Accelerated Evolutionary Rate of the Myoglobin Gene in Long-Diving Whales

Abstract

Cetaceans, early in their evolutionary history, had developed many physiological adaptations to secondarily return to the sea. Among these adaptations, changes in molecules that transport oxygen and that ultimately support large periods of acute tissue hypoxia probably represent one big step toward the conquest of aquatic environments. Myoglobin contributes to intracellular oxygen storage and transcellular diffusion of oxygen in muscle, and plays an important role in supplying oxygen in hypoxic or ischemic conditions. Here we looked for evidence of adaptive molecular evolution of myoglobin in the cetacean lineage, relative to their terrestrial counterparts. We performed a comparative analysis to examine the variation of the parameter ω (d N/d S) and infer past period of adaptive evolution during the cetacean transition from the terrestrial to the aquatic environment. We also analyzed the changes in amino acid properties. At the nucleotide level, the results showed significant differences in selective pressure between cetacean and non-cetacean myoglobin (ω value three times higher in cetaceans when compared to terrestrial mammals), and also among cetacean lineages according to their diving capacities. Interestingly, both families with long duration diving cetaceans present two parallel substitutions (on sites 4 and 12). Regarding the amino acid properties, our analysis identified four significant physicochemical amino acid changes among residues in myoglobin protein under positive destabilizing selection.

Myoglobin oxygen affinity in aquatic and terrestrial birds and mammals

“…Elevated concentrations of respiratory pigments have obvious adaptive advantages for maintaining aerobic metabolism in diving birds and mammals, and recent studies have examined the potential adaptive molecular evolution of the functional properties of these pigments Soegaard et al, 2012;Helbo and Fago, 2012;Schneuer et al, 2012;Mirceta et al, 2013). Oxygen binding globin proteins are obvious candidates for molecular adaptation in diving animals that experience regular hypoxia (Nery et al, 2013a) and Mb has experienced an increased rate of evolution in cetaceans (Nery et al, 2013b). Dasmeh et al (2013) found that mutations that increase Mb protein-fold stability are positively selected for in cetaceans, and this increase in protein stability is positively correlated with Mb concentration.…”

“…Diving vertebrates with unique physiological adaptations for storing and transporting oxygen may experience selective pressure that influences the molecular evolution of Mb (Naylor and Gerstein, 2000). Recent studies have shown that marine mammal Mb experienced an increase in the rate of evolution (Dasmeh et al, 2013;Nery et al, 2013b) that resulted in increased stability (Dasmeh et al, 2013) and net surface charge (Mirceta et al, 2013) compared with terrestrial mammals.…”

Beluga whale pVHL enhances HIF-2α activity via inducing HIF-2α proteasomal degradation under hypoxia

“…To adapt to this diving need, cetaceans have an acute hypoxia tolerance arising from breath holding during diving [18], as well as innate mechanisms for attenuating damage from reactive oxygen stress (ROS) due to re-oxygenation during the return to the water surface [19–21]. Compared to hypoxic tolerance in terrestrial mammals, such as plateau and cave mammals which adapt to chronic hypoxia, cetaceans have adapted to fluctuating oxygen [22, 23], but how this occurs is unclear [24, 25].…”

Physicochemical Evolution and Molecular Adaptation of the Cetacean Osmoregulation-related Gene UT-A2 and Implications for Functional Studies

“…Site 264, which is located on the T2b helix, has an amino acid shift of Thr to Ala (change to limited side chain flexibility, no H-bonds, higher hydrophobicity and nonpolar77) in cetaceans except for the freshwater YFP and baiji. These changes could increase the P α of T2b (Table 2), leading to a longer, more rigid alpha helix with a more stable lipid raft composition, which, in turn, may alter its interactions with amino acid motifs and its efficiency of combination with other substances8485; thus, it may raise the efficiency of UT-A2 of marine cetaceans compared with the freshwater cetaceans. The region was across from the S m region of the urea selectivity filter regulating the rate of urea conduction, which may increase the hydrophobicity of the S m region, and raise the energy of dehydration, affecting urea conduction (Fig.…”