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Rieseberg, L. H.

Publications and source records attributed to Rieseberg, L. H..

At least 19 recordsLinked to original sources

Shared genomic signatures of Arctic adaptation among distantly related plant lineages

Extreme environments impose strong selection pressures that can drive convergent adaptation among distantly related species. Arctic plants survive low temperatures, 24-hour light in summer and darkness in winter, short growing seasons, limited precipitation, nutrient-poor soils, and extreme seasonal variation. To test if these conditions are associated with shared genomic signatures, we generated a chromosome-level genome assembly for Oxyria digyna and compared it with existing reference genomes for three distantly related Arctic species (Cochlearia groenlandica, Draba nivalis, Dryas octopetala) and for 16 non-Arctic species from the same families. We identified 214 orthogroups with signatures of positive selection in all Arctic species, 1.6 times the number shared among the non-Arctic species. Although no gene ontology (GO) categories remained significantly enriched after multiple-testing correction, descriptive annotations included genes involved in general functions including protein folding, glycolysis, transcription, and oxidative-stress responses. Orthogroups showing copy number variation were associated with biotic interactions, sexual reproduction, and nutrient acquisition, suggesting that species may respond to biotic and nutrient stresses by shifts in gene copy number. Arctic and alpine genomes contained lower proportions of some repetitive elements, including terminal inverted repeats, and smaller regions of centromeric repeats than non-Arctic genomes. Overall, we see shared genes under positive selection, similar functions of genes with high copy number variation, and lower counts of some repetitive elements in the Arctic plant genomes. Our findings reveal a shared genomic signature of Arctic adaptation across deeply diverged plant lineages, suggesting that evolution in extreme environments repeatedly targets similar genomic features.

genomics↗

Historical genomes reveal scale-dependent predictability of climate adaptation

Predicting evolution remains a central challenge in biology. Contemporary spatial patterns are increasingly used as space-for-time proxies to forecast evolutionary responses to environmental change, yet the reliability of such predictions--and whether it varies among biological scales--remains unclear. Using historical and contemporary genomes of the invasive weed Ambrosia artemisiifolia--spanning the species' native range, invasions on two continents and nearly two centuries--we show that genomically predicted flowering-time clines remained stable in the native range while introduced populations re-evolved them. Haploblocks--likely structural variants--were likewise temporally stable in the native range, and two showed striking parallel evolution across all three ranges. Climate-associated SNPs with the strongest contemporary clines showed the greatest temporal change, with limited and variable parallelism among introduced ranges. Together, these results suggest adaptive evolution is partly predictable even when individual genomic trajectories remain flexible and contingent, with predictability emerging most clearly at the level of polygenic traits and large structural variants.

evolutionary biology↗

Genomic and eco-geographic features of locally adapted inversions in wild sunflowers

Chromosomal inversions are increasingly recognized as important drivers of local adaptation and ecological divergence because they suppress recombination and maintain adaptive allele combinations despite ongoing gene flow. However, the eco-evolutionary conditions favouring the establishment of such indirectly adaptive inversions, as well as the genomic features that distinguish them from other inversions remain incompletely understood. In this study, we investigated these questions in a wild sunflower system comprising two species: Helianthus debilis and Helianthus praecox, which exhibit diverse ecotypes and varying degrees of geographic overlap across Texas and Florida in the USA. To resolve the evolutionary relationships between and within these species, and identify potentially adaptive inversions, we generated haplotype-resolved reference assemblies and integrated comparative and population genomic analyses. We identified three major genetic clusters that only partially corresponded to taxonomic classifications. We further detected 156 inversions across the genome, 11 of which showed signatures consistent with a role in local adaptation. Notably, nine of the 11 putatively adaptive inversions were found in sympatric Texas populations. Together with a similar enrichment of inversions in genome assemblies from sympatric versus allopatric populations, our results suggest that inversions are more likely to evolve in heterogeneous environments with ongoing gene flow than in allopatry. Lastly, locally adaptive inversions were generally larger, contained more genes, and showed greater sequence divergence between haplotypes than other types of inversions. Our findings provide empirical support for the role of gene flow in promoting inversion establishment and identify genomic characteristics associated with indirectly adaptive inversions.

evolutionary biology↗

The stability of fatty acid composition in sunflower oil is dependent on environment and affected by structural variation

