Evolution of mitochondrial genome fragmentation in Amblycera (Insecta: Psocodea)

Mitochondrial genome content and organization is diverse across Eukaryotes. Most bilaterian animal mitochondrial genomes (mitogenomes) exhibit highly conserved gene content and organisation, with genes encoded on a single circular chromosome. However, many species of parasitic lice (Insecta: Phthiraptera) have mitogenomes fragmented into multiple circular chromosomes seemingly without having detrimental effects on mitochondrial function. To better understand the process of mitogenome fragmentation, we conducted a large-scale comparative study of a major group of lice, Amblycera. Analyses of the evolution of mitogenome structure across a phylogenomic tree of 90 samples from 53 genera revealed evidence for multiple independent origins of mitogenome fragmentation. We inferred some fragmentation events to have occurred less than five million years ago, and fragmentation rate to have changed multiple times in the course of amblyceran evolution. We compared the rates of DNA substitution and gene rearrangement within mitogenome fragmentation events, specifically contrasting branches with fragmented and non-fragmented mitogenomes. We found that lineages with fragmented mitochondrial genomes had significantly higher rates of mitochondrial sequence evolution, and genes in these mitogenomes were likely to be more rearranged than those on single circular chromosomes. Thus, we confirmed suggestions made by prior studies on other groups of parasitic lice. By combining phylogenomics and mitochondrial genomics we provide a detailed portrait of mitogenome evolution across a group of insects with a remarkably unstable mitogenome structure, identifying processes of molecular evolution that are correlated with mitogenome fragmentation.