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

Susana Caballero,Beth Slikas,Sebastian Duchêne,C Scott Baker,Manuel F Garavito,Kentaro Q Sakamoto

doi:10.1371/journal.pone.0123543

Susana Caballero, Beth Slikas + Show 4 more

Open Access

https://doi.org/10.1371/journal.pone.0123543

Copy DOI

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.

Highlights

Genomic evolution between species of marine and freshwater habitats has only recently started to gain attention
A genomic assembly of about 20 populations of marine and freshwater three-spine stickleback fish [3] suggested that changes in the expression of regulatory loci are likely more predominant that those in coding sites when saltwater vs. freshwater adaptation was evaluated and that a small fraction of the genomic regions analysed showed non-synonymous substitutions between marine and freshwater fish (17% of all genomic regions analysed). Most of these studies suggest that regulatory gene expression is a very likely mechanism involved in adaptation to freshwater environments, there is initial evidence showing some degree of amino acid structural differences found in particular proteins that may play an important role in freshwater adaptation
The codon models selected according to the Akaike Information Criterion (AIC) indicated that a proportion of sites were under positive selection in the 8 genes: COI, COIII, ND1, ND2, ND3, ND4, ND5, and Cytb (Table 2)

Summary

Introduction

Genomic evolution between species of marine and freshwater habitats has only recently started to gain attention. A genomic assembly of about 20 populations of marine and freshwater three-spine stickleback fish [3] suggested that changes in the expression of regulatory loci (for example those involved in cellular signalling) are likely more predominant that those in coding sites when saltwater vs freshwater adaptation was evaluated and that a small fraction of the genomic regions analysed showed non-synonymous substitutions between marine and freshwater fish (17% of all genomic regions analysed) Most of these studies suggest that regulatory gene expression is a very likely mechanism involved in adaptation to freshwater environments, there is initial evidence showing some degree of amino acid structural differences found in particular proteins that may play an important role in freshwater adaptation. Whitehead [4] found evidence of fixed amino acid changes in proteins coded in the mitochondrial genome in freshwater populations of killifish when compared with marine populations

Methods

Results

Conclusion