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)

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.

Keywords: Associative genetic effects; assortative reproduction; fertilization success; multiple mating; polyandry; reproductive strategy.

Figure 1

Conceptual view of the relative numbers of (A) within-pair offspring (WPO) and (B–D) extra-pair offspring (EPO) conceived by females and males with low or high additive genetic liabilities for extra-pair reproduction (EPR) and within-pair paternity success (WPPS), respectively, assuming (B) negative, (C) positive, or (D) zero genetic covariance between male within-pair paternity success and extra-pair reproductive success. Circle sizes indicate relative numbers of offspring. Dark and light shading indicates assortative reproduction that would, respectively, generate negative and positive genetic covariance between female liability for extra-pair reproduction and male liability for within-pair paternity success in offspring. These figures are intended to illustrate conceptual points not to be quantitatively accurate: absolute offspring numbers might differ across panels A versus B–D depending on the mean extra-pair reproduction rate, female and male genetic values will vary continuously rather than dichotomously, and offspring proportions will also depend on any assortative pairing or correlated variation in female fecundity.