skip to main content


Title: Genomic signatures of spatially divergent selection at clownfish range margins
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
Award ID(s):
1743711
NSF-PAR ID:
10373857
Author(s) / Creator(s):
; ; ; ; ; ; ;
Date Published:
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Volume:
288
Issue:
1952
ISSN:
0962-8452
Page Range / eLocation ID:
20210407
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Chapman, Mark (Ed.)
    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
  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. Abstract

    Understanding spatial patterns of genetic differentiation and local adaptation is critical in a period of rapid environmental change. Climate change and anthropogenic development have led to population declines and shifting geographic distributions in numerous species. The streamside salamander,Ambystoma barbouri, is an endemic amphibian with a small geographic range that predominantly inhabits small, ephemeral streams. AsAbarbouriis listed as near‐threatened by the IUCN, we describe range‐wide patterns of genetic differentiation and adaptation to assess the species’ potential to respond to environmental change. We use outlier scans and genetic‐environment association analyses to identify genomic variation putatively underlying local adaptation across the species’ geographic range. We find evidence for adaptation with a polygenic architecture and a set of candidate SNPs that identify genes putatively contributing to local adaptation. Our results build on earlier work that suggests that someA. barbouripopulations are locally adapted despite evidence for asymmetric gene flow between the range core and periphery. Taken together, the body of work describing the evolutionary genetics of range limits inA. barbourisuggests that the species may be unlikely to respond naturally to environmental challenges through a range shift orin situadaptation. We suggest that management efforts such as assisted migration may be necessary in future.

     
    more » « less
  4. Abstract

    Disentangling the effects of neutral and adaptive processes in maintaining phenotypic variation across environmental gradients is challenging in natural populations. Song sparrows (Melospiza melodia) on the California Channel Islands occupy a pronounced east‐west climate gradient within a small spatial scale, providing a unique opportunity to examine the interaction of genetic isolation (reduced gene flow) and the environment (selection) in driving variation. We used reduced representation genomic libraries to infer the role of neutral processes (drift and restricted gene flow) and divergent selection in driving variation in thermoregulatory traits with an emphasis on the mechanisms that maintain bill divergence among islands. Analyses of 22,029 neutral SNPs confirm distinct population structure by island with restricted gene flow and relatively large effective population sizes, suggesting bill differences are probably not a product of genetic drift. Instead, we found strong support for local adaptation using 3294 SNPs in differentiation‐based and environmental association analyses coupled with genome‐wide association tests. Specifically, we identified several putatively adaptive and candidate loci in or near genes involved in bill development pathways (e.g.,BMP,CaM,Wnt), confirming the highly complex and polygenic architecture underlying bill morphology. Furthermore, we found divergence in genes associated with other thermoregulatory traits (i.e., feather structure, plumage colour, and physiology). Collectively, these results suggest strong divergent selection across an island archipelago results in genomic changes in a suite of traits associated with climate adaptation over small spatial scales. Future research should move beyond studying univariate traits to better understand multidimensional responses to complex environmental conditions.

     
    more » « less
  5. Abstract

    The study of local adaptation in the presence of ongoing gene flow is the study of natural selection in action, revealing the functional genetic diversity most relevant to contemporary pressures. In addition to individual genes, genome-wide architecture can itself evolve to enable adaptation. Distributed across a steep thermal gradient along the east coast of North America, Atlantic silversides (Menidia menidia) exhibit an extraordinary degree of local adaptation in a suite of traits, and the capacity for rapid adaptation from standing genetic variation, but we know little about the patterns of genomic variation across the species range that enable this remarkable adaptability. Here, we use low-coverage, whole-transcriptome sequencing of Atlantic silversides sampled along an environmental cline to show marked signatures of divergent selection across a gradient of neutral differentiation. Atlantic silversides sampled across 1371 km of the southern section of its distribution have very low genome-wide differentiation (median FST = 0.006 across 1.9 million variants), consistent with historical connectivity and observations of recent migrants. Yet almost 14,000 single nucleotide polymorphisms (SNPs) are nearly fixed (FST > 0.95) for alternate alleles. Highly differentiated SNPs cluster into four tight linkage disequilibrium (LD) blocks that span hundreds of genes and several megabases. Variants in these LD blocks are disproportionately nonsynonymous and concentrated in genes enriched for multiple functions related to known adaptations in silversides, including variation in lipid storage, metabolic rate, and spawning behavior. Elevated levels of absolute divergence and demographic modeling suggest selection maintaining divergence across these blocks under gene flow. These findings represent an extreme case of heterogeneity in levels of differentiation across the genome, and highlight how gene flow shapes genomic architecture in continuous populations. Locally adapted alleles may be common features of populations distributed along environmental gradients, and will likely be key to conserving variation to enable future responses to environmental change.

     
    more » « less