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Integrating evolutionary and functional tests of adaptive hypotheses: a case study of altitudinal differentiation in hemoglobin function in an Andean Sparrow, Zonotrichia capensis.

ABSTRACT: 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 ?(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.

SUBMITTER: Cheviron ZA

PROVIDER: S-EPMC4209134 | biostudies-literature | 2014 Nov

REPOSITORIES: biostudies-literature

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Integrating evolutionary and functional tests of adaptive hypotheses: a case study of altitudinal differentiation in hemoglobin function in an Andean Sparrow, Zonotrichia capensis.

Cheviron Zachary A ZA Natarajan Chandrasekhar C Projecto-Garcia Joana J Eddy Douglas K DK Jones Jennifer J Carling Matthew D MD Witt Christopher C CC Moriyama Hideaki H Weber Roy E RE Fago Angela A Storz Jay F JF

Molecular biology and evolution 20140818 11

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 t ...[more]

PMID: 25135942

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Project description:BACKGROUND:Parasite prevalence and diversity are determined by the distribution of hosts and vectors and by the interplay among a suite of environmental factors. Distributions of parasite lineages vary based on host susceptibility and geographical barriers. Hemoparasites of the genera Haemoproteus and Plasmodium have wide distributions, and high prevalence and genetic diversity within perching birds (Order Passeriformes). The rufous-collared sparrow (Zonotrichia capensis) is widely distributed in Central and South America across an immense diversity of environments from sea level to more than 4000 meters above sea level. It therefore provides an excellent model to investigate whether altitudinal and latitudinal gradients influence the distribution, prevalence and diversity of haemosporidian parasites, their population structure and the biogeographical boundaries of distinct parasite lineages. RESULTS:We assembled samples from 1317 rufous-collared sparrows spanning 75 locales from across Central and South America (between 9.5°N and 54°S; 10-4655 meters above sea level). We used DNA sequence data from a fragment of the mitochondrial cytochrome b gene (cytb) of Haemoproteus and Plasmodium from 325 positive samples and found prevalences of 22 and 3%, respectively. Haemoproteus exhibited a higher prevalence than Plasmodium but with comparatively lower genetic diversity. We detected a relationship of Plasmodium and Haemoproteus prevalence with altitude and latitude; however, altitude and latitude did not influence parasite diversity. CONCLUSIONS:Parasite lineages showed a phylogeographical boundary coincident with the Andes Mountains, although we also observed a north-south disjunction in Peru for Haemoproteus. Haemosporidian distribution was not homogeneous but differed based on latitude and altitude. This is most probably due to environmental factors that have influenced both vector distribution and abundance, as well as parasite development. Our study provides key insights on the distribution of haemoparasite lineages and parasite dynamics within hosts.

Project description:BACKGROUND:The Neotropics are exceptionally diverse, containing roughly one third of all extant bird species on Earth. This remarkable species richness is thought to be a consequence of processes associated with both Andean orogenesis throughout the Tertiary, and climatic fluctuations during the Quaternary. Phylogeographic studies allow insights into how such events might have influenced evolutionary trajectories of species and ultimately contribute to a better understanding of speciation. Studies on continentally distributed species are of particular interest because different populations of such taxa may show genetic signatures of events that impacted the continent-wide biota. Here we evaluate the genealogical history of one of the world's most broadly-distributed and polytypic passerines, the rufous-collared sparrow (Zonotrichia capensis). RESULTS:We obtained control region DNA sequences from 92 Zonotrichia capensis individuals sampled across the species' range (Central and South America). Six additional molecular markers, both nuclear and mitochondrial, were sequenced for a subset of individuals with divergent control region haplotypes. Median-joining network analysis, and Bayesian and maximum parsimony phylogenetic analyses all recovered three lineages: one spanning Middle America, the Dominican Republic, and north-western South America; one encompassing the Dominican Republic, Roraima (Venezuela) and La Paz (Bolivia) south to Tierra del Fuego, Argentina; and a third, including eastern Argentina and Brazil. Phylogenetic analyses suggest that the Middle American/north-western South American clade is sister to the remaining two. Bayesian and maximum likelihood coalescent simulations used to study lineage demographic history, diversification times, migration rates and population expansion together suggested that diversification of the three lineages occurred rapidly during the Pleistocene, with negligible gene flow, leaving genetic signatures of population expansions. CONCLUSIONS:The Pleistocene history of the rufous-collared sparrow involved extensive range expansion from a probable Central American origin. Its remarkable morphological and behavioral diversity probably represents recent responses to local conditions overlying deeper patterns of lineage diversity, which are themselves produced by isolation and the history of colonization of South America.

Project description:Seasonal breeding in temperate zone vertebrates is characterised by pronounced variation in both central and peripheral reproductive physiology as well as behaviour. In contrast, many tropical species have a comparatively longer and less of a seasonal pattern of breeding than their temperate zone counterparts. These extended, more "flexible" reproductive periods may be associate with a lesser degree of annual variation in reproductive physiology. Here we investigated variation in the neuroendocrine control of reproduction in relation to the changes in the neural song control system in a tropical breeding songbird the rufous-collared sparrows (Zonotrichia capensis). Using in situ hybridization, we show that the optical density of GnRH1 mRNA expression is relatively constant across pre-breeding and breeding states. However, males were found to have significantly greater expression compared to females regardless of breeding state. Both males and females showed marked variation in measures of peripheral reproductive physiology with greater gonadal volumes and concentrations of sex steroids in the blood (i.e. testosterone in males; estrogen in females) during the breeding season as compared to the pre-breeding season. These findings suggest that the environmental cues regulating breeding in a tropical breeding bird ultimately exert their effects on physiology at the level of the median eminence and regulate the release of GnRH1. In addition, histological analysis of the song control system HVC, RA and Area X revealed that breeding males had significantly larger volumes of these brain nuclei as compared to non-breeding males, breeding females, and non-breeding females. Females did not exhibit a significant difference in the size of song control regions across breeding states. Together, these data show a marked sex difference in the extent to which there is breeding-associated variation in reproductive physiology and brain plasticity that is dependent on the reproductive state in a tropical breeding songbird.

Dataset Information

Integrating evolutionary and functional tests of adaptive hypotheses: a case study of altitudinal differentiation in hemoglobin function in an Andean Sparrow, Zonotrichia capensis.

Publications

Integrating evolutionary and functional tests of adaptive hypotheses: a case study of altitudinal differentiation in hemoglobin function in an Andean Sparrow, Zonotrichia capensis.

Similar Datasets

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