Multipartite mitochondrial genomes and phylogenetic relationships of five newly characterized chewing-louse species of placental mammals (Parvorder Trichodectera)

Fragmented mitochondrial genomes, in which genes are distributed across multiple minichromosomes rather than a single circular molecule, have evolved multiple times in parasitic lice (Psocodea). Despite this complex history, mitochondrial genomes have been characterized for only six of the roughly 400 trichodecteran louse species. Here we used PCR, cloning, and Sanger sequencing methods to increase the number of species characterized in this parvorder by determining the complete mitochondrial genomes of five additional trichodecteran lice: Geomydoecus geomydis, Geomydoecus centralis, Thomomydoecus minor, Neotrichodectes mephitidis, and Stachiella octomaculatus. Each genome was made up of 12-14 circular minichromosomes, consistent with the range reported in related louse lineages. Gene content and chromosome size were largely conserved among close relatives, though tRNA genes showed more mobility than did protein-coding or rRNA genes. The nad3 gene occurred in multiple genomic positions across species. All chromosomes carried one or two conserved sequence blocks in their non-gene regions. These blocks were highly similar within each species but too divergent for alignment between species, a pattern consistent with ongoing recombination among chromosomes within each lineage. We identified additional signatures of interchromosomal recombination, including shared non-coding sequence among specific chromosome subsets in N. mephitidis, nearly identical trnL1/trnL2 sequences in several species, and identical sequences embedded in the cox1 and nad2 genes. A phylogenetic analysis based on 12 mitochondrial genes resolved relationships among trichodecteran species with strong support. Carnivoran-associated lice were paraphyletic, with N. mephitidis being more closely related to pocket gopher lice than to other carnivoran lice, corroborating independent evidence for an ancient host switch between carnivorans and rodents. These findings expand the taxonomic sampling of fragmented mitochondrial genomes and provide further evidence that recombination actively shapes both coding and non-coding regions of these unusual genomes.