Genomic analysis reveals a polygenic architecture of antler morphology in wild red deer (Cervus elaphus).

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 heritable and repeatable over an individual's lifetime and is likely to have a polygenic architecture. We also show that almost all antler traits are positively genetically correlated which is likely to be driven by both pleiotropic effects of underlying genes and/or linkage disequilibrium between them. Our findings suggest that a large mutational target and extensive genetic correlations are likely to contribute to the maintenance of genetic variation in antler morphology in this population.