skip to main content


The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 5:00 PM ET until 11:00 PM ET on Friday, June 21 due to maintenance. We apologize for the inconvenience.

Title: The role of neutral and adaptive genomic variation in population diversification and speciation in two ground squirrel species of conservation concern

Understanding the neutral (demographic) and adaptive processes leading to the differentiation of species and populations is a critical component of evolutionary and conservation biology. In this context, recently diverged taxa represent a unique opportunity to study the process of genetic differentiation. Northern and southern Idaho ground squirrels (Urocitellus brunneus—NIDGS, andUendemicus—SIDGS, respectively) are a recently diverged pair of sister species that have undergone dramatic declines in the last 50 years and are currently found in metapopulations across restricted spatial areas with distinct environmental pressures. Here we genotyped single‐nucleotide polymorphisms (SNPs) from buccal swabs with restriction site‐associated DNA sequencing (RADseq). With these data we evaluated neutral genetic structure at both the inter‐ and intraspecific level, and identified putatively adaptive SNPs using population structure outlier detection and genotype–environment association (GEA) analyses. At the interspecific level, we detected a clear separation between NIDGS and SIDGS, and evidence for adaptive differentiation putatively linked to torpor patterns. At the intraspecific level, we found evidence of both neutral and adaptive differentiation. For NIDGS, elevation appears to be the main driver of adaptive differentiation, while neutral variation patterns match and expand information on the low connectivity between some populations identified in previous studies using microsatellite markers. For SIDGS, neutral substructure generally reflected natural geographical barriers, while adaptive variation reflected differences in land cover and temperature, as well as elevation. These results clearly highlight the roles of neutral and adaptive processes for understanding the complexity of the processes leading to species and population differentiation, which can have important conservation implications in susceptible and threatened species.

more » « less
Award ID(s):
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
Molecular Ecology
Page Range / eLocation ID:
p. 4673-4694
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Understanding the processes that drive divergence within and among species is a long‐standing goal in evolutionary biology. Traditional approaches to assessing differentiation rely on phenotypes to identify intra‐ and interspecific variation, but many species express subtle morphological gradients in which boundaries among forms are unclear. This intraspecific variation may be driven by differential adaptation to local conditions and may thereby reflect the evolutionary potential within a species. Here, we combine genetic and morphological data to evaluate intraspecific variation within the Nelson's (Ammodramus nelsoni) and salt marsh (Ammodramus caudacutus) sparrow complex, a group with populations that span considerable geographic distributions and a habitat gradient. We evaluated genetic structure among and within five putative subspecies ofA. nelsoniandA. caudacutususing a reduced‐representation sequencing approach to generate a panel of 1929SNPs among 69 individuals. Although we detected morphological differences among some groups, individuals sorted along a continuous phenotypic gradient. In contrast, the genetic data identified three distinct clusters corresponding to populations that inhabit coastal salt marsh, interior freshwater marsh and coastal brackish–water marsh habitats. These patterns support the current species‐level recognition but do not match the subspecies‐level taxonomy within each species—a finding which may have important conservation implications. We identified loci exhibiting patterns of elevated divergence among and within these species, indicating a role for local selective pressures in driving patterns of differentiation across the complex. We conclude that this evidence for adaptive variation among subspecies warrants the consideration of evolutionary potential and genetic novelty when identifying conservation units for this group.

    more » « less
  2. Abstract

    Eco‐phylogeographic approaches to comparative population genetic analyses allow for the inclusion of intrinsic influences as drivers of intraspecific genetic structure. This insight into microevolutionary processes, including changes within a species or lineage, provides better mechanistic understanding of species‐specific interactions and enables predictions of evolutionary responses to environmental change. In this study, we used single nucleotide polymorphisms (SNPs) identified from reduced representation sequencing to compare neutral population structure, isolation by distance (IBD), genetic diversity and effective population size (Ne) across three closely related and co‐distributed saltmarsh sparrow species differing along a specialization gradient—Nelson's (Ammospiza nelsoni subvirgata), saltmarsh (A. caudacuta) and seaside sparrows (A. maritima maritima). Using an eco‐phylogeographic lens within a conservation management context, we tested predictions about species' degree of evolutionary history and ecological specialization to tidal marshes, habitat, current distribution and population status on population genetic metrics. Population structure differed among the species consistent with their current distribution and habitat factors, rather than degree of ecological specialization: seaside sparrows were panmictic, saltmarsh sparrows showed hierarchical structure and Nelson's sparrows were differentiated into multiple, genetically distinct populations. Neutral population genetic theory and demographic/evolutionary history predicted patterns of genetic diversity andNerather than degree of ecological specialization. Patterns of population variation and evolutionary distinctiveness (Shapely metric) suggest different conservation measures for long‐term persistence and evolutionary potential in each species. Our findings contribute to a broader understanding of the complex factors influencing genetic variation, beyond specialist‐generalist status and support the role of an eco‐phylogeographic approach in population and conservation genetics.

