Genotype-environment Association Analyses Research Articles

A genome-guided strategy for climate resilience in American chestnut restoration populations

American chestnut (Castanea dentata) is a deciduous tree species of eastern North America that was decimated by the introduction of the chestnut blight fungus (Cryphonectria parasitica) in the early 20th century. Although millions of American chestnuts survive as root collar sprouts, these trees rarely reproduce. Thus, the species is considered functionally extinct. American chestnuts with improved blight resistance have been developed through interspecific hybridization followed by conspecific backcrossing, and by genetic engineering. Incorporating adaptive genomic diversity into these backcross families and transgenic lines is important for restoring the species across broad climatic gradients. To develop sampling recommendations for ex situ conservation of wild adaptive genetic variation, we coupled whole-genome resequencing of 384 stump sprouts with genotype-environment association analyses and found that the species range can be subdivided into three seed zones characterized by relatively homogeneous adaptive allele frequencies. We estimated that 21 to 29 trees per seed zone will need to be conserved to capture most extant adaptive diversity. We also resequenced the genomes of 269 backcross trees to understand the extent to which the breeding program has already captured wild adaptive diversity, and to estimate optimal reintroduction sites for specific families on the basis of their adaptive portfolio and future climate projections. Taken together, these results inform the development of an ex situ germplasm conservation and breeding plan to target blight-resistant breeding populations to specific environments and provides a blueprint for developing restoration plans for other imperiled tree species.

Seascapes Shaped the Local Adaptation and Population Structure of South China Coast Yellowfin Seabream (Acanthopagrus latus).

Understanding the genetic composition and regional adaptation of marine species under environmental heterogeneity and fishing pressure is crucial for responsible management. In order to understand the genetic diversity and adaptability of yellowfin seabream (Acanthopagrus latus) along southern China coast, this study was conducted a seascape genome analysis on yellowfin seabream from the ecologically diverse coast, spanning over 1600 km. A total of 92 yellowfin seabream individuals from 15 sites were performed whole-genome resequencing, and 4,383,564 high-quality single nucleotide polymorphisms (SNPs) were called. By conducting a genotype-environment association analysis, 29,951 adaptive and 4,328,299 neutral SNPs were identified. The yellowfin seabream exhibited two distinct population structures, despite high gene flow between sites. The seascape genome analysis revealed that genetic structure was influenced by a variety of factors including salinity gradients, habitat distance, and ocean currents. The frequency of allelic variation at the candidate loci changed with the salinity gradient. Annotation of these loci revealed that most of the genes are associated with osmoregulation, such as kcnab2a, kcnk5a, and slc47a1. These genes are significantly enriched in pathways associated with ion transport including G protein-coupled receptor activity, transmembrane signaling receptor activity, and transporter activity. Overall, our findings provide insights into how seascape heterogeneity affects adaptive evolution, while providing important information for regional management in yellowfin seabream populations.

Projection of current and future distribution of adaptive genetic units in an alpine ungulate.

Climate projections predict major changes in alpine environments by the end of the 21st century. To avoid climate-induced maladaptation and extinction, many animal populations will either need to move to more suitable habitats or adapt in situ to novel conditions. Since populations of a species exhibit genetic variation related to local adaptation, it is important to incorporate this variation into predictive models to help assess the ability of the species to survive climate change. Here, we evaluate how the adaptive genetic variation of a mountain ungulate-the Northern chamois (Rupicapra rupicapra)-could be impacted by future global warming. Based on genotype-environment association analyses of 429 chamois using a ddRAD sequencing approach, we identified genetic variation associated with climatic gradients across the European Alps. We then delineated adaptive genetic units and projected the optimal distribution of these adaptive groups in the future. Our results suggest the presence of local adaptation to climate in Northern chamois with similar genetic adaptive responses in geographically distant but climatically similar populations. Furthermore, our results predict that future climatic changes will modify the Northern chamois adaptive landscape considerably, with various degrees of maladaptation risk.

Genetic and environmental drivers of migratory behavior in western burrowing owls and implications for conservation and management.

