Positive and relaxed selection on mitochondrial DNA in parasitic versus predatory mites

Abstract Mitochondrial genomes (mtDNA) have distinct evolutionary trajectories owing to their inheritance, ploidy and underlying mutation rates, making them prone to accumulate slightly deleterious mutations. Positive selection on mtDNA has been suggested to be important during adaptation to ‘high-energy’ lifestyles and environments. Disentangling positive versus relaxed selection in molecular mtDNA evolution studies is therefore important, although common metrics such as elevated dN/dS ratios (the ratio of non-synonymous to synonymous substitution rates) can be interpreted as signs of both relaxed purifying selection and positive selection. Here, we examined mtDNA evolution in mites (superorder Parasitiformes) to characterize selection during transitions from a parasitic to a free-living, predatory lifestyle. We predicted energetic demands on predatory mites would be associated with positive selection on mtDNA and that reduced effective population sizes in parasitic lineages would lead to relaxed selection. Using newly sequenced mite mitogenomes, we found a signature of accelerated mtDNA evolution in predatory lineages. Unexpectedly, this is likely due to relaxed, not positive selection on the mtDNA of predatory mites, which is supported by massive, ongoing gene rearrangements in the mtDNA of some predatory lineages (family Phytoseiidae). We discuss why ‘high-energy’ lifestyles are not always associated with adaptive mtDNA evolution. This article is part of the theme issue ‘Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya’.