Mitonuclear Interactions and the Origin of Macaque Societies

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 mitochondrial 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 diverged ancestor. We identified atypically long runs of homozygosity, low polymorphism, high differentiation and/or rapid protein evolution associated with Ninteract genes compared to non-Ninteract genes. These metrics suggest a subset of Ninteract genes were independently subject to atypically pervasive natural selection in multiple species. Selection on mitonuclear interactions is thus a factor in macaque genome evolution that could have influenced aspects of macaque societies including species diversity, ecological breadth, female-biased adult sex ratio and demography, sexual dimorphism, and mitonuclear phylogenomics.

Conservation Mitonuclear Replacement: Facilitated mitochondrial adaptation for a changing world

“…Mitonuclear co‐introgression provides strong evidence that mitonuclear machinery can be substituted in a modular fashion without disrupting other critical genomic interactions. The process has been documented in Drosophila (Beck et al., 2015 ; Box 1 ), swordtail fishes (Moran et al., 2022 ), several birds (Hermansen et al., 2014 ; Morales et al., 2018 ; Nikelski et al., 2021 ; Trier et al., 2014 ; Wang, Ore, et al., 2021 ), and hares (Seixas et al., 2018 ), and is debated in macaques (Bailey & Stevison, 2021 ; Evans et al., 2021 ; Zhu & Evans, 2023 ). The implication is that when a mt haplotype moves between closely related species, sufficient mitonuclear co‐adaptation can be maintained if just a few key nuclear genes co‐introgress (e.g., Moran et al., 2022 ; Seixas et al., 2018 ), rather than the thousands of nuclear genes with potential interactions.…”