Haplodiploidy accelerates mitogenome evolution in insects

Rates of mitogenome evolution differ among animal lineages, and this
variation has been linked to life history, ecological traits, and—
potentially—to sex-determination system. Insects are a strong model for
examining the latter factor because haplodiploidy (HD) has evolved on
multiple occasions from a diplodiploid (DD) ancestral state. We tested for
rate differences between DD and HD taxa by examining sequence change in a
sentinel segment of the mitogenome, the 658 bp barcode region of the
cytochrome c oxidase I (COI) gene. Specifically, we investigated if amino
acid substitutions and indels are more frequent in HD than DD lineages by
inspecting COI sequences from over 86,000 BINs (a species proxy)
representing 783 insect families and 26 orders. Among them, ten lineages,
varying in rank from tribe to order, are HD. Our analysis, which accounts
for phylogeny, indicates that HD lineages have higher rates (1.7×) of
amino acid substitution, higher Ka/Ks (3.5×), and far more indels than DD
taxa. While our results demonstrate that HD accelerates mitogenome
evolution, future work needs to clarify its mechanistic basis. We
hypothesize that HD facilitates positive selection for mitochondrial
mutations which encode proteins that interact with nuclear gene products.
Such coevolutionary interactions should be facilitated because recessive
mutations in the nuclear genome are fully exposed to selection in males of
HD but not DD lineages.