Molecular evolution of the mitochondrial genome underlies semi-aquatic adaptation in lutrinae

Lutrinae, which contains 13 otter species, is a semi-aquatic subfamily. They reclaimed semi-aquatic environments as their habitat. As aquatic environments can lead high energy loss, otters require a highly efficient energy generating style. Mitochondria play key roles in energy production and supply. Thus, we hypothesized that different selective constraints might influence the mitochondrial genomic DNA (mtDNA) of otters compared to that of other terrestrial Mustelidae. To verify the conjecture, we compared the evolutionary rate of the mitochondrial genomes of 12 otter species (including those we previously assembled from five otter species) with those of 18 terrestrial Mustelidae. The results showed that four of the 13 protein-coding genes (PCGs) (COX2, ND1, ND4 and ND6) in the mitochondrial genomes of semi-aquatic otters possessed higher rate of non-synonymous nucleotide substitutions (d_N) to synonymous substitutions (d_S) (ω values, d_N/d_S), than those in terrestrial Mustelidae. For two genes, ND1 and ND4, this difference remained significant after controlling for evolutionary relationships using phylogenetic independent contrasts (PIC) analysis. Furthermore, ND1 and ND4 are rapidly evolving genes (REG). Overall, these results demonstrate that ND1 and ND4 have undergone divergent evolutionary patterns between otters and terrestrial Mustelidae, along with their niche differentiation. The unique evolutionary pattern of mtDNA in Lutrinae may thus play an important role in their semi-aquatic habitat adaptation.