Molas have mighty mitochondria: intensified purifying selection on mtDNA despite presumed "low-energy" lifestyles in ocean sunfishes (family Molidae).

Abstract

Ocean sunfish (family Molidae) are often perceived as "low-energy" drifters composed largely of connective tissue with noticeably missing fins and even cited as "mistakes" of natural selection. Because locomotory capacity has been identified as a driver of evolution in animal mitochondrial genomes (mtDNA), ocean sunfish are expected to show signatures of relaxed selection on mtDNA compared to closely related, more energetic species. Contrary to expectations, ocean sunfish showed lower dN/dS ratios (the ratio of non-synonymous to synonymous substitution rates) in all mitochondrial-encoded genes and further analyses strongly suggest this is due to increased purifying selection on mtDNA within Molidae. Population genetic data also support more intense selection on ocean sunfish mtDNA. These results agree with recent studies recharacterizing ocean sunfish as active swimmers with a complex lifestyle including extreme vertical migrations, behavioral thermoregulation, and extreme fecundity. Finally, across 64 diverse fishes, mtDNA evolutionary rates did not correlate with swimming speed. More broadly, this study highlights how predicting selection on mitochondrial genes is not straightforward. Assuming different selective pressures on mtDNA given locomotion or different perceived "lifestyles" may be an oversimplification, analogous to regarding an unusual species as an evolutionary "mistake".