skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Pervasive Genomic Signatures of Local Adaptation to Altitude Across Highland Specialist Andean Hummingbird Populations
Abstract Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species, Coeligena violifer (n = 62) and Colibri coruscans (n = 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them “taller” biogeographic barriers.  more » « less
Award ID(s):
1442142
PAR ID:
10299801
Author(s) / Creator(s):
; ; ; ;
Editor(s):
Chapman, Mark
Date Published:
Journal Name:
Journal of Heredity
Volume:
112
Issue:
3
ISSN:
0022-1503
Page Range / eLocation ID:
229 to 240
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Understanding how evolutionary forces interact to drive patterns of selection and distribute genetic variation across a species' range is of great interest in ecology and evolution, especially in an era of global change. While theory predicts how and when populations at range margins are likely to undergo local adaptation, empirical evidence testing these models remains sparse. Here, we address this knowledge gap by investigating the relationship between selection, gene flow and genetic drift in the yellowtail clownfish, Amphiprion clarkii, from the core to the northern periphery of the species range. Analyses reveal low genetic diversity at the range edge, gene flow from the core to the edge and genomic signatures of local adaptation at 56 single nucleotide polymorphisms in 25 candidate genes, most of which are significantly correlated with minimum annual sea surface temperature. Several of these candidate genes play a role in functions that are upregulated during cold stress, including protein turnover, metabolism and translation. Our results illustrate how spatially divergent selection spanning the range core to the periphery can occur despite the potential for strong genetic drift at the range edge and moderate gene flow from the core populations. 
    more » « less
  2. Abstract Sage-grouse are two closely related iconic species of the North American West, with historically broad distributions across sagebrush-steppe habitat. Both species are dietary specialists on sagebrush during winter, with presumed adaptations to tolerate the high concentrations of toxic secondary metabolites that function as plant chemical defenses. Marked range contraction and declining population sizes since European settlement have motivated efforts to identify distinct population genetic variation, particularly that which might be associated with local genetic adaptation and dietary specialization of sage-grouse. We assembled a reference genome and performed whole-genome sequencing across sage-grouse from six populations, encompassing both species and including several populations on the periphery of the species ranges. Population genomic analyses reaffirmed genome-wide differentiation between greater and Gunnison sage-grouse, revealed pronounced intraspecific population structure, and highlighted important differentiation of a small isolated population of greater sage-grouse in the northwest of the range. Patterns of genome-wide differentiation were largely consistent with a hypothesized role of genetic drift due to limited gene flow among populations. Inferred ancient population demography suggested persistent declines in effective population sizes that have likely contributed to differentiation within and among species. Several genomic regions with single-nucleotide polymorphisms exhibiting extreme population differentiation were associated with candidate genes linked to metabolism of xenobiotic compounds. In vitro activity of enzymes isolated from sage-grouse livers supported a role for these genes in detoxification of sagebrush, suggesting that the observed interpopulation variation may underlie important local dietary adaptations, warranting close consideration for conservation strategies that link sage-grouse to the chemistry of local sagebrush. 
    more » « less
  3. Hernandez, R (Ed.)
    Abstract Gene expression links genotypes to phenotypes, so identifying genes whose expression is shaped by selection will be important for understanding the traits and processes underlying local adaptation. However, detecting local adaptation for gene expression will require distinguishing between divergence due to selection and divergence due to genetic drift. Here, we adapt a QST−FST framework to detect local adaptation for transcriptome-wide gene expression levels in a population of diverse maize genotypes. We compare the number and types of selected genes across a wide range of maize populations and tissues, as well as selection on cold-response genes, drought-response genes, and coexpression clusters. We identify a number of genes whose expression levels are consistent with local adaptation and show that genes involved in stress response show enrichment for selection. Due to its history of intense selective breeding and domestication, maize evolution has long been of interest to researchers, and our study provides insight into the genes and processes important for in local adaptation of maize. 
    more » « less
  4. Abstract Introduced and invasive species make excellent natural experiments for investigating rapid evolution. Here, we describe the effects of genetic drift and rapid genetic adaptation in pink salmon (Oncorhynchus gorbuscha) that were accidentally introduced to the Great Lakes via a single introduction event 31 generations ago. Using whole‐genome resequencing for 134 fish spanning five sample groups across the native and introduced range, we estimate that the source population's effective population size was 146,886 at the time of introduction, whereas the founding population's effective population size was just 72—a 2040‐fold decrease. As expected with a severe founder event, we show reductions in genome‐wide measures of genetic diversity, specifically a 37.7% reduction in the number of SNPs and an 8.2% reduction in observed heterozygosity. Despite this decline in genetic diversity, we provide evidence for putative selection at 47 loci across multiple chromosomes in the introduced populations, including missense variants in genes associated with circadian rhythm, immunological response and maturation, which match expected or known phenotypic changes in the Great Lakes. For one of these genes, we use a species‐specific agent‐based model to rule out genetic drift and conclude our results support a strong response to selection occurring in a period gene (per2) that plays a predominant role in determining an organism's daily clock, matching large day length differences experienced by introduced salmon during important phenological periods. Together, these results inform how populations might evolve rapidly to new environments, even with a small pool of standing genetic variation. 
    more » « less
  5. The influence of genetic drift on population dynamics during Pleistocene glacial cycles is well understood, but the role of selection in shaping patterns of genomic variation during these events is less explored. We resequenced whole genomes to investigate how demography and natural selection interact to generate the genomic landscapes of Downy and Hairy Woodpecker, species codistributed in previously glaciated North America. First, we explored the spatial and temporal patterns of genomic diversity produced by neutral evolution. Next, we tested (i) whether levels of nucleotide diversity along the genome are correlated with intrinsic genomic properties, such as recombination rate and gene density, and (ii) whether different demographic trajectories impacted the efficacy of selection. Our results revealed cycles of bottleneck and expansion, and genetic structure associated with glacial refugia. Nucleotide diversity varied widely along the genome, but this variation was highly correlated between the species, suggesting the presence of conserved genomic features. In both taxa, nucleotide diversity was positively correlated with recombination rate and negatively correlated with gene density, suggesting that linked selection played a role in reducing diversity. Despite strong fluctuations in effective population size, the maintenance of relatively large populations during glaciations may have facilitated selection. Under these conditions, we found evidence that the individual demographic trajectory of populations modulated linked selection, with purifying selection being more efficient in removing deleterious alleles in large populations. These results highlight that while genome-wide variation reflects the expected signature of demographic change during climatic perturbations, the interaction of multiple processes produces a predictable and highly heterogeneous genomic landscape. 
    more » « less