In sunflower (Helianthus annuus L.), the composition of fatty acids in the seeds, primarily oleic, linoleic, stearic and palmitic acid, is of utmost importance for oil quality. Despite this, the genetic basis of this trait and its interaction with the environment is poorly understood. Understanding this interaction is critical to improvement of sunflower within the context of climate change. In this work, we incorporated fatty acid composition measurements from the sunflower SAM population and eight environments across an extensive geographic cline into GWAS. The SAM panel consists of 287 varieties representing approximately 90% of sunflower diversity, for which 2.2 million high-quality SNPs with a MAF > 5% are available. For increased power, multivariate GWAS was performed with four different inputs: (i) mean fatty acid composition within each environment, (ii) mean fatty acid composition within each environment omitting high oleic varieties, (iii) trait stability within environments quantified by standard errors among replicate samples ( stability) and (iv) Eberhart and Russells {beta} which quantifies trait stabilities across environments ({beta} stability). All four analyses yielded highly significantly associated SNPs. We found that high oleic varieties exhibited high {beta} trait stability, resulting in substantial overlap in markers between analyses (i) and (iv), with signals being fairly consistent between environments in analysis (i). For analyses (ii) and (iii), significant markers tended to vary between trials. For significant SNPs across all analyses, 147 candidate genes were identified, including promising candidates such as 15 fatty acid metabolism genes, 6 heat shock proteins and 22 transcription factors. Lastly, a large introgression consisting of two flanking inverted sequences on Chromosome 5 was found to coincide with stability in the Georgia trial, suggesting a role in FA composition stability under high heat conditions.

plant biology↗

Genomic offsets predict observed kelp declines and suggest benefits of assisted migration in the Northeast Pacific

Kelp forests are widely distributed along temperate and polar coastlines worldwide and are among the worlds most productive and diverse marine ecosystems. Yet, due in part to ocean warming, they are declining and even disappearing in many parts of the world. While genomic tools can identify local adaptation and predict species responses to global change, these predictions have rarely been validated in the field, hampering their widespread use in conservation practice. Here, we applied a seascape genomics approach to investigate environmental adaptation in the two main canopy-forming species of the Northeast Pacific, Macrocystis tenuifolia and Nereocystis luetkeana. We leveraged whole-genome sequences of 598 individuals across 94 sites along the British Columbia and Washington coasts, together with 37 environmental variables. Both species showed genomic signatures of local adaptation, with distinct environmental drivers shaping adaptation in each species despite their co-occurrence across much of the studied area. Using gradient forests, we modelled the genetic turnover across environmental gradients and predicted populations vulnerability (genomic offset) under projected environmental conditions. Genomic offsets differed greatly among regions and were positively correlated with kelp declines observed to date, especially in Macrocystis, validating the link between genomic models and outcomes in the field and allowing us to translate genomic predictions into an ecologically meaningful metric: the risk of extirpation under global change. Our models predict that assisted migration could significantly attenuate kelps vulnerability to global change. Across environmentally heterogenous coastlines, short-distance migration can often substantially reduce future genomic-environmental mismatches, but in many cases, long-distance migration would be most beneficial. Our results highlight the potential of seascape genomics to predict vulnerability of populations to global change. Importantly, the validated link between our genomic models and ecological outcomes allows quantification of climate-driven extirpation risk and can inform conservation strategies to improve the resilience and sustainable management of these vulnerable ecosystems.

evolutionary biology↗

The genomic response to drought across spatiotemporal scales in Amaranthus tuberculatus

