Article

The Genomic Basis of Local Climatic Adaptation

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Abstract

Studies of Arabidopsis thaliana help to identify the genomic sites associated with adaptation to local climatic conditions.

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... Elle renseigne plus sur les ressemblances génétiques entre les populations testées, dont l'interprétation se rapproche plus de celle des lignées génétiques. Les études génétiques récentes portant sur l'adaptation au climat local mettent en évidence des relations significatives entre certains gènes et le climat dans lequel poussent ces arbres Savolainen, 2011), notamment pour le pin cembro (Mosca et al., 2012). En testant le lien entre la génétique adaptative et la dendrochronologie, on pourrait s'attendre à des corrélations plus élevées relativement à celle des variables non-génétiques. ...
... Par ailleurs, on observe un déficit de survie des semis issus de régénérations naturelles au sein des populations marginales de thuya , et la multiplication végétative reste le mode garantissant actuellement le maintien des populations de thuya (Paul et al., 2014 ;Visnadi, 2014). Étant donné que la reproduction sexuée est le principal vecteur d'apparition de nouvelles combinaisons génétiques (Savolainen, 2011 ...
... Ce facteur est primordial pour l'adaptation rapide des populations en permettant une réponse immédiate au changement climatique par la sélection parmi les variations déjà existante Antoine Kremer et al., 2012 ;Savolainen, 2011). ...
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Cette thèse a pour objectif de déterminer le devenir des populations marginales d’arbres boréo-montagnards dans le contexte des changements climatiques. La réponse dendroclimatique et la structure génétique des espèces sont analysées conjointement sur des gradients incluant les zones de distributions continues et marginales. Les deux modèles biologiques choisis sont le thuya occidental en limite nordique (forêt boréale canadienne) et le pin cembro en limite occidentale (Alpes). Les hypothèses suivantes ont été testées : le réchauffement climatique au cours du XXe siècle a entrainé une augmentation de croissance ; la variabilité de croissance est reliée à la structure génétique aux niveaux intra- et inter-populationnels. Une baisse de croissance du thuya a été observée après 1980 en zone marginale, qui serait liée à une limitation par la sécheresse. Pour les deux espèces, les relations climat-croissance étaient essentiellement modulées par le volume des précipitations, mais également par des variables édaphiques et par la taille des arbres. L’existence d’un lien significatif entre la structure génétique et certaines variables climatiques laisse néanmoins espérer un potentiel d'adaptation génétique, dont l’ampleur dépendra de la diversité génétique disponible pour la sélection naturelle. Par ailleurs, le synchronisme de croissance entre les arbres était à la fois influencé par la diversité génétique intra-populationnelle et par le volume des précipitations. En conclusion, il apparaît très difficile de distinguer les effets du climat et de la génétique sur la croissance des arbres étudiés.
... Empirical studies have found some evidence that alleles responsible for local adaptation show tradeoffs across contrasting environments (Anderson et al. 2011;Ågren et al. 2013). However, it also is clear that many alleles contributing to local adaptation experience conditional neutrality (CN), contributing to higher (or lower) fitness in one environment while having no fitness effect in other locations (Schnee and Thompson 1984;Thompson 2005;Gardner and Latta 2006;Verhoeven et al. 2008;Lowry et al. 2009; Fournier-Level et al. 2011;Anderson et al. 2013Anderson et al. , 2014aYoder et al. 2014). We do not know how often local adaptation in natural populations evolves by AP or under CN. ...
... Landscape genomic scans have become a common method for trying to identify locally adapted loci and in order to understand how geographically variable selection shapes the genetic diversity within species (Savolainen 2011;Tiffin and Ross-Ibarra 2014). These scans provide a means to identify locally adapted genome regions without an a priori list of genes under selection, or even a strong prior hypothesis as to what environmental gradients drive local adaptation, or which traits are responsible for local adaptation. ...
Article
Genomic "scans" to identify loci that contribute to local adaptation are becoming increasingly common. Many methods used for such studies have assumed that local adaptation is created by loci experiencing antagonistic pleiotropy and that the selected locus itself is assayed, and few consider how signals of selection change through time. However, most empirical data sets have marker density too low to assume that a selected locus itself is assayed, researchers seldom know when selection was first imposed, and many locally adapted loci likely experience not antagonistic pleiotropy but conditional neutrality. We simulated data to evaluate how these factors affect the performance of tests for genotype-environment association. We found that three types of regression-based analyses (linear models, mixed linear models, and latent factor mixed models) and an implementation of BayEnv all performed well, with high rates of true positives and low rates of false positives, when the selected locus experienced antagonistic pleiotropy, and when the selected locus was assayed directly. However, all tests had reduced power to detect loci experiencing conditional neutrality, and the probability of detecting associations was sharply reduced when physically linked rather than causative loci were sampled. Antagonistic pleiotropy also maintained detectable genotype-environment associations much longer than conditional neutrality. Our analyses suggest that if local adaptation is often driven by loci experiencing conditional neutrality, genome-scan methods will have limited capacity to find loci responsible for local adaptation.
