Abstract
Sexually selected traits show large variation and rapid evolution across the animal kingdom, yet genetic variation often persists within populations despite apparent directional selection. A key step in solving this long-standing paradox is to determine the genetic architecture of sexually selected traits to understand evolutionary drivers and constraints at the genomic level. Antlers are a form of sexual weaponry in male red deer (Cervus elaphus). On the island of Rum, Scotland, males with larger antlers have increased breeding success, yet there has been no evidence of any response to selection at the genetic level. To try and understand the mechanisms underlying this observation, we investigate the genetic architecture of ten antler traits and their principal components using genomic data from >38,000 SNPs. We estimate the heritabilities and genetic correlations of the antler traits using a genomic relatedness approach. We then use genome-wide association and haplotype-based regional heritability to identify regions of the genome underlying antler morphology, and an empirical Bayes approach to estimate the underlying distributions of allele effect sizes. We show that antler morphology is highly repeatable over an individual's lifetime, heritable and has a polygenic architecture and that almost all antler traits are positively genetically correlated with some loci identified as having pleiotropic effects. Our findings suggest that a large mutational target and genetic covariances among antler traits, in part maintained by pleiotropy, are likely to contribute to the maintenance of genetic variation in antler morphology in this population.
Highlights
Selected traits show great variety and complexity across the animal kingdom, ranging from morphology and behaviours that increase attractiveness to the opposite sex, to traits which increase intersexual competitiveness for access to mates (Andersson, 1994)
Our findings suggest that genetic variation in antler morphology is maintained via a large mutational target and pleiotropy with traits sharing similar complex polygenic architectures in the red deer population
We have shown that antler morphology is heritable and repeatable over an individual's lifetime and that it is likely to be highly polygenic with a moderate degree of shared genetic architecture across different antler traits
Summary
Selected traits show great variety and complexity across the animal kingdom, ranging from morphology and behaviours that increase attractiveness to the opposite sex, to traits which increase intersexual competitiveness for access to mates (Andersson, 1994). Studies of sexual traits should aim to identify specific genetic variants with large effects on phenotype and should aim to determine the distribution of polygenic effect sizes and the degree to which these underlying loci are shared between traits This will shed light on potential evolutionary processes and mechanisms in empirical studies, but will inform the mechanistic details of theoretical models to allow better assumptions to account for the complexities of natural populations (McNamara & Houston, 2009; Wilkinson et al, 2015). In male red deer (Cervus elaphus) on the island of Rum, Scotland, there is directional selection for increased antler weight and number of antler points (known as “form”) Both traits are substantially heritable (h2 = 0.38 and 0.24, respectively) and positively genetically correlated, but no phenotypic response to selection has been observed over a 30-year study period (Kruuk et al, 2002, 2014). Our findings suggest that genetic variation in antler morphology is maintained via a large mutational target and pleiotropy with traits sharing similar complex polygenic architectures in the red deer population
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