How genetic diversity responds to environmental change across spatiotemporal scales remains poorly understood despite its importance for species persistence in changing landscapes. Agricultural weeds offer ideal models for studying these adaptive dynamics as they rapidly evolve under both the intensive management practices designed to eliminate them and increasingly severe climate challenges such as drought. Here, we combine experimental and herbarium genomic approaches spanning within-generation to century-long timescales to understand how genome-wide variation responds to drought in Amaranthus tuberculatus. In this native species, a history of divergent selection between two ancestral lineages followed by secondary contact is thought to have facilitated its invasion into agriculture. A drought survival experiment on accessions from paired agricultural and natural populations across its range revealed substantial phenotypic variation differentiated by habitat, geography, and ancestry. Ancestry mapping revealed 43 independent regions across nearly all chromosomes that confer protective effects under drought, demonstrate particularly rapid allele frequency changes, and exhibit duration-specific selection over the course of the imposed drought. Observation of allele frequencies across the past century reveal evidence for climate-dependent fluctuating selection governing the evolution of drought-associated loci. Selection favors drought alleles during hot/dry years and selects against them in cool/wet years--a pattern more evident in long-term trends than in shorter temporal intervals, suggestive of adaptive lag in rapidly changing environments. By combining short and long-term spatiotemporal data, we demonstrate that fluctuating selection has preserved the polygenic variation underlying population responses to drought, enabling ongoing adaptive responses to contemporary land-use and climate change. Significance StatementUnderstanding how species cope with rapid climate and land use change requires studying evolutionary responses across scales. Using Amaranthus tuberculatus, a native species turned major agricultural weed, we bridge timescales by pairing a drought experiment with century-spanning herbarium genomics. We show that ancestry structures fitness under drought and has driven agricultural populations to be better drought-adapted. This involves many genes whose allele frequencies fluctuate with climate: drought-protective alleles increase during hot/dry years and decline in cool/wet years. These fluctuations maintain genetic diversity and enable climate tracking, which is imperfect over short timescales. By linking experimental and historical data, we uncover evolutionary dynamics missed by snapshots, improving predictions of species adaptation to environmental change and informing weed management.

evolutionary biology↗

Mapping and characterization of a novel powdery mildew resistance locus (PM2) in Cannabis sativa L.

Breeding genetic resistance to economically important crop diseases is the most sustainable strategy for disease management and enhancing agricultural and horticultural productivity, particularly where the application of synthetic pesticides is prohibited. Powdery mildew disease, caused by the biotrophic fungal pathogen Golovinomyces ambrosiae, is one of the most prevalent threats to the cannabis and hemp industry worldwide. In this study, we used bulk-segregant analysis (BSA) combined with high-throughput sequencing to identify and map a novel single dominant resistance (R) locus (designated PM2), that strongly suppresses powdery mildew infection and sporulation in Cannabis sativa. Histochemical analysis revealed that PM2-induced resistance is mediated by a highly localized hypersensitive response mainly in the epidermal cells of the host. Importantly, genetic markers capable of tracking PM2 resistance in breeding populations were developed using associated SNPs identified in this study.

plant biology↗

Evolutionary rescue during extreme drought

Populations declining due to climate change may need to evolve to persist. While evolutionary rescue has been demonstrated in theory and the lab, its relevance to natural populations facing climate change remains unknown. Here we link rapid evolution and population dynamics in scarlet monkeyflower, Mimulus cardinalis, during an exceptional drought. We leverage whole-genome sequencing across 55 populations to identify climate-associated loci. Simultaneously we track demography and allele frequency change throughout the drought. We establish range-wide population decline during the drought, geographically variable rapid evolution, and variable population recovery that is predictable by standing genetic variation in and rapid evolution at climate-associated loci. These findings demonstrate evolutionary rescue in the wild, showing that genetic variation at adaptive, but not neutral loci, predicts population recovery.

evolutionary biology↗

Population genomics reveals strong impacts of genetic drift without purging and guides conservation of bull and giant kelp

Kelp forests are declining in many parts of the northeast Pacific1-4. In small populations, genetic drift can reduce adaptive variation and increase fixation of recessive deleterious alleles5-7, but natural selection may purge harmful variants8-10. To understand evolutionary dynamics and inform restoration strategies, we investigated genetic structure and the outcomes of genetic drift and purging by sequencing the genomes of 429 bull kelp (Nereocystis luetkeana) and 211 giant kelp (Macrocystis pyrifera sensu lato11; cf. 12) from the coastlines of British Columbia and Washington. We identified 6-7 geographically and genetically distinct clusters in each species. Low effective population size was associated with low genetic diversity and high inbreeding coefficients (including increased selfing rates), with extreme variation in these genetic health indices among bull kelp populations but more moderate variation in giant kelp. We found no evidence that natural selection is purging putative recessive deleterious alleles in either species. Instead, genetic drift has fixed many such alleles in small populations of bull kelp, leading us to predict (1) reduced within-population inbreeding depression in small populations, which may be associated with an observed shift toward increased selfing rate, and (2) hybrid vigour in crosses between small populations. Our genomic findings imply several strategies for optimal sourcing and crossing of populations for restoration and aquaculture, but which require experimental validation. Overall, our work reveals strong genetic structure and suggests that conservation strategies should consider the multiple health risks faced by small populations whose evolutionary dynamics are dominated by genetic drift.