    more » « less
  3. Abstract

    Understanding how environmental variation influences population genetic structure is important for conservation management because it can reveal how human stressors influence population connectivity, genetic diversity and persistence. We used riverscape genetics modelling to assess whether climatic and habitat variables were related to neutral and adaptive patterns of genetic differentiation (population‐specific and pairwiseFST) within five metapopulations (79 populations, 4583 individuals) of steelhead trout (Oncorhynchus mykiss) in the Columbia River Basin,USA. Using 151 putatively neutral and 29 candidate adaptiveSNPloci, we found that climate‐related variables (winter precipitation, summer maximum temperature, winter highest 5% flow events and summer mean flow) best explained neutral and adaptive patterns of genetic differentiation within metapopulations, suggesting that climatic variation likely influences both demography (neutral variation) and local adaptation (adaptive variation). However, we did not observe consistent relationships between climate variables andFSTacross all metapopulations, underscoring the need for replication when extrapolating results from one scale to another (e.g. basin‐wide to the metapopulation scale). Sensitivity analysis (leave‐one‐population‐out) revealed consistent relationships between climate variables andFSTwithinthree metapopulations; however, these patterns were not consistent in two metapopulations likely due to small sample sizes (= 10). These results provide correlative evidence that climatic variation has shaped the genetic structure of steelhead populations and highlight the need for replication and sensitivity analyses in land and riverscape genetics.

    more » « less
  4. Abstract

    Understanding the consequences of exotic diseases on native forests is important to evolutionary ecology and conservation biology because exotic pathogens have drastically altered US eastern deciduous forests.Cornus floridaL. (flowering dogwood tree) is one such species facing heavy mortality. Characterizing the genetic structure ofC. floridapopulations and identifying the genetic signature of adaptation to dogwood anthracnose (an exotic pathogen responsible for high mortality) remain vital for conservation efforts. By integrating genetic data from genotype by sequencing (GBS) of 289 trees across the host species range and distribution of disease, we evaluated the spatial patterns of genetic variation and population genetic structure ofC. floridaand compared the pattern to the distribution of dogwood anthracnose. Using genome‐wide association study and gradient forest analysis, we identified genetic loci under selection and associated with ecological and diseased regions. The results revealed signals of weak genetic differentiation of three or more subgroups nested within two clusters—explaining up to 2%–6% of genetic variation. The groups largely corresponded to the regions within and outside the eastern Hot‐Continental ecoregion, which also overlapped with areas within and outside the main distribution of dogwood anthracnose. The fungal sequences contained in the GBS data of sampled trees bolstered visual records of disease at sampled locations and were congruent with the reported range ofDiscula destructiva, suggesting that fungal sequences within‐host genomic data were informative for detecting or predicting disease. The genetic diversity between populations at diseased vs. disease‐free sites across the range ofC. floridashowed no significant difference. We identified 72 single‐nucleotide polymorphisms (SNPs) from 68 loci putatively under selection, some of which exhibited abrupt turnover in allele frequencies along the borders of the Hot‐Continental ecoregion and the range of dogwood anthracnose. One such candidate SNP was independently identified in two prior studies as a possible L‐type lectin‐domain containing receptor kinase. Although diseased and disease‐free areas do not significantly differ in genetic diversity, overall there are slight trends to indicate marginally smaller amounts of genetic diversity in disease‐affected areas. Our results were congruent with previous studies that were based on a limited number of genetic markers in revealing high genetic variation and weak population structure inC. florida.

    more » « less
  5. Abstract

    Adaptive divergence in response to environmental clines are expected to be common in species occupying heterogeneous environments. Despite numerous advances in techniques appropriate for non‐model species, gene–environment association studies in elasmobranchs are still scarce. The bronze whaler or copper shark (Carcharhinus brachyurus) is a large coastal shark with a wide distribution and one of the most exploited elasmobranchs in southern Africa. Here, we assessed the distribution of neutral and adaptive genomic diversity inC. brachyurusacross a highly heterogeneous environment in southern Africa based on genome‐wide SNPs obtained through a restriction site‐associated DNA method (3RAD). A combination of differentiation‐based genome‐scan (outflank) and genotype–environment analyses (redundancy analysis, latent factor mixed models) identified a total of 234 differentiation‐based outlier and candidate SNPs associated with bioclimatic variables. Analysis of 26,299 putatively neutral SNPs revealed moderate and evenly distributed levels of genomic diversity across sites from the east coast of South Africa to Angola. Multivariate and clustering analyses demonstrated a high degree of gene flow with no significant population structuring among or within ocean basins. In contrast, the putatively adaptive SNPs demonstrated the presence of two clusters and deep divergence between Angola and all other individuals from Namibia and South Africa. These results provide evidence for adaptive divergence in response to a heterogeneous seascape in a large, mobile shark despite high levels of gene flow. These results are expected to inform management strategies and policy at the national and regional level for conservation ofC. brachyuruspopulations.

    more » « less