Sexual Conflict Arising from Extrapair Matings in Birds

Abstract

The discovery that extrapair copulation (EPC) and extrapair paternity (EPP) are common in birds led to a paradigm shift in our understanding of the evolution of mating systems. The prevalence of extrapair matings in pair-bonded species sets the stage for sexual conflict, and a recent focus has been to consider how this conflict can shape variation in extrapair mating rates. Here, we invert the causal arrow and consider the consequences of extrapair matings for sexual conflict. Extrapair matings shift sexual conflict from a simple two-player (male vs. female) game to a game with three or more players, the nature of which we illustrate with simple diagrams that highlight the net costs and benefits of extrapair matings to each player. This approach helps identify the sorts of traits that might be under selection because of sexual conflict. Whether EPP is driven primarily by the extrapair male or the within-pair female profoundly influences which players are in conflict, but the overall pattern of conflict varies little among different mating systems. Different aspects of conflict are manifest at different stages of the breeding cycle and can be profitably considered as distinct episodes of selection caused by conflict. This perspective is illuminating both because conflict between specific players can change across episodes and because the traits that evolve to mediate conflict likely differ between episodes. Although EPP clearly leads to sexual conflict, we suggest that the link between sexual conflict and multiple paternity might be usefully understood by examining how deviations from lifetime sexual monogamy influence sexual conflict.T he development of genetic tools for determining parentage fundamentally altered our understanding of animal mating systems (Jeffreys et al. 1985;Avise 1996;Reynolds 1996) and provided invaluable insights into the consequences and causes of females mating with more than one male. Particularly for the study of birds, these methods revealed that social pair bonds often fail to match the actual patterns of copulations that produced offspring (Gowaty and Karlin 1984;Birkhead and Møller 1992;Reynolds 1996;Petrie and Kempenaers 1998), revolutionizing the study of avian mating systems. Extensive research and two recent reviews point out the progress we have made in this field and show how little we still understand extrapair behavior (Griffith et al. 2002;Westneat and Stewart 2003).

Extrapair mating and the strength of sexual selection: insights from a polymorphic species

“…Females may gain genetic or direct benefits for offspring through multiple, extrapair mating (Foerster et al 2003;Suter et al 2007;Townsend et al 2010). However, the hypothesis that females elevate fitness through multiple mating is not consistently supported, and substantial costs are also possible, for instance, injury, disease transmission, and loss of paternal support (Westneat and Rambo 2000;Westneat and Stewart 2003;Albrecht et al 2006;Akçay and Roughgarden 2007;Chaine et al 2015). Rather than deriving benefits, extrapair mating by females may instead occur due to male coercion (Westneat and Stewart 2003), or arise through nonadaptive genetic correlation with males (Halliday and Arnold 1987;Forstmeier et al 2014).…”

High fidelity: extra‐pair fertilisations in eight Charadrius plover species are not associated with parental relatedness or social mating system

“…First, females may seek out copulations with extra‐pair males if this increases their reproductive success even though these EPCs reduce the reproductive success of their social mate (Westneat and Stewart , Székely et al ). Interactions between the female, her social mate and other members of the population can lead to complex dynamics, since the social mate may retaliate and subsequently reduce his care (Chaine et al ). Second, EPP can lead to brood desertion whereby one, or both, parents abandon their young and seek out new mates to increase their reproductive success (Székely ).…”

Postmating sexual conflict and female control over fertilization during gamete interaction

“…Covert EPCs unbeknownst to their social partner present to be a reliable counterstrategy that allows females to benefit from mating multiply but also offset any potential loss of male care. Sexual conflict now becomes a multiplayer game not only involving a male–female pair but also extra‐pair partner/s …”

“…For example, serial monogamy will create conflict over parental care, while female multiple mating (polyandry), including pair-bonds with extra-pair copulations (EPCs) and multipartner systems, will lead to conflict over parental care and fertilization. 42 A number of theories have been developed to account for the evolution of polyandry, [43][44][45] and empirical studies have confirmed that females can gain fitness benefits by copulating with more than one male to create a situation where rival ejaculates compete for fertilizations. [46][47][48][49][50][51][52][53][54] Selection via sperm competition is expected to favor traits that enhance competitive paternity success and elevate male fitness.…”

“…Sexual conflict now becomes a multiplayer game not only involving a male-female pair but also extra-pair partner/s. 42,70 After mating, disparity over paternity outcomes is recognized to be a common source of sexual conflict, and both sexes have evolved different strategies to manipulate sperm that are locked in competition within the FRT (in females referred to as cryptic female choice (CFC)). 25,26 Internal fertilization typically results in a delay between mating and gamete fusion, and thus requires sperm to remain viable from the time of insemination until the time of ovulation.…”