Migration is driven by a combination of environmental and genetic factors, but many questions remain about those drivers. Potential interactions between genetic and environmental variants associated with different migratory phenotypes are rarely the focus of study. We pair low coverage whole genome resequencing with a de novo genome assembly to examine population structure, inbreeding, and the environmental factors associated with genetic differentiation between migratory and resident breeding phenotypes in a species of conservation concern, the western burrowing owl (Athene cunicularia hypugaea). Our analyses reveal a dichotomy in gene flow depending on whether the population is resident or migratory, with the former being genetically structured and the latter exhibiting no signs of structure. Among resident populations, we observed significantly higher genetic differentiation, significant isolation-by-distance, and significantly elevated inbreeding. Among migratory breeding groups, on the other hand, we observed lower genetic differentiation, no isolation-by-distance, and substantially lower inbreeding. Using genotype-environment association analysis, we find significant evidence for relationships between migratory phenotypes (i.e., migrant versus resident) and environmental variation associated with cold temperatures during the winter and barren, open habitats. In the regions of the genome most differentiated between migrants and residents, we find significant enrichment for genes associated with the metabolism of fats. This may be linked to the increased pressure on migrants to process and store fats more efficiently in preparation for and during migration. Our results provide a significant contribution toward understanding the evolution of migratory behavior and vital insight into ongoing conservation and management efforts for the western burrowing owl.

Evolutionary history and seascape genomics of Harbour porpoises (Phocoena phocoena) across environmental gradients in the North Atlantic and adjacent waters.

The Harbour porpoise (Phocoena phocoena) is a highly mobile cetacean species primarily occurring in coastal and shelf waters across the Northern hemisphere. It inhabits heterogeneous seascapes broadly varying in salinity and temperature. Here, we produced 74 whole genomes at intermediate coverage to study Harbour porpoise's evolutionary history and investigate the role of local adaptation in the diversification into subspecies and populations. We identified ~6 million high quality SNPs sampled at eight localities across the North Atlantic and adjacent waters, which we used for population structure, demographic and genotype-environment association analyses. Our results suggest a genetic differentiation between three subspecies (P.p. relicta, P.p. phocoena and P.p. meridionalis), and three distinct populations within P.p. phocoena: Atlantic, Belt Sea and Proper Baltic Sea. Effective population size and Tajima's D suggest population contraction in Black Sea and Iberian porpoises, but expansion in the P.p. phocoena populations. Phylogenetic trees indicate post-glacial colonization from a southern refugium. Genotype-environment association analysis identified salinity as major driver in genomic variation and we identified candidate genes putatively underlying adaptation to different salinity. Our study highlights the value of whole genome resequencing to unravel subtle population structure in highly mobile species, shows how strong environmental gradients and local adaptation may lead to population differentiation, and how neutral and adaptive markers can give different perspectives on population subdivision. The results have great conservation implications as we found inbreeding and low genetic diversity in the endangered Black Sea subspecies and identified the critically endangered Proper Baltic Sea porpoises as a separate population.

Adaptive phenotypic and genomic divergence in the common chaffinch (Fringilla coelebs) following niche expansion within a small oceanic island.

According to models of ecological speciation, adaptation to adjacent, contrasting habitat types can lead to population divergence given strong enough environment-driven selection to counteract the homogenizing effect of gene flow. We tested this hypothesis in the common chaffinch (Fringilla coelebs) on the small island of La Palma, Canary Islands, where it occupies two markedly different habitats. Isotopic (δ13 C, δ15 N) analysis of feathers indicated that birds in the two habitats differed in ecosystem and/or diet, and analysis of phenotypic traits revealed significant differences in morphology and plumage colouration that are consistent with ecomorphological and ecogeographical predictions respectively. A genome-wide survey of single-nucleotide polymorphism revealed marked neutral structure that was consistent with geography and isolation by distance, suggesting low dispersal. In contrast, loci putatively under selection identified through genome-wide association and genotype-environment association analyses, revealed amarked adaptive divergence between birds in both habitats. Loci associated with phenotypic and environmental differences among habitats were distributed across the genome, as expected for polygenic traits involved in local adaptation. Our results suggest a strong role for habitat-driven local adaptation in population divergence in the chaffinches of La Palma, a process that appears to be facilitated by a strong reduction in effective dispersal distances despite the birds' high dispersal capacity.

