A key question in evolutionary genetics is why certain mutations or certain types of mutation make disproportionate contributions to adaptive phenotypic evolution. In principle, the preferential fixation of particular mutations could stem directly from variation in the underlying rate of mutation to function-altering alleles. However, the influence of mutation bias on the genetic architecture of phenotypic evolution is difficult to evaluate because data on rates of mutation to function-altering alleles are seldom available. Here, we report the discovery that a single point mutation at a highly mutable site in the β A -globin gene has contributed to an evolutionary change in hemoglobin (Hb) function in high-altitude Andean house wrens (Troglodytes aedon). Results of experiments on native Hb variants and engineered, recombinant Hb mutants demonstrate that a nonsynonymous mutation at a CpG dinucleotide in the β A -globin gene is responsible for an evolved difference in Hb-O 2 affinity between high-and low-altitude house wren populations. Moreover, patterns of genomic differentiation between high-and low-altitude populations suggest that altitudinal differentiation in allele frequencies at the causal amino acid polymorphism reflects a history of spatially varying selection. The experimental results highlight the influence of mutation rate on the genetic basis of phenotypic evolution by demonstrating that a large-effect allele at a highly mutable CpG site has promoted physiological differentiation in blood O 2 transport capacity between house wren populations that are native to different elevations.biochemical adaptation | hemoglobin | high altitude | hypoxia | mutation bias
Examining physiological traits across large spatial scales can shed light on the environmental factors driving physiological variation. For endotherms, flexibility in aerobic metabolism is especially important for coping with thermally challenging environments and recent research has shown that aerobic metabolic scope [the difference between maximum thermogenic capacity (Msum) and basal metabolic rate (BMR)] increases with latitude in mammals. One explanation for this pattern is the climatic variability hypothesis, which predicts that flexibility in aerobic metabolism should increase as a function of local temperature variability. An alternative explanation is the cold adaptation hypothesis, which predicts that cold temperature extremes may also be an important driver of variation in metabolic scope. To determine the thermal drivers of aerobic metabolic flexibility in birds, we combined data on metabolic scope from 40 bird species sampled across a range of environments with several indices of local ambient temperature. Using phylogenetically‐informed analyses, we found that minimum winter temperature was the best predictor of variation in avian metabolic scope, outperforming all other thermal variables. Additionally, Msum was a better predictor of latitudinal patterns of metabolic scope than BMR, with species inhabiting colder environments exhibiting increased Msum over their counterparts in warmer environments. Taken together, these results suggest that cold temperature extremes drive latitudinal patterns of metabolic scope via selection for enhanced thermogenic performance in cold environments, supporting the cold adaptation hypothesis. Temperature extremes may therefore be an important selective pressure driving macrophysiological trends of aerobic performance in endotherms.
Aim To assess geographical and temporal patterns of diversification in Metallura hummingbirds, particularly with respect to topographical barriers and climatic variation between different populations.Location Tropical Andes.Methods We estimated a multilocus phylogeny for all nine species of Metallura and evaluated phylogeographical patterns within Metallura tyrianthina using mitochondrial DNA sequences from across its range (n = 192). We tested mechanisms of diversification using climatic classification of sampling sites, coalescent-based dating, lineages-through-time plots and dispersal-vicariance analysis.Results Metallura consists of two main clades: (1) the tree line specialists in the M. aeneocauda superspecies; and (2) a habitat-generalist clade that includes M. tyrianthina and M. iracunda. Metallura phoebe was recovered as sister to the tree line clade in some analyses. In both clades, there was marked genetic structure across topographical barriers and almost no structure between climatically distinct regions in the absence of barriers. The tree line clade exhibited deeper divergences in the Central Andes than elsewhere, and a south-to-north history of diversification, whereas the habitat-generalist clade showed deeper divergences in the Northern Andes and a history of southward expansion. A pure-birth model explained the steady net rate of diversification of Metallura hummingbirds through the Pliocene and the Pleistocene.Main conclusions Isolation across topographical barriers best explained the genetic structure in M. tyrianthina. The two Metallura clades expanded from opposite ends of the Andes, leading to asynchronous divergence across common topographical barriers. Cycles of expansion followed by isolation may explain the preponderance of idiosyncratic area relationships that are typical of Andean clades. Geoclimatic dynamism during the Pleistocene caused Metallura and other Andean bird clades to undergo radical range shifts, including dispersal across topographical barriers, that became key to their diversification.
Theory suggests that different taxa having colonized a similar, challenging environment will show parallel or lineage‐specific adaptations to shared selection pressures, but empirical examples of parallel evolution in independent taxa are exceedingly rare. We employed comparative genomics to identify parallel and lineage‐specific responses to selection within and among four species of North American sparrows that represent four independent, post‐Pleistocene colonization events by an ancestral, upland subspecies and a derived salt marsh specialist. We identified multiple cases of parallel adaptation in these independent comparisons following salt marsh colonization, including selection of 12 candidate genes linked to osmoregulation. In addition to detecting shared genetic targets of selection across multiple comparisons, we found many novel, species‐specific signatures of selection, including evidence of selection of loci associated with both physiological and behavioral mechanisms of osmoregulation. Demographic reconstructions of all four species highlighted their recent divergence and small effective population sizes, as expected given their rapid radiation into saline environments. Our results highlight the interplay of both shared and lineage‐specific selection pressures in the colonization of a biotically and abiotically challenging habitat and confirm theoretical expectations that steep environmental clines can drive repeated and rapid evolutionary diversification in birds.
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