skip to main content


Title: Genomic variation in the American pika: signatures of geographic isolation and implications for conservation
Abstract Background

Distributional responses by alpine taxa to repeated, glacial-interglacial cycles throughout the last two million years have significantly influenced the spatial genetic structure of populations. These effects have been exacerbated for the American pika (Ochotona princeps), a small alpine lagomorph constrained by thermal sensitivity and a limited dispersal capacity. As a species of conservation concern, long-term lack of gene flow has important consequences for landscape genetic structure and levels of diversity within populations. Here, we use reduced representation sequencing (ddRADseq) to provide a genome-wide perspective on patterns of genetic variation across pika populations representing distinct subspecies. To investigate how landscape and environmental features shape genetic variation, we collected genetic samples from distinct geographic regions as well as across finer spatial scales in two geographically proximate mountain ranges of eastern Nevada.

Results

Our genome-wide analyses corroborate range-wide, mitochondrial subspecific designations and reveal pronounced fine-scale population structure between the Ruby Mountains and East Humboldt Range of eastern Nevada. Populations in Nevada were characterized by low genetic diversity (π = 0.0006–0.0009; θW = 0.0005–0.0007) relative to populations in California (π = 0.0014–0.0019; θW = 0.0011–0.0017) and the Rocky Mountains (π = 0.0025–0.0027; θW = 0.0021–0.0024), indicating substantial genetic drift in these isolated populations. Tajima’sDwas positive for all sites (D = 0.240–0.811), consistent with recent contraction in population sizes range-wide.

Conclusions

Substantial influences of geography, elevation and climate variables on genetic differentiation were also detected and may interact with the regional effects of anthropogenic climate change to force the loss of unique genetic lineages through continued population extirpations in the Great Basin and Sierra Nevada.

 
more » « less
Award ID(s):
1637686
NSF-PAR ID:
10385075
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Springer Science + Business Media
Date Published:
Journal Name:
BMC Ecology and Evolution
Volume:
21
Issue:
1
ISSN:
2730-7182
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    It is often expected that temperate plants have expanded their geographical ranges northward from primarily southern refugia. Evidence for this hypothesis is mixed in eastern North American species, and there is increasing support for colonization from middle latitudes. We studied genome‐wide patterns of variation in RADseq loci to test hypotheses concerning range expansion in a North American forest herb (Campanula americana). First, spatial patterns of genetic differentiation were determined. Then phylogenetic relationships and divergence times were estimated. Spatial signatures of genetic drift were also studied to identify the directionality of recent range expansion and its geographical origins. Finally, spatially explicit scenarios for the spread of plants across the landscape were compared, using variation in the population mutation parameter and Tajima'sD. We found strong longitudinal subdivision, with populations clustering into groups west and east of the Mississippi River. While the southeastern region was probably part of a diverse Pleistocene refugium, there is little evidence that range expansion involved founders from these southern locales. Instead, declines in genetic diversity and the loss of rare alleles support a westward colonization wave from a middle latitude refugium near the southern Appalachian Mountains, with subsequent expansion from a Pleistocene staging ground in the Mississippi River Valley (0.51–1.27 million years ago). These analyses implicate stepping stone colonization from middle latitudes as an important mechanism of species range expansion in eastern North America. This study further demonstrates the utility of population genetics as a tool to infer the routes travelled by organisms during geographical range expansion.

     
    more » « less
  2. Abstract Aim

    A central aim of biogeography is to understand how biodiversity is generated and maintained across landscapes. Here, we establish phylogenetic and population genetic patterns in a widespread reptile to quantify the influence of historical biogeography and current environmental variation on patterns of genetic diversity.

    Location

    Western North America.

    Taxon

    Western terrestrial garter snake,Thamnophis elegans.

    Methods

    We used double‐digest RADseq to estimate phylogenetic relationships and characterize population genetic structure across the three widespread subspecies ofTelegans:T. e. vagrans(wandering garter snake),Teelegans(mountain garter snake) andTeterrestris(coast garter snake). We assessed patterns of dispersal and vicariance across biogeographic regions using ancestral area reconstruction (AAR) and deviations from isolation‐by‐distance across the landscape using estimated effective migration surfaces (EEMS). We identified environmental variables potentially shaping local adaptation in regional lineages using genetic‐environment association (GEA) analyses.

    Results

    We recovered three well‐differentiated genetic groups that correspond to the three subspecies. AAR analyses inferred the eastern Cascade Range as the ancestral area, with dispersal to both the east and west across western North America. Populations ofT. e. elegansdisplayed a latitudinal gradient in genetic variation across the Sierra Nevada and northern California, while populations ofTeterrestrisshow discrete genetic breaks consistent with well‐known biogeographic barriers. Lastly, GEA analyses identified allele frequency shifts at loci associated with a common set of environmental variables in bothTeelegansandTeterrestris.

