When does female multiple mating evolve to adjust inbreeding? Effects of inbreeding depression, direct costs, mating constraints, and polyandry as a threshold trait

Abstract

Polyandry is often hypothesized to evolve to allow females to adjust the degree to which they inbreed. Multiple factors might affect such evolution, including inbreeding depression, direct costs, constraints on male availability, and the nature of polyandry as a threshold trait. Complex models are required to evaluate when evolution of polyandry to adjust inbreeding is predicted to arise. We used a genetically explicit individual‐based model to track the joint evolution of inbreeding strategy and polyandry defined as a polygenic threshold trait. Evolution of polyandry to avoid inbreeding only occurred given strong inbreeding depression, low direct costs, and severe restrictions on initial versus additional male availability. Evolution of polyandry to prefer inbreeding only occurred given zero inbreeding depression and direct costs, and given similarly severe restrictions on male availability. However, due to its threshold nature, phenotypic polyandry was frequently expressed even when strongly selected against and hence maladaptive. Further, the degree to which females adjusted inbreeding through polyandry was typically very small, and often reflected constraints on male availability rather than adaptive reproductive strategy. Evolution of polyandry solely to adjust inbreeding might consequently be highly restricted in nature, and such evolution cannot necessarily be directly inferred from observed magnitudes of inbreeding adjustment.

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).…”

“…For instance, polyandrous females might produce female and/or male offspring of higher additive genetic or phenotypic value for fitness (e.g., Garcia-Gonzalez and Simmons 2005;Forstmeier et al 2011;Reid and Sardell 2012) or produce offspring that are less inbred and hence express less inbreeding depression (Stockley et al 1993;Wedell 2000, 2002;Michalczyk et al 2011;Duthie et al 2016). However, such mechanisms often require some form of active female mate choice and/or paternity allocation, which may impose additional costs such as male harassment or increased risk of predation during mate searching (e.g., Rowe et al 1994Rowe et al , 1998Parker and Pizzari 2010;Duthie et al 2016) or invoke genetic constraints on female strategies (Forstmeier et al 2011(Forstmeier et al , 2014. Further, empirical evidence of substantial indirect fitness benefits to polyandrous females' offspring remains scant (Jennions and Petrie 2000; Arnqvist and Kirkpatrick 2005;Evans and Simmons 2008;Reid and Sardell 2012;Forstmeier et al 2014;Hsu et al 2014).…”

Evolution of precopulatory and post-copulatory strategies of inbreeding avoidance and associated polyandry

“…Further, such polyandry might itself evolve because it allows females to mate with additional unrelated males following an initial mating with a relative, potentially including males that were unavailable for initial mate choice (e.g. Reid et al ., ; Duthie et al ., ). Polyandry can thereby facilitate precopulatory inbreeding avoidance even without any post‐copulatory female choice or otherwise biased fertilization among sperm (i.e.…”

“…Key requirements were that direct negative selection (i.e. ‘costs’) on polyandry was weak, that very few males were available for a female's initial mate choice but many were available for additional mate choice(s) or that polyandry was conditionally expressed when a focal female was related to her initial mate (Duthie et al ., ). Without these conditions, polyandrous females tended to increase rather than decrease their overall degree of inbreeding, ultimately reducing offspring fitness.…”

“…In one‐first step, Duthie et al . () used a genetically explicit individual‐based model to examine conditions under which polyandry is predicted to evolve due to selection stemming from precopulatory inbreeding avoidance in the absence of post‐copulatory inbreeding avoidance. Simulations showed that even when selection for precopulatory inbreeding avoidance was strong and females consequently preferred unrelated mates, selection for polyandry specifically to facilitate this inbreeding avoidance occurred only under highly restricted conditions.…”