Abstract
Animals that are able to sustain life under hypoxic conditions have long captured the imagination of biologists and medical practitioners alike. Although the associated morphological modifications have been extensively described, the mechanisms underlying the evolution of hypoxia tolerance are not well understood. To provide such insights, we investigated genes in four major energy metabolism pathways, and provide evidence of distinct evolutionary paths to mammalian hypoxia-tolerance. Positive selection of genes in the oxidative phosphorylation pathway mainly occurred in terrestrial hypoxia-tolerant species; possible adaptations to chronically hypoxic environments. The strongest candidate for positive selection along cetacean lineages was the citrate cycle signaling pathway, suggestive of enhanced aerobic metabolism during and after a dive. Six genes with cetacean-specific amino acid changes are rate-limiting enzymes involved in the gluconeogenesis pathway, which would be expected to enhance the lactate removal after diving. Intriguingly, 38 parallel amino acid substitutions in 29 genes were observed between hypoxia-tolerant mammals. Of these, 76.3% were radical amino acid changes, suggesting that convergent molecular evolution drives the adaptation to hypoxic stress and similar phenotypic changes. This study provides further insights into life under low oxygen conditions and the evolutionary trajectories of hypoxia-tolerant species.
Highlights
Ever since Charles Darwin published his book ‘On the Origin of Species by Means of Natural Selection’ nearly 160 years ago (Darwin, 1859), adaptive evolution has remained a critical research question
To estimate the selective pressure acting on genes in energy metabolism pathways in mammals, we ran separate branchsite tests on the ancestral and terminal branches leading to cetaceans, pinnipeds (Weddell seal and Pacific walrus), sirenian (West Indian manatee), highland species (Tibetan yak, and Tibetan antelope), and a subterranean species (Figure 2 and Supplementary Table S2)
For the remaining aquatic mammals, the Likelihood ratio tests (LRTs) test showed evidence for positive selection on the genes PC and OGDH, respectively, in the lineages leading to Weddell seal (Figure 2: branch t) and West Indian manatee (Figure 2: branch x)
Summary
Ever since Charles Darwin published his book ‘On the Origin of Species by Means of Natural Selection’ nearly 160 years ago (Darwin, 1859), adaptive evolution has remained a critical research question. Of particular interest are insights from hypoxia-tolerant animals – species adapted to oxygen (O2) poor aquatic or terrestrial environments (Nathaniel et al, 2015). Oxygen is vital to animals and hypoxia is associated with cell death and organ failure, as observed in stroke and ischemia reperfusion injury in humans (Buck and Pamenter, 2006). Hypometabolism, in marine mammals is associated with an increased reliance on anaerobic (‘without oxygen’; nitrate) metabolism; the advantage of which is that energy in the form of adenosine triphosphate (ATP) can be produced in the Evolution of Energy Metabolism Genes in Hypoxia-Tolerant Mammal absence of oxygen (Costa, 2007). Higher concentrations or activity of key glycolytic enzymes that enhance the ability to process lactic acid, such as lactate dehydrogenase (LDH), may be associated with greater tolerance to hypoxia (Costa, 2007)
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