    Main Conclusion

    T. elegansis composed of distinct evolutionary lineages, each with its own geographic range and history of diversification.TeelegansandTeterrestrisshow unique patterns of diversification as populations dispersed from east to west and while adapting to the new environments they colonized. Historical events, landscape features and environmental variation have all contributed to patterns of differentiation inTelegans.

     
    more » « less
  3. Abstract

    The Hengduan Mountains region is a biodiversity hotspot known for its topologically complex, deep valleys and high mountains. While landscape and glacial refugia have been evoked to explain patterns of interspecies divergence, the accumulation of intra‐species (i.e., population level) genetic divergence across the mountain‐valley landscape in this region has received less attention. We used genome‐wide restriction site‐associated DNA sequencing (RADseq) to reveal signatures of Pleistocene glaciation in populations ofThitarodes shambalaensis(Lepidoptera: Hepialidae), the host moth of parasiticOphiocordyceps sinensis(Hypocreales: Ophiocordycipitaceae) or caterpillar fungus” endemic to the glacier of eastern Mt. Gongga. We used moraine history along the glacier valleys to model the distribution and environmental barriers to gene flow across populations ofT.shambalaensis. We found that moth populations separated by less than 10 km exhibited valley‐based population genetic clustering and isolation‐by‐distance (IBD), while gene flow among populations was best explained by models using information about their distributions at the local last glacial maximum (LGML, 58 kya), not their contemporary distribution. Maximum likelihood lineage history among populations, and among subpopulations as little as 500 m apart, recapitulated glaciation history across the landscape. We also found signals of isolated population expansion following the retreat of LGMLglaciers. These results reveal the fine‐scale, long‐term historical influence of landscape and glaciation on the genetic structuring of populations of an endangered and economically important insect species. Similar mechanisms, given enough time and continued isolation, could explain the contribution of glacier refugia to the generation of species diversity among the Hengduan Mountains.

     
    more » « less
  4. Abstract

    Despite its economic importance as a bioenergy crop and key role in riparian ecosystems, little is known about genetic diversity and adaptation of the eastern cottonwood (Populus deltoides). Here, we report the first population genomics study for this species, conducted on a sample of 425 unrelated individuals collected in 13 states of the southeastern United States. The trees were genotyped by targeted resequencing of 18,153 genes and 23,835 intergenic regions, followed by the identification of single nucleotide polymorphisms (SNPs). This naturalP. deltoidespopulation showed low levels of subpopulation differentiation (FST = 0.022–0.106), high genetic diversity (θW = 0.00100, π = 0.00170), a large effective population size (Ne ≈ 32,900), and low to moderate levels of linkage disequilibrium. Additionally, genomewide scans for selection (Tajima'sD), subpopulation differentiation (XTX), and environmental association analyses with eleven climate variables carried out with two different methods (LFMMandBAYENV2) identified genes putatively involved in local adaptation. Interestingly, many of these genes were also identified as adaptation candidates in another poplar species,Populus trichocarpa, indicating possible convergent evolution. This study constitutes the first assessment of genetic diversity and local adaptation inP. deltoidesthroughout the southern part of its range, information we expect to be of use to guide management and breeding strategies for this species in future, especially in the face of climate change.

     
    more » « less
  5. Abstract Aim

    To investigate how putative barriers, forest refugia, and ecological gradients across the lower Guineo‐Congolian rain forest shape genetic and phenotypic divergence in the leaf‐folding frogAfrixalus paradorsalis, and examine the role of adjacent land bridge and sky‐islands in diversification.

    Location

    The Lower Guineo‐Congolian Forest, the Cameroonian Volcanic Line (CVL), and Bioko Island, Central Africa.

    Taxon

    Afrixalus paradorsalis(Family: Hyperoliidae), an African leaf‐folding frog.

    Methods

    We used molecular and phenotypic data to investigate diversity and divergence among theA. paradorsalisspecies complex distributed across lowland rain forests, a land bridge island, and mountains in Central Africa. We examined the coincidence of population boundaries, landscape features, divergence times, and spatial patterns of connectivity and diversity, and subsequently performed demographic modelling using genome‐wide SNP variation to distinguish among divergence mechanisms in mainland (riverine barriers, forest refugia, ecological gradients) and land bridge island populations (vicariance, overwater dispersal).

    Results

    We detected four genetically distinct allopatric populations corresponding to Bioko Island, the CVL, and two lowland rain forest populations split by the Sanaga River. Although lowland populations are phenotypically indistinguishable, pronounced body size evolution occurs at high elevation, and the timing of the formation of the high elevation population coincides with mountain uplift in the CVL. Spatial analyses and demographic modelling revealed population divergence across mainland Lower Guinea is best explained by forest refugia rather than riverine barriers or ecological gradients, and that the Bioko Island population divergence is best explained by vicariance (marine incursion) rather than overseas dispersal.

    Main conclusions

    We provide growing support for the important role of forest refugia in driving intraspecific divergences in the Guineo‐Congolian rain forest. InA. paradorsalis, sky‐islands in the CVL have resulted in greater genetic and phenotypic divergences than marine incursions of the land bridge Bioko Island, highlighting important differences in patterns of island‐driven diversification in Lower Guinea.

     
    more » « less