Evolutionary characteristics and origin of fragmented mitochondrial genomes in Psocodea

<p indent="0mm">The mitochondrial genome (mtDNA) of insects exhibits high conservation in gene content, gene order, and topological structure. However, Psocodean insects display notable variability in their mitochondrial genomes, including gene duplication and lost, extensive gene rearrangement, and mtDNA fragmentation. In order to gain a deeper understanding of the evolutionary attributes and fragmentation mechanism within Psocodea, comparative analyses of the complete mitochondrial genomes of 81 Psocodean species were conducted in this paper. The results are listed as follows: (i) Twenty-seven species have fragmented mitochondrial genomes, with parasitic lice exhibiting significantly higher fragmentation levels compared to booklice. (ii) The AT content of fragmented mtDNA is significantly lower than that of unfragmented mtDNA. (iii) Mitochondrial genes in booklice underwent extensive rearrangements, resulting in the absence of shared gene boundaries. However, the level of gene rearrangement was not directly related to mtDNA fragmentation. (iv) Mitochondrial genomes of booklice often contain different types of mitochondrial pseudogenes. (v) The fragmentation of mtDNA structure may be associated with the purification selection of relaxed mitochondrial protein-coding genes. (vi) Phylogenetic analysis supported that booklice and parasitic lice are sister groups, suggesting that Psocoptera and Phthiraptera should be merged into the Psocodea superorder. (vii) The mechanism of mtDNA fragmentation in Psocodea primarily involves the loss of key genes responsible for mtDNA stability, mtDNA recombination, mitochondrial gene duplication and random deletion events. (viii) mtDNA fragmentation occurred independently at least 18 times in Psocodea. Additionally, this paper summarizes the application of mitochondrial genes in the study of Psocodean insects and proposes future research direction for Psocodean mitochondrial genomes. In summary, this review provides a new perspective for understanding the evolutionary characteristics and formation mechanism of fragmented mitochondrial genomes in animals.