Mitonuclear interactions and the origin of macaque society

Abstract

In most eukaryotes, aerobic respiration requires interactions between autosomally- encoded genes (Ninteract genes) and mitochondrial DNA, RNA, and protein. In species where females are philopatric, contrasting distributions of genetic variation in mito- chondrial and nuclear genomes creates variation in mitonuclear interactions that may be subject to natural selection. To test this expectation, we turned to a group with extreme female philopatry: the macaque monkeys. We examined four genomic datasets from (i) wild caught and (ii) captive populations of rhesus macaque, which is the most widely distributed non-human primate, and (iii) the stump-tailed macaque and (iv) a subspecies of longtail macaque, both of whose mitochondrial DNA is introgressed from a highly di- verged ancestor. We identified atypically long runs of homozygosity, low polymorphism, high differentiation and/or rapid protein evolution associated with Ninteract genes com- pared to non-Ninteract genes. These metrics suggest a subset of Ninteract genes were independently subject to natural selection in multiple species. Selection on mitonuclear interactions is thus a factor in macaque genome evolution that could have influenced as- pects of macaque societies including species diversity, ecological breadth, female-biased adult sex ratio and demography, sexual dimorphism, and mitonuclear phylogenomics.