Evolved changes in the intracellular distribution and physiology of muscle mitochondria in high-altitude native deer mice

Abstract

High-altitude natives that have evolved to live in hypoxic environments provide a compelling system to understand how animals can overcome impairments in oxygen availability. We examined whether these include changes in mitochondrial physiology or intracellular distribution that contribute to hypoxia resistance in high-altitude deer mice (Peromyscus maniculatus). Mice from populations native to high- and low-altitudes were born and raised in captivity, and as adults were acclimated to normoxia or hypobaric hypoxia (equivalent to 4,300 m elevation). We found that highlanders had higher respiratory capacities in the gastrocnemius (but not soleus) muscle than lowlanders (assessed using permeabilized fibres with single or multiple inputs to the electron transport system), due in large part to higher mitochondrial volume densities in the gastrocnemius. The latter was attributed to an increased abundance of subsarcolemmal (but not intermyofibrillar) mitochondria, such that more mitochondria were situated near the cell membrane and adjacent to capillaries. Hypoxia acclimation had no significant effect on these population differences, but it did increase mitochondrial cristae surface densities of mitochondria in both populations. Hypoxia acclimation also altered the physiology of isolated mitochondria by affecting respiratory capacities and cytochrome c oxidase activities in population-specific manners. Chronic hypoxia decreased the release of reactive oxygen species by isolated mitochondria in both populations. There were subtle differences in O₂ kinetics between populations, with highlanders exhibiting increased mitochondrial O₂ affinity or catalytic efficiency in some conditions. Our results suggest that evolved changes in mitochondrial physiology in high-altitude natives are distinct from the effects of hypoxia acclimation, and likely provide a better indication of adaptive traits that improve performance and hypoxia resistance at high altitudes.

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