In air-breathing vertebrates, the physiologically optimal blood-O2 affinity is jointly determined by the prevailing partial pressure of atmospheric O2, the efficacy of pulmonary O2 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 α(A)-globin gene, which encodes the α-chain subunits of the major HbA isoform, and one in the α(D)-globin gene, which encodes the α-chain subunits of the minor HbD isoform. We then constructed and experimentally tested single- and double-mutant rHbs representing each of the alternative α(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.

Phenotypic flexibility allows individuals to reversibly modify trait values and theory predicts an individual’s relative degree of flexibility positively correlates with the environmental heterogeneity it experiences. We test this prediction by integrating surveys of population genetic and physiological variation with thermal acclimation experiments and indices of environmental heterogeneity in the Dark-eyed Junco (Junco hyemalis) and its congeners. We combine field measures of thermogenic capacity for 335 individuals, 22,006 single nucleotide polymorphisms genotyped in 181 individuals, and laboratory acclimations replicated on five populations. We show that Junco populations: (1) differ in their thermogenic responses to temperature variation in the field; (2) harbor allelic variation that also correlates with temperature heterogeneity; and (3) exhibit intra-specific variation in thermogenic flexibility in the laboratory that correlates with the heterogeneity of their native thermal environment. These results provide comprehensive support that phenotypic flexibility corresponds with environmental heterogeneity and highlight its importance for coping with environmental change.

Phenotypic flexibility allows individuals to reversibly modify trait values and theory predicts an individual’s relative degree of flexibility positively correlates with the environmental heterogeneity it experiences. We tested this prediction by integrating surveys of population genetic and physiological variation with thermal acclimation experiments and indices of environmental heterogeneity in the Dark-eyed Junco (Junco hyemalis) and its congeners. We combined measures of thermogenic capacity for ~300 individuals, >21,000 single nucleotide polymorphisms genotyped in 192 individuals, and laboratory acclimations replicated on five populations. We found that Junco populations: (1) differ in their thermal performance responses to temperature variation in situ; (2) exhibit intra-specific variation in their thermogenic flexibility in the laboratory that correlates with heterogeneity in their native thermal environment; and (3) harbor genetic variation that also correlates with temperature heterogeneity. These results provide comprehensive support that phenotypic flexibility corresponds with environmental heterogeneity and highlight its importance for coping with environmental change.

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Avian haemosporidia are blood parasites that can have dramatic fitness consequences on their hosts, including largescale population declines when introduced to naïve hosts. Yet the physiological effects that accompany haemosporidian infection and underlie these fitness decrements are poorly characterized in most wild birds. Because haemosporidia destroy host red blood cells and consume host hemoglobin, they are predicted to have detrimental impacts on avian blood-oxygen transport and, as a result, reduce aerobic performance. However, the documented effects of infection on avian hematological traits vary across species and no effects have been demonstrated on avian aerobic performance to date. Here we quantified the physiological effects of haemosporidian infections on wild 'Pink-sided' Juncos (Junco hyemalis mearnsi) breeding in northwestern Wyoming, USA. We assayed hematological traits (hemoglobin concentration and hematocrit) and aerobic performance (resting and summit metabolic rates, thermogenic endurance, and aerobic scope), then screened individuals for haemosporidian infection post-hoc (n = 106 adult juncos). We found that infection status did not correlate with any of the physiological indices that we measured, suggesting there is little cost of haemosporidian infection on either junco aerobic performance or energy budgets. Our results highlight the need for more studies of haemosporidia infections in a broader range of species and in a wider array of environmental contexts.