evolutionary biology↗

Genomic stability in the Galapagos Scalesia adaptive radiation: Consistent transposable element accumulation despite hybridization and ecological niche shifts

Transposable elements (TEs) have been hypothesized to play a pivotal role in driving diversification by facilitating the emergence of novel phenotypes and the accumulation of divergence between species. Hybridization and adaptation to novel niches are hypothesized to influence TE accumulation in genomes by disrupting genomic regulation, including the suppression of TE replication. The rapid speciation and ecological diversification characteristic of adaptive radiations offer a unique opportunity to examine the link between TE accumulation and speciation, diversification, hybridization and adaptation. Here, focusing on all 15 species of the genus Scalesia (Asteraceae), a radiation endemic to the Galapagos Islands, we test whether hybridization or shifts in ecological niche are associated with changes in TE accumulation in genomes. Our analyses reveal little to no variation in TE accumulation among Scalesia species nor its hybrid populations. Shifts in ecological niches, linked to climatic variation, did not result in discernible changes in TE accumulation, a surprising finding given the anticipated selective pressure imposed by aridity, a factor often linked to genome size reduction. We found no distinct patterns in the temporal accumulation of TEs, and no effects at the class or superfamily level. Our findings challenge the assertion that TEs have directly driven diversification, speciation and local adaptation. Instead, we suggest that TEs may simply be along for the ride, rather than actively contributing to plant diversification.

evolutionary biology↗

Rapid parallel adaptation in distinct invasions of Ambrosia artemisiifolia is driven by large-effect structural variants

When introduced to multiple distinct ranges, invasive species provide a compelling natural experiment for understanding the repeatability of adaptation. Ambrosia artemisiifolia is an invasive, noxious weed and chief cause of hay fever. Leveraging over 400 whole-genome sequences spanning the native range in North America and two invasions in Europe and Australia, we inferred demographically distinct invasion histories on each continent. Despite substantial differences in genetic source and effective population size changes during introduction, scans of both local climate adaptation and divergence from the native range revealed genomic signatures of parallel adaptation between invasions. Disproportionately represented among these parallel signatures are 37 large haploblocks - indicators of structural variation - that cover almost 20% of the genome and exist as standing genetic variation in the native range. Many of these haploblocks are associated with traits important for adaptation to local climate, like size and the timing of flowering, and have rapidly reformed native range clines in invasive ranges. Others show extreme frequency divergence between ranges, consistent with a response to divergent selection on different continents. Our results demonstrate the key role of large-effect standing variants in rapid adaptation during range expansion, a pattern that is robust to diverse invasion histories.

genomics↗

The evolution, diversity, and genetic architecture of sex in waterhemp (Amaranthus tuberculatus)

The evolution of separate sexes is hypothesized to occur through distinct pathways involving few large-effect or many small-effect alleles. However, we lack empirical evidence for how these different genetic architectures shape the transition from quantitative variation in sex expression to distinct male and female phenotypes. To explore these processes, we leveraged the recent transition of Amaranthus tuberculatus to dioecy within a predominantly monoecious genus, along with a sex-phenotyped population genomic dataset, and six newly generated chromosome-level haplotype phased assemblies. We identify a [~]3 Mb region strongly associated with sex through complementary SNP genotype and sequence-depth based analyses. Comparative genomics of these proto-sex chromosomes within the species and across the Amaranthus genus demonstrates remarkable variability in their structure and genic content, including numerous polymorphic inversions. No such inversion underlies the extended linkage we observe associated with sex determination. Instead, we identify a complex presence/absence polymorphism reflecting substantial Y-haplotype variation--structured by ancestry, geography, and habitat-- but only partially explaining phenotyped sex. Just over 10% of sexed individuals show phenotype-genotype mismatch in the sex-linked region, and along with observation of leakiness in the phenotypic expression of sex, suggest additional modifiers of sex and dynamic gene content within and between the proto-X and Y. Together, this work reveals a complex genetic architecture of sex determination in A. tuberculatus characterized by the maintenance of substantial haplotype diversity, and variation in the expression of sex.

evolutionary biology↗

Shared selection and genetic architecture drive strikingly repeatable evolution in long-term experimental hybrid populations

