Evolution of hypoxia tolerance: Diving pinniped model and human hypobaric hypoxia model.

Abstract

To physiologists, the term 'adaptation' usually refers to any trait which is considered advantageous; evolutionary biologists restrict the definition to traits arising and maintained under selection. By their definition, many physiological traits may merely reflect inheritance passed on through lineage. In considering the evolution of tolerance to reduced oxygen availability, we studied the pininpeds where the two dominant groups, phocids and otariids, varying in diving capacities, and human lineages exposed for varying generational time periods to hypobaric hypoxia. Basic principles of evolution of complex physiological systems first emerged from analysis of the diving response. We then analyzed human responses to hypobaric hypoxia in three different lineages: lowlanders, Andean natives (Quechuas), and Himalayan natives (Sherpas). As in the pinniped example, we found 'conservative' and 'adaptable' physiological characters involved in human responses to hypoxia. Conservative characters are clearly dominant and are too numerous to outline in detail; three examples are hemoglobin oxygen affinities, muscle organization into different fiber types, and the brain's almost exclusive preference for glucose as a fuel. Most notably, we also found evidence for 'adaptable' characters at all levels of organization examined. At the whole body level in Quechuas and Sherpas, we found (i) that maximum aerobic and anaerobic exercise. capacities were down-regulated, (ii) that the acute effect of hypoxia (making up the energy deficit due to oxygen lack; i.e., the Pasteur effect) expected from lowlanders was blunted, and (iii) that acclimation effects were also attenuated. The biochemical behaviour of skeletal muscles was consistent with lowered reliance on anaerobic glycolytic contributions to energy supply, thus improved yield of ATP per mole of carbon fuel utilized. Heart adaptations also seemed to rely upon stoichiometric effficiency adjustments, improving the yield of ATP per mole of oxygen consumed (by using glucose in preference to fatty acids). Most of the biochemical and physiological adaptations we noted (both as acute and acclimation responses) were similar in Sherpas and Quechuas. These two lineages have not shared a common ancestor for about 1/3 of our species history, so we tentatively assume that their similar physiological traits arose independently as hypoxia defense adaptations in two different times and places in our history. As in the evolution of exquisitve capacities for management of oxygen down to vanishing low levels in diving animals, the evolution of human hypoxia tolerance can be described in terms of how two (consesative vs adaptable) categories of physiological characters are assembled in different human lineages and how the assembly changes through generational time. More recent evidence indicating that our species evolved under 'colder, drier, and higher' conditions, suggests that these adaptations may represent the 'ancestral' physiological condition for humans.