Polyandry and Mating System Evolution

Abstract

Our understanding of animal mating systems has been considerably enhanced in recent years by the development of molecular methods to reliably assay female multiple mating (polyandry). These techniques have demonstrated that polyandry is widespread across animal groups, even in species thought to be strictly monogamous and pair‐bonded. The research that has arisen from this paradigm shift has shown that females can gain substantial material benefits from mating with multiple males, in terms of increased fecundity, infanticide avoidance and sperm replenishment. Polyandry can also provide indirect or genetic benefits to females, increasing the likelihood that they will mate with at least one compatible or high‐quality male. By mating multiply females can also increase the genetic diversity of their offspring, which may be advantageous in changeable environments. Importantly polyandry has demonstrated that mating systems extend beyond copulation and sexual selection occurs not just over mates but also over their gametes.

Key Concepts

  • Recent developments in molecular ecology have allowed researchers to rapidly and easily test whether multiple fathers sire female offspring.
  • Multiple mating by females (polyandry) is now known to be widespread across taxa.
  • While mating can be costly, polyandry has been shown to provide substantial benefits to females.
  • Direct, or material benefits of polyandry increase female offspring production, for instance by providing females with additional resources in nuptial gifts or seminal fluids.
  • Indirect, or genetic benefits of polyandry arise when multiple mating increases the chances that a female mates with at least one compatible or high‐quality male.
  • Polyandry can also increase offspring genetic diversity, and this can be beneficial in unstable or harsh environments, increasing the chances that at least some offspring will survive.
  • Polyandry means that sexual selection continues after mating, males compete not only for mates but also their gametes (post‐copulatory sexual selection).
  • Post‐copulatory sexual selection can render certain male traits beneficial, which can alter the costs and benefits of polyandry for females and change the optimal female mating rate.
  • As a result of the realisation that polyandry is widespread, mating systems research now integrates formerly unappreciated concepts such as sperm competition, cryptic female choice and co‐evolutionary feedbacks between male and female mating strategies.

Keywords: polyandry; mating systems; mate choice; sexual selection; sexual conflict

Figure 1. How selection operates on the female mating rate under convenience polyandry, benefits‐driven polyandry, and null polyandry. When the costs of resistance (CR) exceed the costs of mating (CM) polyandry can be convenient (orange). When polyandry is beneficial CM < CR (blue). Under null polyandry (green), selection acts to reduce the risk of mating failure (MF). In this figure, we show how different forms of polyandry can result in selective feedback loops between sexually selected male traits (grey boxes, dashed outline) and the female mating rate. For instance, convenience polyandry and null polyandry generate selection on males that may facilitate benefits‐driven polyandry. Likewise, if strategic ejaculate allocation renders females sperm depleted, selection will increase the female mating rate (to reduce mating failures, MF). Boulton et al. (). Reproduced with permission of Elsevier.
Figure 2. (a) A male dance fly (Diptera: Empididae) provides a female with a nuptial gift which she consumes during copulation. Courtesy of Tom Houslay. (b) A newly mated female Mormon cricket (Orthoptera: Tettigoniidae) bends to consume a spermatophylax (the edible part surrounding the spermatophore) transferred by the male. Courtesy of Darryl Gwynne. Nuptial gift giving can increase the likelihood that a female will mate with the gift giver and/or increase the time in‐copula (which can increase sperm transfer and improve fertilisation success). Gift‐giving also increases the benefits of polyandry particularly for food‐deprived females.
Figure 3. A simple model of the effects of increased mating rate on female fitness. In species in which nuptial feeding occurs (I), female fitness is expected to increase with mating rate. As females become saturated, however, the net effects of further elevated mating rate should become insignificant. In species without nuptial feeding (II), in contrast, female fitness should be maximised at a relatively well‐defined optimal mating rate (A). Arnqvist and Nilsson (). Reproduced with permission of Elsevier.
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Birkhead TR and Møller AP (eds) (1998) Sperm Competition and Sexual Selection. Academic Press: San Diego.

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Boulton RA and Shuker DM (2013) Polyandry. Current Biology 23 (24): R1080–R1081.

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Parker GA and Birkhead TR (2013) Polyandry: the history of a revolution. Philosophilcal Transactions of the Royal Society B 368 (1613): 20120335.

Shuker DM and Simmons LW (eds) (2014) The Evolution of Insect Mating Systems. Oxford University Press: Oxford.

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Boulton, Rebecca A(May 2020) Polyandry and Mating System Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0029005]