Key triggers of adaptive genetic variability of sessile oak [Q. petraea (Matt.) Liebl.] from the Balkan refugia: outlier detection and association of SNP loci from ddRAD-seq data

Knowledge on the genetic composition of Quercus petraea in south-eastern Europe is limited despite the species’ significant role in the re-colonisation of Europe during the Holocene, and the diverse climate and physical geography of the region. Therefore, it is imperative to conduct research on adaptation in sessile oak to better understand its ecological significance in the region. While large sets of SNPs have been developed for the species, there is a continued need for smaller sets of SNPs that are highly informative about the possible adaptation to this varied landscape. By using double digest restriction site associated DNA sequencing data from our previous study, we mapped RAD-seq loci to the Quercus robur reference genome and identified a set of SNPs putatively related to drought stress-response. A total of 179 individuals from eighteen natural populations at sites covering heterogeneous climatic conditions in the southeastern natural distribution range of Q. petraea were genotyped. The detected highly polymorphic variant sites revealed three genetic clusters with a generally low level of genetic differentiation and balanced diversity among them but showed a north–southeast gradient. Selection tests showed nine outlier SNPs positioned in different functional regions. Genotype-environment association analysis of these markers yielded a total of 53 significant associations, explaining 2.4–16.6% of the total genetic variation. Our work exemplifies that adaptation to drought may be under natural selection in the examined Q. petraea populations.

Landscape genomics reveals signals of climate adaptation and a cryptic lineage in Arthropodium fimbriatum

Habitat loss and fragmentation are critical threats to biodiversity. Consequent decreases in population size and connectivity can impact genetic diversity and, thus, future adaptability and resilience to environmental change. Understanding landscape patterns of genetic diversity, including patterns of adaptive variation, can assist in developing conservation strategies that maximise population persistence and adaptability in the face of environmental change. Using a reduced-representation genomic approach, we investigated genetic diversity, structure, and adaptive variation across an aridity gradient in the woodland forb Arthropodium fimbriatum. Moderate levels of genetic diversity (HS = 0.14–0.23) were found in all 13 sampled provenances. Inbreeding varied among provenances (FIS = 0.08–0.42) but was not associated with estimated population size. Four genetic clusters were identified, including one highly differentiated cluster. Higher pairwise FST (0.23–0.42) between the three provenances of this cluster and the remaining 10 provenances (pairwise FST between 10 provenances 0.02–0.32) suggested two highly divergent lineages or potentially a cryptic species. After excluding the three highly differentiated populations, outlier and genotype-environment association analysis identified 275 putatively adaptive loci suggesting genomic signatures of climate adaptation in A. fimbriatum is primarily associated with changes in aridity. Combined, these results suggest that all provenances have conservation value, contributing to the maintenance of genetic diversity and adaptive variation in this species. The uncovering of a potential cryptic taxon highlights the power of genomics approaches in conservation genetics and the importance of understanding the role of landscape variation shaping genetic variation to effectively define conservation management units in an era of rapid biodiversity decline.

Genomic vulnerability to climate change in Quercus acutissima, a dominant tree species in East Asian deciduous forests.

Understanding the evolutionary processes that shape the landscape of genetic variation and influence the response of species to future climate change is critical for biodiversity conservation. Here, we sampled 27 populations across the distribution range of a dominant forest tree, Quercus acutissima, in East Asia, and applied genome-wide analyses to track the evolutionary history and predict the fate of populations under future climate. We found two genetic groups (East and West) in Q.acutissima that diverged during Pliocene. We also found a heterogeneous landscape of genomic variation in this species, which may have been shaped by population demography and linked selections. Using genotype-environment association analyses, we identified climate-associated SNPs in a diverse set of genes and functional categories, indicating a model of polygenic adaptation in Q.acutissima. We further estimated three genetic offset metrics to quantify genomic vulnerability of this species to climate change due to the complex interplay between local adaptation and migration. We found that marginal populations are under higher risk of local extinction because of future climate change, and may not be able to track suitable habitats to maintain the gene-environment relationships observed under the current climate. We also detected higher reverse genetic offsets in northern China, indicating that genetic variation currently present in the whole range of Q.acutissima may not adapt to future climate conditions in this area. Overall, this study illustrates how evolutionary processes have shaped the landscape of genomic variation, and provides a comprehensive genome-wide view of climate maladaptation in Q.acutissima.

