Convergent changes in muscle metabolism depend on duration of high-altitude ancestry across Andean waterfowl.

Neal J Dawson,Gabriele Nandal,Kevin G Mccracken,Luis Alza,Graham R Scott

doi:10.7554/elife.56259

Neal J Dawson, Gabriele Nandal + Show 3 more

Open Access

https://doi.org/10.7554/elife.56259

Copy DOI

Abstract

High-altitude environments require that animals meet the metabolic O2 demands for locomotion and thermogenesis in O2-thin air, but the degree to which convergent metabolic changes have arisen across independent high-altitude lineages or the speed at which such changes arise is unclear. We examined seven high-altitude waterfowl that have inhabited the Andes (3812-4806 m elevation) over varying evolutionary time scales, to elucidate changes in biochemical pathways of energy metabolism in flight muscle relative to low-altitude sister taxa. Convergent changes across high-altitude taxa included increased hydroxyacyl-coA dehydrogenase and succinate dehydrogenase activities, decreased lactate dehydrogenase, pyruvate kinase, creatine kinase, and cytochrome c oxidase activities, and increased myoglobin content. ATP synthase activity increased in only the longest established high-altitude taxa, whereas hexokinase activity increased in only newly established taxa. Therefore, changes in pathways of lipid oxidation, glycolysis, and mitochondrial oxidative phosphorylation are common strategies to cope with high-altitude hypoxia, but some changes require longer evolutionary time to arise.

Highlights

Given a common set of environmental challenges, evolution often converges upon a phenotype that maximizes fitness in that environment
By integrating population genetic data to infer how long each species has been established at high altitude, we show that some high-altitude phenotypes arose quickly whereas others required much longer evolutionary time to arise
Convergent changes have occurred in many pathways of metabolism across high-altitude waterfowl, with increases in capacity for beta oxidation of lipids and adjustments in the activity of oxidative phosphorylation (OXPHOS) enzymes that likely fine-tune mitochondrial function (Figure 1)

Summary

Introduction

Given a common set of environmental challenges, evolution often converges upon a phenotype that maximizes fitness in that environment (i.e., fitness optimum). Flying birds face the additional challenge of maintaining lift with reductions in air density, which more than offsets the metabolic savings from reductions in drag, such that birds flying at high altitude must flap their wings harder and maintain higher metabolic rates to stay aloft (Bishop et al, 2015) Both evolved and phenotypically plastic changes in respiratory physiology and metabolism are believed to help mitigate the challenges posed by the cold and hypoxic environment at high altitude (Beall, 2000; Lague et al, 2017; Monge and Leon-Velarde, 1991). Except for studies of a few key proteins like hemoglobin (Natarajan et al, 2018; Natarajan et al, 2015; ProjectoGarcia et al, 2013; Storz et al, 2010), we still know little about whether convergent phenotypic changes have arisen across independent high-altitude lineages, for the pathways of energy metabolism that support locomotion and thermogenesis. By integrating population genetic data to infer how long each species has been established at high altitude, we show that some high-altitude phenotypes arose quickly whereas others required much longer evolutionary time to arise

Results and discussion

Conclusions

Materials and methods