Haplodiploidy accelerates mitogenome evolution in insects

TL;DR

This study shows that haplodiploid insects have faster mitogenome evolution compared to diplodiploid insects, possibly due to differences in how mutations are selected.

Contribution

The study demonstrates that haplodiploidy accelerates mitogenome evolution in insects through higher amino acid substitution and indel rates.

Findings

Haplodiploid lineages show 1.7× higher amino acid substitution rates than diplodiploid lineages.

Haplodiploid lineages have 3.5× higher Ka/Ks ratios and more indels compared to diplodiploid lineages.

The study suggests that haplodiploidy may facilitate positive selection for mitochondrial mutations.

Abstract

Rates of mitogenome evolution differ among animal lineages, and this variation has been linked to life history, to ecological traits and—potentially—to the sex-determination system. Insects are a compelling model for examining the latter factor because haplodiploid (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 subunit 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, 10 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 is needed 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 the HD but not the DD lineages.

Figures