Initial Evidence for Adaptive Selection on the NADH Subunit Two of Freshwater Dolphins by Analyses of Mitochondrial Genomes

Abstract

A small number of cetaceans have adapted to an entirely freshwater environment, having colonized rivers in Asia and South America from an ancestral origin in the marine environment. This includes the ‘river dolphins’, early divergence from the odontocete lineage, and two species of true dolphins (Family Delphinidae). Successful adaptation to the freshwater environment may have required increased demands in energy involved in processes such as the mitochondrial osmotic balance. For this reason, riverine odontocetes provide a compelling natural experiment in adaptation of mammals from marine to freshwater habitats. Here we present initial evidence of positive selection in the NADH dehydrogenase subunit 2 of riverine odontocetes by analyses of full mitochondrial genomes, using tests of selection and protein structure modeling. The codon model with highest statistical support corresponds to three discrete categories for amino acid sites, those under positive, neutral, and purifying selection. With this model we found positive selection at site 297 of the NADH dehydrogenase subunit 2 (dN/dS>1.0,) leading to a substitution of an Ala or Val from the ancestral state of Thr. A phylogenetic reconstruction of 27 cetacean mitogenomes showed that an Ala substitution has evolved at least four times in cetaceans, once or more in the three ‘river dolphins’ (Families Pontoporidae, Lipotidae and Inidae), once in the riverine Sotalia fluviatilis (but not in its marine sister taxa), once in the riverine Orcaella brevirostris from the Mekong River (but not in its marine sister taxa) and once in two other related marine dolphins. We located the position of this amino acid substitution in an alpha-helix channel in the trans-membrane domain in both the E. coli structure and Sotalia fluviatilis model. In E. coli this position is located in a helix implicated in a proton translocation channel of respiratory complex 1 and may have a similar role in the NADH dehydrogenases of cetaceans.

Mitochondrial DNA diversity and population structure in the Irrawaddy dolphin (Orcaella brevirostris) from the Gulf of Thailand and the Mekong River

“…; Caballero et al . ). However, significant levels of genetic differentiation was found among sampling locations, particularly at the Φ ST level, evidencing strong genetic differentiation between coastal and riverine populations and among sampling locations.…”

Signals of positive selection in mitochondrial protein‐coding genes of woolly mammoth: Adaptation to extreme environments?

“…Here, all Clade 1 and Clade 3 shared isoleucine while Clade 2/A displayed methionine. Taking into consideration that ND5 186 and ND5 191 are binding sites for other residues in chains encoded by ND4 and ND2 subunits, respectively, coupled with their location near a possible Na + translocation channel, mutations at these residues might have likely influenced protein functions including catalytic mechanisms in complex I. Mutations affecting H + / Na + transport activity has been found in dolphins, although their key role in adaptive selection could not be determined (Caballero, Duchêne, Garavito, Slikas, & Baker, 2015). Meanwhile, the mutation in ND5 191 was located in cytoplasmic region, where threonine was replaced with isoleucine.…”

Demography or selection on linked cultural traits or genes? Investigating the driver of low mtDNA diversity in the sperm whale using complementary mitochondrial and nuclear genome analyses

“…Following Caballero, Duchene, Garavito, Slikas, and Baker (2015), 3D homology models of proteins for genes where positive selection was detected in sperm whales (ND1, ND2, ATP8, COX3, ND4L, COX3, ND4, ND5, CYTB) were generated by the SWISS-MODEL server (Schwede, Kopp, Guex, & Peitsch, 2003), using the templates specified in Figure S4 (best-fitting model based out of the top four templates for each gene region), and visualized using UCSF CHIMERA v1.11 (Pettersen et al, 2004). This 3D model was annotated with domains based on alignment to the best-fitting template.…”