Pervasive relaxed selection on spermatogenesis genes in gorillas coincident with the evolution of polygyny

Gorillas have a polygynous social system in which the highest-ranking male
has almost exclusive access to females and sires most of the offspring in
the troop. Such behavior results in a  dramatic reduction of
sperm competition, which is ultimately associated with  numerous
traits leading to a low efficacy of gorilla spermatogenesis. However, the
molecular basis behind the remarkable erosion of the gorilla male
reproductive system remains unknown. Here, we explored the genetic
consequences of the polygynous social system in gorillas by testing for
altered selection intensity across 13,310 orthologous protein-coding genes
from 261 Eutherian mammals. We identified 578 genes with relaxed purifying
selection in the gorilla lineage, compared with only 96 that were
positively selected. Genes under relaxed purifying selection in gorillas
have accumulated numerous deleterious amino acid substitutions; their
expression is biased towards male germ cells, and are enriched in
functions related to meiosis and sperm biology. We tested the function of
gorilla relaxed genes previously not implicated in sperm biology using the
Drosophila model system and identified 41 novel spermatogenesis genes
required for normal fertility. Furthermore, by exploring exome/genome
sequencing data of infertile men with severe spermatogenic impairment, we
found that the human orthologs of the gorilla relaxed genes are enriched
for loss-of-function variants in infertile men. These data provide
compelling evidence that reduced sperm competition in gorillas is
associated with  relaxed purifying selection on genes related to
male reproductive function. The accumulation of deleterious mutations in
these genes likely provides the mechanistic basis behind the low efficacy
of gorilla spermatogenesis and uncovers new candidate genes for human male
infertility.