Conservation genomics of an endangered arboreal mammal following the 2019–2020 Australian megafire

The impacts of a changing climate threaten species, populations and ecosystems. Despite these significant and large-scale impacts on threatened species, many remain understudied and have little to no genetic information available. The greater glider, Petauroides volans, is an endangered species highly sensitive to the predicted changes in temperature under a changing climate and was recently severely impacted by a megafire natural disaster (85% estimated population loss). Baseline genetic data is essential for conservation management and for detecting detrimental changes in fire-effected populations. We collected genetic samples within 2 years post the 2019–2020 catastrophic Australian bushfires to examine adaptive potential, baseline genetic diversity and population structure, across their southern range in the state of New South Wales. Population genomic analyses were conducted using 8493 genome-wide SNPs for 86 greater glider individuals across 14 geographic locations. Substantial genetic structure was detected across locations, with low genetic diversity and effective population sizes observed in isolated areas. Additionally, we found signals of putative adaptation in response to temperature in greater gliders using a genotype-environment association analysis. These findings have important implications for the management of greater glider populations by identifying at-risk populations and identifying adaptive potential. We demonstrate the importance of baseline genetic information for endangered species as a practical approach to conservation. This is particularly important given the threat that changes in temperatures and megafire events, as predicted under a changing climate, poses for this species.

Whole genome resequencing identifies local adaptation associated with environmental variation for redband trout.

Aquatic ectotherms are predicted to harbour genomic signals of local adaptation resulting from selective pressures driven by the strong influence of climate conditions on body temperature. We investigated local adaptation in redband trout (Oncorhynchus mykiss gairdneri) using genome scans for 547 samples from 11 populations across a wide range of habitats and thermal gradients in the interior Columbia River. We estimated allele frequencies for millions of single nucleotide polymorphism loci (SNPs) across populations using low-coverage whole genome resequencing, and used population structure outlier analyses to identify genomic regions under divergent selection between populations. Twelve genomic regions showed signatures of local adaptation, including two regions associated with genes known to influence migration and developmental timing in salmonids (GREB1L, ROCK1, SIX6). Genotype-environment association analyses indicated that diurnal temperature variation was a strong driver of local adaptation, with signatures of selection driven primarily by divergence of two populations in the northern extreme of the subspecies range. We also found evidence for adaptive differences between high-elevation desert vs. montane habitats at a smaller geographical scale. Finally, we estimated vulnerability of redband trout to future climate change using ecological niche modelling and genetic offset analyses under two climate change scenarios. These analyses predicted substantial habitat loss and strong genetic shifts necessary for adaptation to future habitats, with the greatest vulnerability predicted for high-elevation desert populations. Our results provide new insight into the complexity of local adaptation in salmonids, and important predictions regarding future responses of redband trout to climate change.

Genomic divergence between two sister Ostrya species through linked selection and recombination.

Studying the evolution of genomic divergence between lineages is a topical issue in evolutionary biology. However, the evolutionary forces that shape the heterogeneous divergence of the genomic landscape are still poorly understood. Here, two wind-pollinated sister-species (Ostrya japonica and O. chinensis) are used to explore what these potential forces might be. A total of 40 individuals from 16 populations across their main distribution areas in China were sampled for genome-wide resequencing. Population demography analyses revealed that these two sister-species diverged at 3.06-4.43 Mya. Both population contraction and increased gene flow were detected during glacial periods, suggesting secondary contact at those times. All three parameters (D XY, π, and ρ) decreased in those regions showing high levels of differentiation (F ST). These findings indicate that linked selection and recombination played a key role in the genomic heterogeneous differentiation between the two Ostrya species. Genotype-environment association analyses showed that precipitation was the most important ecological factor for speciation. Such environmentally related genes and positive selection genes may have contributed to local adaptation and the maintenance of species boundaries.

