Evolution of muscle phenotype for extreme high altitude flight in the bar-headed goose

Abstract

Bar-headed geese migrate over the Himalayas at up to 9000 m elevation, but it is unclear how they sustain the high metabolic rates needed for flight in the severe hypoxia at these altitudes. To better understand the basis for this physiological feat, we compared the flight muscle phenotype of bar-headed geese with that of low altitude birds (barnacle geese, pink-footed geese, greylag geese and mallard ducks). Bar-headed goose muscle had a higher proportion of oxidative fibres. This increased muscle aerobic capacity, because the mitochondrial volume densities of each fibre type were similar between species. However, bar-headed geese had more capillaries per muscle fibre than expected from this increase in aerobic capacity, as well as higher capillary densities and more homogeneous capillary spacing. Their mitochondria were also redistributed towards the subsarcolemma (cell membrane) and adjacent to capillaries. These alterations should improve O 2 diffusion capacity from the blood and reduce intracellular O 2 diffusion distances, respectively. The unique differences in bar-headed geese were much greater than the minor variation between low altitude species and existed without prior exercise or hypoxia exposure, and the correlation of these traits to flight altitude was independent of phylogeny. In contrast, isolated mitochondria had similar respiratory capacities, O 2 kinetics and phosphorylation efficiencies across species. Bar-headed geese have therefore evolved for exercise in hypoxia by enhancing the O 2 supply to flight muscle.

Functional modulation of mitochondrial cytochrome c oxidase underlies adaptation to high-altitude hypoxia in a Tibetan migratory locust

“…Aside from the mechanism that enhances COX activity for oxygen use in Tibetan locusts living in hypoxic conditions, several other physiological mechanisms critical for oxygen supply have also been reported. For example, bar-headed geese have exhibited significant improvement through a series of cascading physiological steps of oxygen transport during hypoxia [15,33]. The genetic basis of the improved haemoglobin-oxygen affinity has been correlated with the substitutions in five exterior amino acid residues in high-altitude deer mice [34].…”

Modelling capillary oxygen supply capacity in mixed muscles: Capillary domains revisited

“…1B) generate a space-filling alternative (Egginton & Ross, 1989 thereby allowing the exploration of the local influences associated with microvascular remodelling, as well as any mismatch between angiogenesis and local O 2 demand (Degens et al, 1992(Degens et al, , 2002(Degens et al, , 2006(Degens et al, , 2008Egginton et al, 2001;Wüst et al, 2009a). This gives Voronoi polygons an advantage in assessing the efficacy of applications to pathological scenarios, such as ischaemia, where potential therapeutic interventions include strength training (Deveci & Egginton, 2002;Suzuki et al, 2000), endurance exercise (Ahmed et al, 1997;Scott et al, 2009), electrical stimulation (Ebina et al, 2002), and alterations in muscle temperature (Egginton et al, 2001;Egginton, 2002). In addition to their ability to reproduce robust versions of the aforementioned global measures, Voronoi polygons have the capacity to provide indices of capillary supply to individual fibres, with both direct contact and indirect influence, and to fibres of different metabolic activities.…”

The biogeography of mitochondrial and nuclear discordance in animals

“…Blier et al (2006) also found little evidence to suggest that functional differences in enzyme activity could explain the introgression of Arctic charr (Salvelinus alpinus) mtDNA into brook charr (S. fontinalis). Combining these types of approach with more sensitive techniques assaying mitochondrial function directly, such as respiration in isolated mitochondrial preparations (Scott et al 2009), will be valuable in determining whether introgressed mitochondria differ phenotypically from the native type and, ideally, how this might affect whole-animal fitness (reviewed by Dalziel et al 2009 andMelvin 2010). In this way, cases of mitochondrial introgression could potentially be used to link the effects of specific mtDNA mutations in introgressed genetic variants to phenotypic differences (Dalziel et al 2009;Scott et al 2011).…”