Female and male genetic effects on offspring paternity: additive genetic (co)variances in female extra-pair reproduction and male paternity success in song sparrows (Melospiza melodia).

Jane M Reid,Lukas F Keller,Peter Arcese,Sylvain Losdat

doi:10.1111/evo.12424

Abstract

Ongoing evolution of polyandry, and consequent extra-pair reproduction in socially monogamous systems, is hypothesized to be facilitated by indirect selection stemming from cross-sex genetic covariances with components of male fitness. Specifically, polyandry is hypothesized to create positive genetic covariance with male paternity success due to inevitable assortative reproduction, driving ongoing coevolution. However, it remains unclear whether such covariances could or do emerge within complex polyandrous systems. First, we illustrate that genetic covariances between female extra-pair reproduction and male within-pair paternity success might be constrained in socially monogamous systems where female and male additive genetic effects can have opposing impacts on the paternity of jointly reared offspring. Second, we demonstrate nonzero additive genetic variance in female liability for extra-pair reproduction and male liability for within-pair paternity success, modeled as direct and associative genetic effects on offspring paternity, respectively, in free-living song sparrows (Melospiza melodia). The posterior mean additive genetic covariance between these liabilities was slightly positive, but the credible interval was wide and overlapped zero. Therefore, although substantial total additive genetic variance exists, the hypothesis that ongoing evolution of female extra-pair reproduction is facilitated by genetic covariance with male within-pair paternity success cannot yet be definitively supported or rejected either conceptually or empirically.

Highlights

One intriguing and influential hypothesis is that ongoing evolution of polyandry is facilitated by cross-sex genetic covariances that result from the male–male competition for paternity that polyandry itself intrinsically generates (Keller and Reeve 1995; Evans and Simmons 2008)
We provide an empirical example by estimating additive genetic variances in female liability for extra-pair reproduction and male liability for within-pair paternity success, and the cross-sex genetic covariance between the two, in free-living song sparrows (Melospiza melodia), and consider the degree to which resulting extra-pair reproduction could continue to evolve due to selection on either or both sexes
The 966 broods were reared by 445 unique social pairings; individual females bred with a mean of 1.8 ± 1.1 different socially paired males, 148 (58%) females paired with only one male

Summary

FEMALE AND MALE EFFECTS ON PATERNITY

2007; House et al 2008; Forstmeier et al 2011). Net genetic covariances that do not entirely match those expected given observed or expected assortative reproduction could potentially arise. We first fitted two separate univariate animal models to data describing the paternity status of offspring (WPO or EPO) in each brood to independently estimate additive genetic variance (VA) in female liability for extra-pair reproduction across females that produced each brood, and in male liability for within-pair paternity success across males that were socially paired to these females and reared each brood, and to check for potential biases. We fitted a single univariate animal model that simultaneously estimated VA in both female and male liabilities and the additive genetic covariance between the two, thereby treating the single observed phenotype of offspring paternity status as a joint trait of the female and her socially paired male with direct and associative effects, respectively (e.g., Bijma et al 2007; McGlothlin and Brodie 2009; Wilson et al 2009).

Individuals that contributed phenotypic data

Results

Individualyear variance

Liabilityscale heritability

Discussion

Supporting Information