The degree to which evolution repeats itself has implications regarding the major forces driving evolution and the potential for evolutionary biology to be a predictive (versus solely historical) science. To understand the factors that control evolutionary repeatability, we experimentally evolved four replicate hybrid populations of sunflowers at natural sites for up to 14 years and tracked ancestry across the genome. We found that there was very strong negative selection against introgressed ancestry in several chromosomes, but positive selection for introgressed ancestry in one chromosome. Further, the strength of selection was influenced by recombination rate. High recombination regions had lower selection against introgressed ancestry due to more frequent recombination away from incompatible backgrounds. Strikingly, evolution was highly parallel across replicates, with shared selection driving 88% of variance in introgressed allele frequency change. Parallel evolution was driven by both high levels of sustained linkage in introgressed alleles and strong selection on large-effect quantitative trait loci. This work highlights the repeatability of evolution through hybridization and confirms the central roles that natural selection, genomic architecture, and recombination play in the process.

evolutionary biology↗

A chromosome-level genome assembly of the varied leaved jewelflower, Streptanthus diversifolius, reveals a recent whole genome duplication

The Streptanthoid complex, a clade of primarily Streptanthus and Caulanthus genera in the Thelypodieae tribe (Brassicaceae) is an emerging model system for ecological and evolutionary studies. This Complex spans the full range of the California Floristic Province including desert, foothill, and mountain environments. The ability of these related species to radiate into dramatically different environments makes them a desirable study subject for exploring how plant species expand their ranges and adapt to new environments over time. Ecological and evolutionary studies for this complex have revealed fascinating variation in serpentine soil adaptation, defense compounds, germination, flowering, and life history strategies. Until now a lack of available genomic resources has hindered the ability to relate these phenotypic observations to their underlying genetic and molecular mechanisms. To help remedy this situation we present here a chromosome-level genome assembly of Streptanthus diversifolius, a member of the Streptanthoid Complex, developed using Illumina, Hi-C, and HiFi sequencing technologies. Construction of this assembly also provides further evidence to support the previously reported recent whole genome duplication unique to the Thelypodieae tribe. This whole genome duplication may have provided individuals in the Streptanthoid Complex the genetic arsenal to rapidly radiate throughout the California Floristic Province and to occupy commonly inhospitable environments including serpentine soils.

genomics↗

Admixture with cultivated sunflower likely facilitated establishment and spread of wild sunflower (H. annuus) in Argentina

A better understanding of the genetic and ecological factors underlying successful invasions is critical to mitigate the negative impacts of invasive species. Here, we study the invasion history of Helianthus annuus populations from Argentina, with particular emphasis on the role of post-introduction admixture with cultivated sunflower (also H. annuus) and climate adaptation driven by large haploblocks. We conducted genotyping-by-sequencing of samples of wild populations as well as Argentinian cultivars and compared them with wild (including related annual Helianthus species) and cultivated samples from the native range. We also characterized samples for 11 known haploblocks associated with environmental variation in native populations to test whether haploblocks contributed to invasion success. Population genomics analyses supported two independent geographic sources for Argentinian populations, the central United States and Texas, but no significant contribution of related annual Helianthus species. We found pervasive admixture with cultivated sunflower, likely as result of post-introduction hybridization. Genomic scans between invasive populations and their native sources identified multiple genomic regions with evidence of selection in the invaded range. These regions significantly overlapped between the two native-invasive comparisons and showed disproportionally high crop ancestry, suggesting that crop alleles contributed to invasion success. We did not find evidence of climate adaptation mediated by haploblocks, yet outliers of genome scans were enriched in haploblock regions and, for at least two haploblocks, the cultivar haplotype was favored in the invaded range. Our results show that admixture with cultivated sunflower played a major role in the establishment and spread of H. annuus populations in Argentina.

