Mitonuclear interactions and introgression genomics of macaque monkeys (Macaca) highlight the influence of behaviour on genome evolution

In most macaques, females are philopatric and males migrate from their
natal ranges, which results in pronounced divergence of mitochondrial
genomes within and among species. We therefore predicted that some nuclear
genes would have to acquire compensatory mutations to preserve
compatibility with diverged interaction partners from the mitochondria. We
additionally expected that these sex-differences would have distinctive
effects on gene flow in the X and autosomes. Using new genomic data from
29 individuals from eight species of Southeast Asian macaque, we
identified evidence of natural selection associated with mitonuclear
interactions, including extreme outliers of interspecies differentiation
and metrics of positive selection, low intraspecies polymorphism, and
atypically long runs of homozygosity associated with nuclear-encoded genes
that interact with mitochondria-encoded genes. In one individual with
introgressed mitochondria, we detected a small but significant enrichment
of autosomal introgression blocks from the source species of her
mitochondria that contained genes that interact with mitochondria-encoded
loci. Our analyses also demonstrate that sex-specific demography sculpts
genetic exchange across multiple species boundaries. These findings show
that behaviour can have profound but indirect effects on genome evolution
by influencing how interacting components of different genomic
compartments (mitochondria, the autosomes, the sex chromosomes) move
through time and space.