A multivariate analysis of genetic constraints to life history evolution in a wild population of red deer.

Craig A Walling,Katharina Foerster,Josephine M Pemberton,Michael B Morrissey,Tim H Clutton-Brock,Loeske E B Kruuk

doi:10.1534/genetics.114.164319

Abstract

Evolutionary theory predicts that genetic constraints should be widespread, but empirical support for their existence is surprisingly rare. Commonly applied univariate and bivariate approaches to detecting genetic constraints can underestimate their prevalence, with important aspects potentially tractable only within a multivariate framework. However, multivariate genetic analyses of data from natural populations are challenging because of modest sample sizes, incomplete pedigrees, and missing data. Here we present results from a study of a comprehensive set of life history traits (juvenile survival, age at first breeding, annual fecundity, and longevity) for both males and females in a wild, pedigreed, population of red deer (Cervus elaphus). We use factor analytic modeling of the genetic variance–covariance matrix (G) to reduce the dimensionality of the problem and take a multivariate approach to estimating genetic constraints. We consider a range of metrics designed to assess the effect of G on the deflection of a predicted response to selection away from the direction of fastest adaptation and on the evolvability of the traits. We found limited support for genetic constraint through genetic covariances between traits, both within sex and between sexes. We discuss these results with respect to other recent findings and to the problems of estimating these parameters for natural populations.

Highlights

By far the most common approach to studying genetic trade-offs and genetic constraints is to estimate the bivariate genetic correlation between two traits (Blows and Hoffmann 2005; Walsh and Blows 2009)
Given the inherently multivariate nature of selection and phenotypic variation, the focus on bivariate correlations may give a misleading impression of the extent of genetic constraints and in particular may lead to an underestimate of their importance (Dickerson 1955; Pease and Bull 1988)
The degree to which multiple traits respond to selection is determined both by the distribution of genetic variances across those traits and by the genetic covariances among them, which jointly determine the amount of genetic variation that exists in the direction of selection (Lande 1979; Blows 2007)

Summary

Introduction

By far the most common approach to studying genetic trade-offs and genetic constraints is to estimate the bivariate genetic correlation between two traits (Blows and Hoffmann 2005; Walsh and Blows 2009). Our aim in this study was to use multivariate techniques to assess the potential for genetic constraints to the evolution of four life history traits in a wild population of red deer (C. elaphus) on the Isle of Rum, Scotland Previous studies in this population have shown genetic variation for numerous traits (Kruuk et al 2000; Wilson et al 2007; Nussey et al 2008; Clements et al 2011) and in line with theoretical predictions, that the heritability of traits decreases with increasing association with fitness [i.e., increasing strength of selection (Kruuk et al 2000)]. In particular, we assess estimates of deflection (u) and evolvability [e(b)] when genetic covariances are fixed to zero vs. not zero, to assess the importance of genetic variance vs. covariances in generating any constraint

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Conclusion