Feed-backs among inbreeding, inbreeding depression in sperm traits, and sperm competition can drive evolution of costly polyandry

Abstract

Ongoing ambitions are to understand the evolution of costly polyandry and its consequences for species ecology and evolution. Emerging patterns could stem from feed‐back dynamics between the evolving mating system and its genetic environment, defined by interactions among kin including inbreeding. However, such feed‐backs are rarely considered in nonselfing systems. We use a genetically explicit model to demonstrate a mechanism by which inbreeding depression can select for polyandry to mitigate the negative consequences of mating with inbred males, rather than to avoid inbreeding, and to elucidate underlying feed‐backs. Specifically, given inbreeding depression in sperm traits, costly polyandry evolved to ensure female fertility, without requiring explicit inbreeding avoidance. Resulting sperm competition caused evolution of sperm traits and further mitigated the negative effect of inbreeding depression on female fertility. The evolving mating system fed back to decrease population‐wide homozygosity, and hence inbreeding. However, the net overall decrease was small due to compound effects on the variances in sex‐specific reproductive success and paternity skew. Purging of deleterious mutations did not eliminate inbreeding depression in sperm traits or hence selection for polyandry. Overall, our model illustrates that polyandry evolution, both directly and through sperm competition, might facilitate evolutionary rescue for populations experiencing sudden increases in inbreeding.

An Inconvenient Truth: The Unconsidered Benefits of Convenience Polyandry

“…What is more, other bet-hedging strategies that promote genetic diversity [17] and genetic compatibility [49], or ensure fertility under inbreeding [49] or outbreeding [9], might mean that polyandry is the optimal strategy for an individual to adopt because it spreads the risk of mating failure [19; 33; 51-52]. Moreover, polyandry can be advantageous to populations, for instance reducing extinction risk by purging mutation load, increasing effective population size [53] and rescuing populations from the effects of inbreeding [22]. Indeed, the importance of polyandry in preventing extinction has been demonstrated in populations of Drosophila pseudobscura harbouring a selfish X-linked drive [ If polyandry arises because of a baseline level of receptivity that ensures fertility, but leads to multiple mating across the population, then we should re-evaluate the convenience polyandry hypothesis.…”

“…Polyandry may represent another area where socio-cultural unconscious biases have influenced interpretations of female mating behaviour (45). The lack of thorough theoretical and empirical scrutiny that the convenience polyandry hypothesis has received, which contrasts markedly with the benefits-driven and bet-hedging approaches [16][17][18][19][20][21][22], leads us to question why convenience is commonly described as an explanation for female multiple mating. We suggest that socio-normative biases about female behaviour may contribute to this pattern.…”

“…Importantly, the idea that females engage in polyandry not to gain benefits, but rather to limit the costs imposed upon them by harassing males, has been discussed throughout the polyandry revolution. This hypothesis is known as convenience polyandry [2], and while it continues to be highlighted by those seeking to understand why females engage in multiple matings [for recent papers see: 6-17], we argue that it would benefit from more rigorous theoretical and empirical testing that other, benefits-driven hypotheses for the evolution of polyandry, have been subject [16][17][18][19][20][21][22].…”

The Consequences of Polyandry for Sibship Structures, Distributions of Relationships and Relatedness, and Potential for Inbreeding in a Wild Population

“…Simultaneous polyandry is widely hypothesized to have evolved to facilitate inbreeding avoidance in populations where relatives interact and inbreeding depression is strong (e.g., Stockley et al 1993;Tregenza and Wedell 2000;Michalczyk et al 2011;Duthie et al 2016;Bocedi and Reid 2017). Consequently, numerous empirical studies on diverse systems have tested whether polyandrous females avoid inbreeding by expressing precopulatory and/or postcopulatory choice for less closely related mates (Keller and Arcese 1998;Tregenza and Wedell 2002;Reid et al 2006Reid et al , 2015aFirman and Simmons 2008;Brouwer et al 2011).…”

No evidence of inbreeding depression in sperm performance traits in wild song sparrows

“…Such inbreeding depression could reduce male and hence female fertilities and thereby reduce individual and population‐wide reproductive fitness (Pizzari & Parker, ; Snow & Spira, ). Furthermore, by reducing female fertility through sperm limitation, inbreeding depression in sperm traits could potentially drive evolution of female multiple mating (Bocedi & Reid, ; see also Birkhead & Pizzari, ; Forbes, ). As female multiple mating causes sperm competition (i.e., postcopulatory competition among different males’ sperm to fertilize ova, Parker, ), inbreeding depression in male sperm traits and fertilization success might then be exacerbated in an analogous way as precopulatory competition exacerbates inbreeding depression in male mating success (Joron & Brakefield, ; Meagher, Penn, & Potts, ).…”