Re-evaluating Coho salmon (Oncorhynchus kisutch) conservation units in Canada using genomic data.

Conservation units (CUs) are important tools for supporting the implementation of standardized management practices for exploited species. Following the adoption of the Wild Salmon Policy in Canada, CUs were defined for Pacific salmon based on characteristics related to ecotype, life history and genetic variation using microsatellite markers as indirect measures of local adaptation. Genomic data sets have the potential to improve the definition of CUs by reducing variance around estimates of population genetic parameters, thereby increasing the power to detect more subtle patterns of population genetic structure and by providing an opportunity to incorporate adaptive information more directly with the identification of variants putatively under selection. We used one of the largest genomic data sets recently published for a nonmodel species, comprising 5662 individual Coho salmon (Oncorhynchus kisutch) from 149 sampling locations and a total of 24,542 high-quality SNPs obtained using genotyping-by-sequencing and mapped to the Coho salmon reference genome to (1) evaluate the current delineation of CUs for Coho in Canada and (2) compare patterns of population structure observed using neutral and outlier loci from genotype-environment association analyses to determine whether separate CUs that capture adaptive diversity are needed. Our results reflected CU boundaries on the whole, with the majority of sampling locations managed in the same CU clustering together within genetic groups. However, additional groups that are not currently represented by CUs were also uncovered. We observed considerable overlap in the genetic clusters identified using neutral or candidate loci, indicating a general congruence in patterns of genetic variation driven by local adaptation and gene flow in this species. Consequently, we suggest that the current CU boundaries for Coho salmon are largely well-suited for meeting the Canadian Wild Salmon Policy's objective of defining biologically distinct groups, but we highlight specific areas where CU boundaries may be refined.

Genotype-environment associations across spatial scales reveal the importance of putative adaptive genetic variation in divergence.

Identifying areas of high evolutionary potential is a judicious strategy for developing conservation priorities in the face of environmental change. For wide‐ranging species occupying heterogeneous environments, the evolutionary forces that shape distinct populations can vary spatially. Here, we investigate patterns of genomic variation and genotype–environment associations in the hermit thrush (Catharus guttatus), a North American songbird, at broad (across the breeding range) and narrow spatial scales (at a hybrid zone). We begin by building a genoscape or map of genetic variation across the breeding range and find five distinct genetic clusters within the species, with the greatest variation occurring in the western portion of the range. Genotype–environment association analyses indicate higher allelic turnover in the west than in the east, with measures of temperature surfacing as key predictors of putative adaptive genomic variation rangewide. Since broad patterns detected across a species' range represent the aggregate of many locally adapted populations, we investigate whether our broadscale analysis is consistent with a finer scale analysis. We find that top rangewide temperature‐associated loci vary in their clinal patterns (e.g., steep clines vs. fixed allele frequencies) across a hybrid zone in British Columbia, suggesting that the environmental predictors and the associated candidate loci identified in the rangewide analysis are of variable importance in this particular region. However, two candidate loci exhibit strong concordance with the temperature gradient in British Columbia, suggesting a potential role for temperature‐related barriers to gene flow and/or temperature‐driven ecological selection in maintaining putative local adaptation. This study demonstrates how patterns identified at the broad (macrogeographic) scale can be validated by investigating genotype–environment correlations at the local (microgeographic) scale. Furthermore, our results highlight the importance of considering the spatial distribution of putative adaptive variation when assessing population‐level sensitivity to climate change and other stressors.

Hybrid enrichment of adaptive variation revealed by genotype-environment associations in montane sedges.

