Abstract
Understanding the genetic underpinning of adaptive divergence among populations is a key goal of evolutionary biology and conservation. Gunnison sage‐grouse (Centrocercus minimus) is a sagebrush obligate species with a constricted range consisting of seven discrete populations, each with distinctly different habitat and climatic conditions. Though geographically close, populations have low levels of natural gene flow resulting in relatively high levels of differentiation. Here, we use 15,033 SNP loci in genomic outlier analyses, genotype–environment association analyses, and gene ontology enrichment tests to examine patterns of putatively adaptive genetic differentiation in an avian species of conservation concern. We found 411 loci within 5 kbp of 289 putative genes associated with biological functions or pathways that were overrepresented in the assemblage of outlier SNPs. The identified gene set was enriched for cytochrome P450 gene family members (CYP4V2, CYP2R1, CYP2C23B, CYP4B1) and could impact metabolism of plant secondary metabolites, a critical challenge for sagebrush obligates. Additionally, the gene set was also enriched with members potentially involved in antiviral response (DEAD box helicase gene family and SETX). Our results provide a first look at local adaption for isolated populations of a single species and suggest adaptive divergence in multiple metabolic and biochemical pathways may be occurring. This information can be useful in managing this species of conservation concern, for example, to identify unique populations to conserve, avoid translocation or release of individuals that may swamp locally adapted genetic diversity, or guide habitat restoration efforts.
Highlights
The investigation of adaption in populations and the underlying mo‐ lecular mechanisms are key topics in ecology, evolutionary biology, and conservation
Future work could confirm FST of outliers in a larger sample of individuals and/or with whole‐genome resequencing within the Gunnison sage‐grouse populations, sequence haplotype blocks in the vicinity of outliers, measure expression of putatively adaptive genes as a function of SNP genotype, and/or evaluate the role of cytochrome P450 genes in chicken models of response to plant secondary compounds
The potential adaptive divergence associated with local adapta‐ tion to different sagebrush species and response to viral pathogens observed in Gunnison sage‐grouse suggest that individuals from one population may be less fit in the environment of a differently adapted population
Summary
The investigation of adaption in populations and the underlying mo‐ lecular mechanisms are key topics in ecology, evolutionary biology, and conservation. The Gunnison sage‐grouse (Centrocercus minimus) is a sagebrush (Artemisia spp.) obligate avian species persisting as seven isolated populations with low gene flow and high genetic differentiation (Oyler‐McCance, St John, Taylor, Apa, & Quinn, 2005). Each population is centered in a rela‐ tively isolated area of the species range and has variable topography and environmental conditions covering a range of average annual precipitation, average annual temperature, and dominant vegeta‐ tion (Gunnison sage‐grouse Rangewide Steering Committee, 2005; Table 1 and Figure S1.1). An evaluation of genetic variation at cytochrome P450 genes and additional candidate genes related to metabolism of plant secondary metabolites (PSMs) in greater sage‐grouse identified evidence for positive selection, potentially pointing to local dietary adaptation (Oh et al, 2019). Is there evidence of adaptive divergence among populations of Gunnison sage‐grouse? Second, can we link signals of adaptive divergence to putative gene function? Identification of genes or groups of related genes potentially under adaptive divergence can help elucidate critical factors in the ecology of this threatened spe‐ cies, to be validated and elaborated with further targeted study
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