Mitogenome fragmentation evolves multiple times within a major group of parasitic lice

Abstract

Animal mitochondrial genomes (mitogenomes) typically exhibit a highly conserved gene content and organisation, with genes encoded on a single circular chromosome. However, many species of parasitic lice (Insecta: Phthiraptera) are notable exceptions, having mitogenomes fragmented into multiple circular chromosomes. To understand the process of mitogenome fragmentation, we conducted a large-scale genomic study of a major group of lice, Amblycera, with extensive taxon sampling. 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, some inferred to have occurred less than five million years ago. We leveraged these many independent origins of fragmentation to compare the rates of DNA substitution and gene rearrangement, 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. In addition, lineages with fragmented mitochondrial genomes were more likely to have mitogenome gene rearrangements than those with single-chromosome mitochondrial genomes. By combining phylogenomics and mitochondrial genomics we provide a detailed portrait of mitogenome evolution across this group of insects with a remarkably unstable mitogenome structure, identifying processes of molecular evolution that are correlated with mitogenome fragmentation. Author SummaryMitochondria are organelles that play a key role in providing energy to cells essential for life. The structure of the mitochondrial genome is conserved across most animal groups, being a single circular chromosome containing 37 genes. Deviations from this structure are typically detrimental and associated with some human diseases. However, in very few animal groups, the mitochondrial genome is fragmented into multiple circular chromsomes. In one group of insects, parasitic lice, fragmentation varies among species, with some having a complete circular genome and others having their mitochondrial genome fragmented in two or more smaller chromosomes. Here, we use whole genome sequencing reads to analyze an unprecedented number of species from a diverse group of lice (Amblycera) that exhibits both single-chromosome and fragmented mitochondrial genomes to understand how this fragmentation evolved. We found that fragmentation evolved many times independently in this group and this fragmentation is correlated faster rates mitochondrial molecular evolution and with an increased frequency of gene rearrangement. We also provide evidence that the rate of mitochondrial genome fragmentation changes over time. Altogether, our combination of broad sampling and phylogenomic and comparative analyses provide new insights into the mechanisms and dynamics of mitochondrial genome fragmentation.