Elevated performance: the unique physiology of birds that fly at high altitudes
ABSTRACT Birds that fly at high altitudes must support vigorous exercise in oxygen-thin environments. Here I discuss the characteristics that help high fliers sustain the high rates of metabolism needed for flight at elevation. Many traits in the O(2) transport pathway distinguish birds in general from other vertebrates. These include enhanced gas-exchange efficiency in the lungs, maintenance of O(2) delivery and oxygenation in the brain during hypoxia, augmented O(2) diffusion capacity in peripheral tissues and a high aerobic capacity. These traits are not high-altitude adaptations, because they are also characteristic of lowland birds, but are nonetheless important for hypoxia tolerance and exercise capacity. However, unique specializations also appear to have arisen, presumably by high-altitude adaptation, at every step in the O(2) pathway of highland species. The distinctive features of high fliers include an enhanced hypoxic ventilatory response, an effective breathing pattern, larger lungs, haemoglobin with a higher O(2) affinity, further augmentation of O(2) diffusion capacity in the periphery and multiple alterations in the metabolic properties of cardiac and skeletal muscle. These unique specializations improve the uptake, circulation and efficient utilization of O(2) during high-altitude hypoxia. High-altitude birds also have larger wings than their lowland relatives to reduce the metabolic costs of staying aloft in low-density air. High fliers are therefore unique in many ways, but the relative roles of adaptation and plasticity (acclimatization) in high-altitude flight are still unclear. Disentangling these roles will be instrumental if we are to understand the physiological basis of altitudinal range limits and how they might shift in response to climate change.
- SourceAvailable from: Chandrasekhar Natarajan[Show abstract] [Hide abstract]
ABSTRACT: In air-breathing vertebrates, the physiologically optimal blood-O 2 affinity is jointly determined by the prevailing partial pressure of atmospheric O 2 , the efficacy of pulmonary O 2 transfer, and internal metabolic demands. Consequently, genetic variation in the oxygenation properties of hemoglobin (Hb) may be subject to spatially varying selection in species with broad elevational distributions. Here we report the results of a combined functional and evolutionary analysis of Hb polymorphism in the rufous-collared sparrow (Zonotrichia capensis), a species that is continuously distributed across a steep elevational gradient on the Pacific slope of the Peruvian Andes. We integrated a population genomic analysis that included all postnatally expressed Hb genes with functional studies of naturally occurring Hb variants, as well as recombinant Hb (rHb) mutants that were engineered through site-directed mutagenesis. We identified three clinally varying amino acid polymorphisms: Two in the A -globin gene, which encodes the -chain subunits of the major HbA isoform, and one in the D -globin gene, which encodes the -chain subunits of the minor HbD isoform. We then constructed and experimentally tested single-and double-mutant rHbs representing each of the alternative A -globin genotypes that predominate at different elevations. Although the locus-specific patterns of altitudinal differentiation suggested a history of spatially varying selection acting on Hb polymorphism, the experimental tests demonstrated that the observed amino acid mutations have no discernible effect on respiratory properties of the HbA or HbD isoforms. These results highlight the importance of experimentally validating the hypothesized effects of genetic changes in protein function to avoid the pitfalls of adaptive storytelling.Molecular Biology and Evolution 10/2014; 31(11). DOI:10.1093/molbev/msu234
- [Show abstract] [Hide abstract]
ABSTRACT: The aim of this work is to describe for the first time the skin and the subcutaneous diverticula at histological level (by light microscopy) of the Southern Screamer Chauna torquata. We found that the main distinguishing features of the skin were the presence of deep and branched epidermal invaginations whereas in the dermis abundant elastic fibers were found. These skin features could provide a great stretchability to the skin which, in turn, are related to the change of volume that may experience the subcutaneous diverticula.. Since screamers are flying birds that soar to great heights, the presence of subcutaneous diverticula together with another anatomical features (like a great skeletal pneumaticity) could favor a body mass reduction and an optimization in its mode of locomotion.
- [Show abstract] [Hide abstract]
ABSTRACT: Hypoxia is a key factor determining survival, and haemoglobins are targets of selection in species native to high-altitude regions. We studied population genetic structure and evaluated evidence for local adaptation in the crested duck (Lophonetta specularioides). Differentiation, gene flow and time since divergence between highland and lowland populations were assessed for three haemoglobin genes (α(A) , α(D) , β(A) ) and compared to seven reference loci (six autosomal introns and mtDNA). Four derived amino acid replacements were found in the globin genes that had elevated Φ(ST) values between the Andean highlands and Patagonian lowlands. A single β(A) -globin polymorphism at a site known to influence O(2) affinity was fixed for different alleles in the two populations, whereas three α(A) - and α(D) -globin polymorphisms exhibited high heterozygosity in the highlands but not in the lowlands. Coalescent analyses supported restricted gene flow for haemoglobin alleles and mitochondrial DNA but nonzero gene flow for the introns. Simulating genetic data under a drift-migration model of selective neutrality, the β(A) -globin fell outside the 95% confidence limit of simulated data, suggesting that directional selection is maintaining different variants in the contrasting elevational environments, thereby restricting migration of β(A) -globin alleles. The α(A) - and α(D) -globins, by contrast, did not differ from the simulated values, suggesting that variants in these genes are either selectively neutral, or that the effects of selection could not be differentiated from background levels of population structure and linkage disequilibrium. This study illustrates the combined effects of selection and population history on inferring levels of population divergence for a species distributed across an altitudinal gradient in which selection for hypoxia resistance has likely played an important role.Molecular Ecology 12/2011; 21(2):350-68. DOI:10.1111/j.1365-294X.2011.05400.x