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Abstract BackgroundComplex organismal traits are often the result of multiple interacting genes and sub-organismal phenotypes, but how these interactions shape the evolutionary trajectories of adaptive traits is poorly understood. We examined how functional interactions between cardiorespiratory traits contribute to adaptive increases in the capacity for aerobic thermogenesis (maximal O2consumption,V̇O2max, during acute cold exposure) in high-altitude deer mice (Peromyscus maniculatus). We crossed highland and lowland deer mice to produce F2inter-population hybrids, which expressed genetically based variation in hemoglobin (Hb) O2affinity on a mixed genetic background. We then combined physiological experiments and mathematical modeling of the O2transport pathway to examine the links between cardiorespiratory traits andV̇O2max. ResultsPhysiological experiments revealed that increases in Hb-O2affinity of red blood cells improved blood oxygenation in hypoxia but were not associated with an enhancement inV̇O2max. Sensitivity analyses performed using mathematical modeling showed that the influence of Hb-O2affinity onV̇O2max in hypoxia was contingent on the capacity for O2diffusion in active tissues. ConclusionsThese results suggest that increases in Hb-O2affinity would only have adaptive value in hypoxic conditions if concurrent with or preceded by increases in tissue O2diffusing capacity. In high-altitude deer mice, the adaptive benefit of increasing Hb-O2affinity is contingent on the capacity to extract O2from the blood, which helps resolve controversies about the general role of hemoglobin function in hypoxia tolerance.
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Gas exchange, oxygen transport and metabolism in high-altitude waterfowl
High-altitude life poses physiological challenges to all animals due to decreased environmental oxygen (O2) availability (hypoxia) and cold. Supporting high metabolic rates and body temperatures with limited O2is challenging. Many birds, however, thrive at high altitudes. The O2-transport cascade describes the pathway involved in moving O2from the environment to the tissues encompassing: (i) ventilation, (ii) pulmonary O2diffusion, (iii) circulation, (iv) tissue O2diffusion, and (v) mitochondrial O2use for ATP production. Shared avian traits such as rigid lungs with cross-current gas exchange and unidirectional airflow aid in O2acquisition and transport in all birds. Many high-altitude birds, however, have evolved enhancements to some or all steps in the cascade. In this review, we summarize the current literature on gas exchange and O2transport in high-altitude birds, providing an overview of the O2-transport cascade that principally draws on the literature from high-altitude waterfowl, the most well-studied group of high-altitude birds. We close by discussing two important avenues for future research: distinguishing between the influences of plasticity and evolution and investigating whether the morphological and physiological differences discussed contribute to enhanced locomotor or thermogenic performance, a potential critical link to fitness. This article is part of the theme issue ‘The biology of the avian respiratory system’.
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- Award ID(s):
- 2419773
- PAR ID:
- 10621583
- Publisher / Repository:
- The Royal Society
- Date Published:
- Journal Name:
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Volume:
- 380
- Issue:
- 1920
- ISSN:
- 0962-8436
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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