Mitochondrial phylogenomics and genome rearrangements in the barklice (Insecta: Psocodea)

Abstract

The mitochondrial genome arrangement in the insect order Psocodea (booklice, barklice, and parasitic lice) is extremely variable. Genome organization ranges from the rearrangement of a few tRNAs and protein coding genes, through extensive tRNA and protein coding gene rearrangements, to subdivision into multiple mini-chromosomes. Evolution of the extremely modified mitochondrial genome in parasitic lice (Phthiraptera) has been the subject of several studies, but limited information is available regarding the mitochondrial genome organization of the more plesiomorphic, free-living Psocodea (formerly known as the “Psocoptera”). In particular, the ancestral state of the psocodean mitochondrial genome arrangement and the evolutionary pathway to the rearranged conditions are still unknown. In this study, we addressed mitochondrial evolutionary questions within the Psocodea by using mitochondrial genome sequences obtained from a wide range of Psocoptera, covering all three suborders. We identified seven types of mitochondrial genome arrangements in Psocoptera, including the first example in Psocodea of retention of the ancestral pancrustacean condition in Prionoglaris (Prionoglarididae). Two methods (condition-based parsimony reconstruction and common-interval genome distances) were applied to estimate the ancestral mitochondrial arrangement in Psocodea, and both provided concordant results. Specifically, the common ancestor of Psocodea retained the ancestral pancrustacean condition, and most of the gene arrangement types have originated independently from this ancestral condition. We also utilized the genomic data for phylogenetic estimation. The tree estimated from the mitochondrial genomic data was well resolved, strongly supported, and in agreement with previously estimated phylogenies. It also provided the first robust support for the family Prionoglarididae, as its monophyly was uncertain in previous morphological and molecular studies.