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. 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.