The role of hybridization in diversification is complex and may result in many possible outcomes. Not only can hybridization produce new lineages, but those lineages may contain unique combinations of adaptive genetic variation derived from parental taxa that allow hybrid‐origin lineages to occupy unique environmental space relative to one (or both) parent(s). We document such a case of hybridization between two sedge species, Carex nova and Carex nelsonii (Cyperaceae), that occupy partially overlapping environmental space in the southern Rocky Mountains, USA. In the region hypothesized to be the origin of the hybrid lineage, one parental taxon (C. nelsonii) is at the edge of its environmental tolerance. Hybrid‐origin individuals display mixed ancestry between the parental taxa—of nearly 7000 unlinked loci sampled, almost 30% showed evidence of excess ancestry from one parental lineage—approximately half displayed a genomic background skewed towards one parent, and half skewed towards the other. To test whether excess ancestry loci may have conferred an adaptive advantage to the hybrid‐origin lineage, we conducted genotype–environment association analyses on different combinations of loci—with and without excess ancestry—and with multiple contrasts between the hybrids and parental taxa. Loci with skewed ancestry showed significant environmental associations distinguishing the hybrid lineage from one parent (C. nelsonii), whereas loci with relatively equal representation of parental ancestries showed no such environmental associations. Moreover, the overwhelming majority of candidate adaptive loci with respect to environmental gradients also had excess ancestry from a parental lineage, implying these loci have facilitated the persistence of the hybrid lineage in an environment unsuitable to at least one parent.

Seascape genomics of coastal bottlenose dolphins along strong gradients of temperature and salinity.

Heterogeneous seascapes and strong environmental gradients in coastal waters are expected to influence adaptive divergence, particularly in species with large population sizes where selection is expected to be highly efficient. However, these influences might also extend to species characterized by strong social structure, natal philopatry and small home ranges. We implemented a seascape genomic study to test this hypothesis in Indo-Pacific bottlenose dolphins (Tursiops aduncus) distributed along the environmentally heterogeneous coast of southern Australia. The data sets included oceanographic and environmental variables thought to be good predictors of local adaptation in dolphins and 8081 filtered single nucleotide polymorphisms (SNPs) genotyped for individuals sampled from seven different bioregions. From a neutral perspective, population structure and connectivity of the dolphins were generally influenced by habitat type and social structuring. Genotype-environment association analysis identified 241 candidate adaptive loci and revealed that sea surface temperature and salinity gradients influenced adaptive divergence in these animals at both large- (1000km) and fine-scales (<100km). Enrichment analysis and annotation of candidate genes revealed functions related to sodium-activated ion transport, kidney development, adipogenesis and thermogenesis. The findings of spatial adaptive divergence and inferences of putative physiological adaptations challenge previous suggestions that marine megafauna is most likely to be affected by environmental and climatic changes via indirect, trophic effects. Our work contributes to conservation management of coastal bottlenose dolphins subjected to anthropogenic disturbance and to efforts of clarifying how seascape heterogeneity influences adaptive diversity and evolution in small cetaceans.

Moths passing in the night: Phenological and genomic divergences within a forest pest complex.

Temporal separation of reproductive timing can contribute to species diversification both through allochronic speciation and later reinforcement of species boundaries. Such phenological differences are an enigmatic component of evolutionary divergence between two major forest defoliator species of the spruce budworm complex: Choristoneura fumiferana and C. occidentalis. While these species interbreed freely in laboratory settings, natural hybridization rates have not been reliably quantified due to their indistinguishable morphology. To assess whether temporal isolation is contributing to reproductive isolation, we collected adult individuals throughout their expected zone of sympatry in western Canada at 10‐day intervals over two successive years, assigning taxonomic identities using thousands of single nucleotide polymorphisms. We found unexpectedly broad sympatry between C. fumiferana and C. occidentalis biennis and substantial overlap of regional flight periods. However, flight period divergence was much more apparent on a location‐by‐location basis, highlighting the importance of considering spatial scale in these analyses. Phenological comparisons were further complicated by the biennial life cycle of C. o. biennis, the main subspecies of C. occidentalis in the region, and the occasional occurrence of the annually breeding subspecies C. o. occidentalis. Nonetheless, we demonstrate that biennialism is not a likely contributor to reproductive isolation within the species complex. Overall, interspecific F1 hybrids comprised 2.9% of sequenced individuals, confirming the genomic distinctiveness of C. fumiferana and C. occidentalis, while also showing incomplete reproductive isolation of lineages. Finally, we used F ST‐based outlier and genotype–environment association analyses to identify several genomic regions under putative divergent selection. These regions were disproportionately located on the Z linkage region of C. fumiferana, and contained genes, particularly antifreeze proteins, that are likely to be associated with overwintering success and diapause. In addition to temporal isolation, we conclude that other mechanisms, including ecologically mediated selection, are contributing to evolutionary divergence within the spruce budworm species complex.