... Since sessile plants are subject to spatially divergent selection, elucidating the effects of local adaptation on population differentiation has become more important in light of adaptation to changing environments, including global climate change (Ehrich & Raven, 1969;Savolainen, 2011;Colautti et al., 2012). A commonly used way to infer the impact of divergent selection on plant population differentiation is by comparing Q ST (reflecting differentiation caused by both neutral and selective forces) versusF ST estimates (reflecting differentiation due to neutral processes including genetic drift) (Whitlock, 2008). ...
Preprint
Increased access to genome-wide data provides new opportunities for plant conservation. However, information on neutral genetic diversity in a small number of marker loci can still be valuable because genomic data are not available to most rare plant species. In the hope of bridging the gap between conservation science and practice, we outline how conservation practitioners can more efficiently employ population genetic information in plant conservation. We first review the current knowledge about the within-population genetic variation and among-population differentiation in neutral genetic variation (NGV) and adaptive genetic variation (AGV) in seed plants. We then introduce the estimates of among-population genetic differentiation in quantitative traits ( Q ) and neutral markers ( F ) to plant biology and summarize conservation applications derived from Q – F comparisons, particularly on how to capture most AGV and NGV on both in-situ and ex-situ programs. Based on a review of published studies, we found that, on average, two and four populations would be needed for woody perennials ( n = 18) to capture 99% of neutral and adaptive genetic variation, respectively, whereas four populations would be needed in case of herbaceous perennials ( n = 14). On average, Q is about 3.6, 1.5, and 1.1 times greater than F in woody plants, annuals, and herbaceous perennials, respectively. We suggest using maximum Q rather than average Q among trait comparisons. Hence, conservation and management policies or suggestions based solely on inference on F could be misleading, particularly in woody species. We recommend conservation managers and practitioners consider this when formulating further conservation and restoration plans for plant species, and for woody species in particular.
... contrasting habitats. Indeed, local adaptation along environmental gradients was found in plants and animals (Reznick and Ghalambor 2001;Leimu and Fischer 2008;Savolainen 2011). Environmental gradients might not only be of natural origin but might also be determined by anthropogenic influences. ...
Article
Grassland species might be under differential selection pressure due to management regimes by man or unmanaged grazers. To investigate microevolutionary changes in plants, I used a meta-analysis and a comparative approach. This analysis incorporates 28 studies on 19 species in 3 paired management regimes with a total of 152 reported trait values resulting in 40 pooled Hedge’s d effect sizes on genetic, vegetative and reproductive traits as well as 83 Hedge’s ds of 14 specific traits. Of the pooled and specific traits, 60 and 72 % indicated divergent selection pressures within a management regime. The pooled Hedge’s ds did not differ among the management regimes. Within mown versus grazed sites, trait groups were affected differently with increased reproductive traits in plants originating from grazed sites. In the other management regimes, the trait groups were affected similarly, except of some specific traits. Longevity, palatability, clonality and biome origin did not explain differences in pooled effect sizes, but tended to explain differences in some specific traits. Overall, general selection patterns were rare probably due to a high heterogeneity of among and within species responses, which might level each other out. Moreover, the number of data points per group of interest is often low and thus, for a final conclusion more studies are needed. Nonetheless, the divergent plant reactions indicate that selection pressures within paired management regimes might be large enough to induce microevolutionary changes in grasslands. Subsequently, the increased variation within species under different management techniques might buffer species persistence in the long term.
... For example, Arabidopsis thaliana displays patterns of phenotypic clinal variation 162 . However, clines are generally stronger in randomly mating species with large population sizes, in which selection is expected to be more efficient 101,163 . The analysis of phenotypic clinal variation due to selection can be, as a first step, a fruitful approach to uncover local adaptations and their genetic underpinnings. ...
