonjones et al.

    Differences in potential reproductive rates of male and female seahorses related to courtship roles

    Anim. Behav.

    (2000)
  • N. Okuda et al.

    Filial cannibalism in a paternal mouthbrooding fish in relation to mate availability

    Anim. Behav.

    (1996)
  • L.W. Oring

    Avian mating systems

  • L.W. Oring et al.

    Hormonal changes associated with natural and manipulated incubation in the sex-role reversed Wilson's phalarope

    Gen. Comp. Endocrinol.

    (1988)
  • L.W. Oring et al.

    Seasonal changes in prolactin and luteinizing hormone in the polyandrous spotted sandpiper, Actitis macularia

    Gen. Comp. Endocrinol.

    (1986)
  • E.F. Rissman et al.

    Hormonal correlates of polyandry in the Spotted Sandpiper, Actitis macularia

    Gen. Comp. Endocrinol.

    (1984)
  • G. Rosenqvist

    Male mate choice and female–female competition for mates in the pipefish Nerophis ophidion

    Anim. Behav.

    (1990)
  • M.L. Stephens

    Male takeover and possible infanticide by a female northern jacana (Jacana spinosa)

    Anim. Behav.

    (1982)
  • K. Summers

    Sexual selection and intra-female competition in the green poison-dart frog, Dendrobates auratus

    Anim. Behav.

    (1989)
  • K. Summers

    Mating strategies in two species of dart-poison frogs: a comparative study

    Anim. Behav.

    (1992)
  • A. Vincent et al.

    Pipefishes and seahorses: are they all sex role reversed?

    Trends Ecol. Evol.

    (1992)
  • I. Ahnesjö

    Consequences of male brood care, weight and number of newborn in a sex-role reversed pipefish

    Funct. Ecol.

    (1992)
  • I. Ahnesjö

    Fewer newborn result in superior juveniles in the paternally brooding pipefish Syngnathus typhle

    J. Fish. Biol.

    (1992)
  • I. Ahnesjö et al.

    The role of females in influencing mating patterns

    Behav. Ecol.

    (1993)
  • M. Andersson
  • G.F. Ball
  • S. Balshine-Earn et al.

    Sex-role reversal in the Black-chinned Tilapia, Sarotherodon melanotheron (Rüppel) (Cichlidae)

    Behaviour

    (1995)
  • A.J. Bateman

    Intra-sexual selection in Drosophila

    Heredity

    (1948)
  • A. Berglund

    Egg competition in a sex-role reversed pipefish: subdominant females trade reproduction for growth

    Evolution

    (1991)
  • A. Berglund et al.

    Reversed sex roles and parental energy investment in zygotes of two pipefish (Syngnathidae) species

    Mar. Ecol. Prog. Ser.

    (1986)
  • A. Berglund et al.

    Mate choice, fecundity and sexual dimorphism in two pipefish species (Syngnathidae)

    Behav. Ecol. Sociobiol.

    (1986)
  • A. Berglund et al.

    Male limitation of female reproductive success in a pipefish: effects of body-size differences

    Behav. Ecol. Sociobiol.

    (1990)
  • A. Berglund et al.

    Reproductive success of females limited by males in two pipefish species

    Am. Nat.

    (1989)
  • A. Berglund et al.

    Female–female competition over reproduction

    Behav. Ecol.

    (1993)
  • A. Berglund et al.

    Ornamentation predicts reproductive success in female pipefish

    Behav. Ecol. Sociobiol.

    (1997)
  • J.D. Bunting et al.

    An analysis of sex and breeding stage differences in prolactin binding activity in brain and hypothalamic GnRH concentrations in Wilson's Phalarope, a sex role-reversed species

    Gen. Comp. Endocrinol.

    (1998)
  • S.H.M. Butchart

    Population structure and breeding system of the sex-role reversed, polyandrous Bronze-winged Jacana Metopidius indicus

    Ibis

    (2000)
  • T.H. Clutton-Brock et al.

    Potential reproductive rates and the operation of sexual selection

    Quart. Rev. Biol.

    (1992)
  • T.H. Clutton-Brock et al.

    Sexual selection and the potential reproductive rates of males and females

    Nature

    (1991)
  • J. Dale et al.

    Frequency and timing of extrapair fertilisation in the polyandrous red phalarope (Phalaropus fulicarius)

    Behav. Ecol. Sociobiol.

    (1999)
  • C. Darwin

    The descent of man, and selection in relation to sex

    (1871)
  • C.M. Drea et al.
  • Eens, M. Van Duyse, E. Pinxten, R., 1998. Sex role reversal in the moorhen: behavioral and endocrinological evidence....
  • S.T. Emlen et al.

    Ecology, sexual selection, and the evolution of mating systems

    Science

    (1977)
  • Cited by (116)

    • Ecological determinants of sex roles and female sexual selection

      2020, Advances in the Study of Behavior
      Citation 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).

    View all citing articles on Scopus
    View full text