Massive gene rearrangement in mitogenomes of phytoseiid mites

Mitochondrial (mt) gene sequences have been widely used to infer phylogeny in animals. The relative order of mt genes in the mitogenome can also be a useful marker for evolution, but the propensity of mt gene rearrangements vary tremendously among taxa. Ticks and mites in Acari exemplify this trend as some families retain the ancestral arthropod gene order, while others show highly divergent gene orders. Mites in Phytoseiidae, many of which are effective biological control agents, show some of the most divergent gene orders. However, the diversity of mitogenome order within this family is little known. We thus sequenced three mt genomes of phytoseiid mites from two of the most speciose genera: Amblyseius swirskii (Athias-Henriot), Amblyseius tsugawai (Ehara) and Neoseiulus womersleyi (Schicha). We find differences in mt GC skew and nucleotide composition, especially between N. womersleyi and the two Amblyseius species. Each species within Phytoseiidae (including three previously available sequences) present a unique gene order. Phytoseiid mitogenomes show some of the highest numbers of breakpoints when compared to the ancestral arthropod order (up to 33), as well as high numbers of breakpoints within the family (14-30). This suggests a history of massive, ongoing mitogenome rearrangements in the family. Phylogenetic analyses of mt sequences confirm that the degree of gene rearrangements follows phylogenetic relatedness. We discuss possible causes for the high degree of mt gene rearrangement within phytoseiid mites as well as selection in the mt and nuclear genome tied to the independent evolution of many diverse feeding strategies in the family. Finally, we suggest N. womersleyi should be used instead of the synonym Amblyseius pseudolongispinosus.