Gene flow influences the genomic architecture of local adaptation in six riverine fish species.

Understanding how gene flow influences adaptive divergence is important for predicting adaptive responses. Theoretical studies suggest that when gene flow is high, clustering of adaptive genes in fewer genomic regions would protect adaptive alleles from recombination and thus be selected for, but few studies have tested it with empirical data. Here, we used restriction site-associated sequencing to generate genomic data for six fish species with contrasting life histories from six reaches of the Upper Mississippi River System, USA. We used four differentiation-based outlier tests and three genotype-environment association analyses to define neutral single nucleotide polymorphisms (SNPs) and outlier SNPs that were putatively under selection. We then examined the distribution of outlier SNPs along the genome and investigated whether these SNPs were found in genomic islands of differentiation and inversions. We found that gene flow varied among species, and outlier SNPs were clustered more tightly in species with higher gene flow. The two species with the highest overall FST (0.0303-0.0720) and therefore lowest gene flow showed little evidence of clusters of outlier SNPs, with outlier SNPs in these species spreading uniformly across the genome. In contrast, nearly all outlier SNPs in the species with the lowest FST (0.0003) were found in a single large putative inversion. Two other species with intermediate gene flow (FST ~0.0025-0.0050) also showed clustered genomic architectures, with most islands of differentiation clustered on a few chromosomes. Our results provide important empirical evidence to support the hypothesis that increasingly clustered architecture of local adaptation is associated with high gene flow.

Genomic signatures of domestication and adaptation during geographical expansions of rice cultivation

Rice (Oryza sativa L.), a global staple food now grown on all inhabited continents, was domesticated from its wild progenitor, O. rufipogon Griff., in tropical and subtropical regions of Asia (Oka, 1988). After domestication, the expansions of rice landraces into the present-day range required a diverse array of adaptations to local environments, which included changes in daylight sensitivity, expanded thermal tolerance (for excess cold and heat), adaptations to water availability (drought and waterlogging), and resistance to biotic stresses (Garris et al., 2005; Glaszmann, 1987).

Adaptive and nonadaptive causes of heterogeneity in genetic differentiation across the Mimulus guttatus genome.

Genetic diversity becomes structured among populations over time due to genetic drift and divergent selection. Although population structure is often treated as a uniform underlying factor, recent resequencing studies of wild populations have demonstrated that diversity in many regions of the genome may be structured quite dissimilar to the genome-wide pattern. Here, we explored the adaptive and nonadaptive causes of such genomic heterogeneity using population-level, whole genome resequencing data obtained from annual Mimulus guttatus individuals collected across a rugged environment landscape. We found substantial variation in how genetic differentiation is structured both within and between chromosomes, although, in contrast to other studies, known inversion polymorphisms appear to serve only minor roles in this heterogeneity. In addition, much of the genome can be clustered into eight among-population genetic differentiation patterns, but only two of these clusters are particularly consistent with patterns of isolation by distance. By performing genotype-environment association analysis, we also identified genomic intervals where local adaptation to specific climate factors has accentuated genetic differentiation among populations, and candidate genes in these windows indicate climate adaptation may proceed through changes affecting specialized metabolism, drought resistance, and development. Finally, by integrating our findings with previous studies, we show that multiple aspects of plant reproductive biology may be common targets of balancing selection and that variants historically involved in climate adaptation among populations have probably also fuelled rapid adaptation to microgeographic environmental variation within sites.