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While mitochondrial genome content and organization is quite diverse across all Eukaryotes, most bilaterian animal mitochondrial genomes (mitogenomes) exhibit highly conserved gene content and organisation, with genes typically encoded on a single circular chromosome. However, many species of parasitic lice (Insecta: Phthiraptera) are among the notable exceptions, having mitogenomes fragmented into multiple circular chromosomes. To better 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. 

Abstract Recently, genomic approaches have helped to resolve phylogenetic questions in many groups of parasitic organisms, including lice (Phthiraptera). However, these approaches have still not been applied to one of the most diverse groups of lice, Amblycera. To fill this gap, we applied phylogenomic methods based on genome‐level exon sequence data to resolve the relationships within and among the families of Amblycera. Our phylogenomic trees support the monophyly of the families Ricinidae and Laemobothriidae. However, the families Trimenoponidae and Gyropidae are not monophyletic, indicating that they should be merged into a single family. The placement ofTrinotonis unstable with respect to Boopiidae and Menoponidae, and we suggest recognizing Trinotonidae as a separate family. At the genus level, the generaColpocephalum,Hohorstiella,MenacanthusandRicinuswere recovered as paraphyletic. Regarding generic complexes, the tree revealed theMenacanthuscomplex to be monophyletic, but theColpocephalumcomplex paraphyletic, including genera not traditionally placed in this group. Dating analysis suggests that the divergence among families of Amblycera occurred shortly after the Cretaceous–Paleogene boundary 66 Mya. Cophylogenetic analyses revealed many host‐switching events during the diversification of Amblycera, indicating that the evolutionary history of Amblycera does not tightly mirror that of its hosts. Ancestral host reconstructions revealed that the ancestral host of Amblycera was most likely a bird, with two host switching events to mammals. By combining phylogenomics, molecular dating and cophylogenetic analyses, we provide the first large‐scale picture of amblyceran evolution, which will serve as a basis for future studies of this group.