Predicting evolutionary responses to selection on polyandry in the wild: additive genetic covariances with female extra-pair reproduction

Jane M Reid

doi:10.1098/rspb.2012.1835

Abstract

The evolutionary forces that underlie polyandry, including extra-pair reproduction (EPR) by socially monogamous females, remain unclear. Selection on EPR and resulting evolution have rarely been explicitly estimated or predicted in wild populations, and evolutionary predictions are vulnerable to bias due to environmental covariances and correlated selection through unmeasured traits. However, evolutionary responses to (correlated) selection on any trait can be directly predicted as additive genetic covariances (covA) with appropriate components of relative fitness. I used comprehensive life-history, paternity and pedigree data from song sparrows (Melospiza melodia) to estimate covA between a female's liability to produce extra-pair offspring and two specific fitness components: relative annual reproductive success (ARS) and survival to recruitment. All three traits showed non-zero additive genetic variance. Estimates of covA were positive, predicting evolution towards increased EPR, but 95% credible intervals overlapped zero. There was therefore no conclusive prediction of evolutionary change in EPR due to (correlated) selection through female ARS or recruitment. Negative environmental covariance between EPR and ARS would have impeded evolutionary prediction from phenotypic selection differentials. These analyses demonstrate an explicit quantitative genetic approach to predicting evolutionary responses to components of (correlated) selection on EPR that should be unbiased by environmental covariances and unmeasured traits.

Highlights

Extra-pair reproduction (EPR) by socially monogamous females, and the resulting polyandry, could substantially alter distributions of reproductive success and the evolutionary dynamics of sexually selected traits compared with those arising given strict monogamy [1,2,3]
Definition a female’s liability to produce an extra-pair offspring (EPO) rather than a within-pair offspring (WPO) a female’s relative annual reproductive success (ARS) defined as the number of ringed offspring a female produced per year divided by the population mean an individual’s relative survival to recruitment (SR) defined as 1 or 0 for individuals that did or did not survive to age 1 year divided by the population mean; SRw was analysed as a binomial trait (SRwB) and as a Gaussian trait (SRwG) additive genetic variance and covariance, respectively year variance and covariance, respectively permanent individual variance and covariance, respectively residual variance and covariance, respectively of evolutionary change
Direct costs and benefits of EPR have instead been postulated in terms of decreased paternal care by a female’s cuckolded social mate, time, energy or disease costs of mating, or increased fertility or foraging opportunities [1,5,8,47]

Summary

INTRODUCTION

Extra-pair reproduction (EPR) by socially monogamous females, and the resulting polyandry, could substantially alter distributions of reproductive success and the evolutionary dynamics of sexually selected traits compared with those arising given strict monogamy [1,2,3]. Parameters can be estimated for single or multiple traits given sufficient data describing variation in phenotype and fitness components among relatives These include phenotypic selection differentials and gradients with respect to specific fitness components, heritabilities and additive genetic (co)variances [9,10,17,18]. Predicted evolutionary responses can be substantially biased [13 – 16,19 – 23] These problems can in theory be resolved by measuring all relevant environmental covariates and traits, and estimating multivariate (partial) selection gradients with respect to fitness components of interest [9,11,13,14]. Correlated selection through individuals that die before trait expression, or on reproductive traits through adults that fail to breed, could substantially bias predictions

EPRL ARSw

Findings

DISCUSSION