evolutionary biology↗

Biotic interactions promote local adaptation to soil in plants

Although different ecological factors shape adaptative evolution in natural habitats, we know little about how their interactions impact local adaptation. Here we used eight generations of experimental evolution with outcrossing Brassica rapa plants as a model system, in eight treatment groups that varied in soil type, herbivory (with/without aphids), and pollination mode (hand- or bumblebee-pollination), to study how biotic interactions affect local adaptation to soil. First, we show that several plant traits evolved in response to biotic interactions in a soil-specific way. Second, using a reciprocal transplant experiment, we demonstrate that significant local adaptation to soil-type evolved in the "number of open flowers", a trait used as a fitness proxy, but only in plants that evolved with herbivory and bee pollination. Whole genome re-sequencing of experimental lines revealed that biotic interactions caused a 10-fold increase in the number of SNPs across the genome with significant allele frequency change, and that alleles with opposite allele frequency change in different soil types (antagonistic pleiotropy) were most common in plants with an evolutionary history of herbivory and bee pollination. Our results demonstrate that the interaction of mutualists and antagonists can facilitate local adaptation to soil type through antagonistic pleiotropy.

evolutionary biology↗

Reticulate evolution and rapid development of reproductive barriers upon secondary contact pose challenges for species delineation in a forest fungus

Reproductive barriers within morphospecies of the mushroom-forming fungi tend to be stronger between sympatric lineages, leading to speculation on whether they are being reinforced by selection against hybrids. In this study we use population genomic analyses together with in vitro crosses of a global sample of the wood decay fungus Trichaptum abietinum to investigate reproductive barriers within this morphotaxon and the processes that have shaped them. Our phylogeographic analyses show that the morphospecies is delimited into six major lineages, one in Asia, two in Europe, and three in North America. The two lineages present in Europe are interfertile and admixed, whereas our crosses show that the North American lineages are reproductively isolated. In Asia a more complex pattern appears, with partial intersterility between multiple sub-lineages that likely originated independently and more recently than the reproductive barriers in North America. We found pre-mating barriers in T. abietinum to be moderately correlated with genomic divergence, whereas fitness of the mated hybrids showed a strong positive correlation with increasing genomic divergence. Genome wide association analyses identified candidate genes with programmed cell death annotations, which are known to be involved in intersterility in distantly related fungi. Our demographic modelling and phylogenetic network analyses suggest that reproductive barriers in Trichaptum abietinum could have been reinforced upon secondary contact between lineages that diverged in allopatry during the Pleistocene glacial cycles. Our combination of experimental and genomic approaches demonstrate how T. abietinum is a tractable system for studying speciation mechanims.

evolutionary biology↗

Multiple Pleistocene refugia for Arctic White Heather (Cassiope tetragona) supported by population genomics analyses of contemporary and Little-Ice-Age samples

AimArctic plants survived the Pleistocene glaciations in unglaciated refugia, but the number of these refugia is often unclear. We use high-resolution genomic data from present-day and Little-Ice-Age populations of Arctic White Heather (Cassiope tetragona) to re-evaluate the biogeography of this species and determine whether it had multiple independent refugia or a single refugium in Beringia. LocationCircumpolar Arctic and Coastal British Columbia (BC) alpine TaxonCassiope tetragona L., subspecies saximontana and tetragona, outgroup C. mertensiana (Ericaceae) MethodsWe built genotyping-by-sequencing (GBS) libraries using Cassiope tetragona tissue from 36 Arctic locations, including two [~]250-500-year-old populations collected under glacial ice on Ellesmere Island, Canada. We assembled a de novo GBS reference and called variants in dDocent. Population structure, genetic diversity, and demography were inferred from PCA, ADMIXTURE, fastsimcoal2, SplitsTree, and several population genomics statistics. ResultsPopulation structure analyses identified 4-5 clusters that align with geographic locations. Nucleotide diversity was highest in Beringia and decreased eastwards across Canada. Demographic coalescent analysis of the site-frequency-spectrum dated the following splits from Alaska: BC subspecies saximontana (6 mya), Russia (1.5 mya), Europe (>300-600 kya), Greenland (100 kya). Northern Canada populations appear to be from the current interglacial (7-9 kya). Genetic variants from Alaska appeared more frequently in present-day than historic plants on Ellesmere Island. ConclusionsDemographic analyses show BC, Alaska, Russia, Europe, and Greenland all had separate refugia during the last major glaciations. Northern Canadian populations appear to be founded during the current interglacial with genetic contributions from Alaska, Europe, and Greenland. On Ellesmere Island, there is evidence for continued, recent gene flow with foreign variants introduced in the last 250-500 years. These results suggest that a re-analysis of other Arctic species with shallow population structure using higher resolution genomic markers and demographic analyses may help reveal deeper structure and other circumpolar glacial refugia.

genomics↗