Article
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It is increasingly important to improve our understanding of the genetic basis of local adaptation because of its relevance to climate change, crop and animal production, and conservation of genetic resources. Phenotypic patterns that are generated by spatially varying selection have long been observed, and both genetic mapping and field experiments provided initial insights into the genetic architecture of adaptive traits. Genomic tools are now allowing genome-wide studies, and recent theoretical advances can help to design research strategies that combine genomics and field experiments to examine the genetics of local adaptation. These advances are also allowing research in non-model species, the adaptation patterns of which may differ from those of traditional model species.
... Many tree species survived these sudden climate changes and persisted for tens of thousands of years in relatively restricted refugia, indicating a considerable capacity to cope with strong selective pressures (Bennett et al. 1991;Svenning et al. 2008;Shafer et al. 2011). The successful post-glacial migration of many tree species out of these refugia has been suggested to be largely driven by standing adaptive genetic variation (Petit & Hampe 2006;Barrett & Schluter 2008;Temunović et al. 2013), likely maintained by efficient gene flow from refugial populations (Savolainen 2011;Kremer et al. 2012;Hendry 2013). Considering that these past processes gave rise to extant patterns of climatic adaptation, the current distribution of adaptive over neutral genetic differentiation may lend highly valuable insights in the processes governing the adaptive potential of extant tree ...
Article
The adaptive potential of tree species to cope with climate change has important ecological and economic implications. Many temperate tree species experience a wide range of environmental conditions, suggesting high adaptability to new environmental conditions. We investigated adaptation to regional climate in the drought-sensitive tree species Alnus glutinosa (Black alder), using a complementary approach that integrates genomic, phenotypic and landscape data. A total of 24 European populations were studied in a common garden and through landscape genomic approaches. Genotyping-By-Sequencing was used to identify SNPs across the genome, resulting in 1990 SNPs. Although a relatively low percentage of putative adaptive SNPs was detected (2.86% outlier SNPs), we observed clear associations among outlier allele frequencies, temperature, and plant traits. In line with the typical drought avoiding nature of A. glutinosa, leaf size varied according to a temperature gradient and significant associations with multiple outlier loci were observed, corroborating the ecological relevance of the observed outlier SNPs. Moreover, the lack of isolation-by-distance, the very low genetic differentiation among populations and the high intra-population genetic variation all support the notion that high gene exchange combined with strong environmental selection promotes adaptation to environmental cues. This article is protected by copyright. All rights reserved.
... Third, unlike annual plants, the seeds of forest trees often colonize new sites substantial distances from their parent populations, thus exposing them to greater environmental selective pressures. Furthermore, current methods may not efficiently detect selection based on polygenic traits (Pavlidis et al. 2012a), which are involved in much climatic adaptation (Howe et al. 2003;Savolainen 2011;Savolainen et al. 2011;Alberto et al. 2013;Yoder et al. 2014), and selection may have often acted on standing variation instead of new mutations. It should be more difficult to detect effects of selection in such cases (Hermisson & Pennings 2005;Savolainen et al. 2013). ...
Article
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Climate is one of the most important drivers for adaptive evolution in forest trees. Climatic selection contributes greatly to local adaptation and intraspecific differentiation, but this kind of selection could also have promoted interspecific divergence through ecological speciation. To test this hypothesis, we examined intra- and inter-specific genetic variation at 25 climate-related candidate genes and 12 reference loci in two closely related pine species, Pinus massoniana Lamb. and Pinus hwangshanensis Hisa, using population genetic and landscape genetic approaches. These two species occur in Southeast China but have contrasting ecological preferences in terms of several environmental variables, notably altitude, although hybrids form where their distributions overlap. One or more robust tests detected signals of recent and/or ancient selection at two thirds (17) of the 25 candidate genes, at varying evolutionary timescales, but only three of the 12 reference loci. The signals of recent selection were species specific, but signals of ancient selection were mostly shared by the two species likely because of the shared evolutionary history. FST outlier analysis identified six SNPs in five climate-related candidate genes under divergent selection between the two species. In addition, a total of 24 candidate SNPs representing nine candidate genes showed significant correlation with altitudinal divergence in the two species based on the covariance matrix of population history derived from reference SNPs. Genetic differentiation between these two species was higher at the candidate genes than at the reference loci. Moreover, analysis using the Isolation with Migration model indicated that gene flow between the species has been more restricted for climate-related candidate genes than the reference loci, in both directions. Taken together, our results suggest that species-specific and divergent climatic selection at the candidate genes might have counteracted interspecific gene flow and played a key role in the ecological divergence of these two closely related pine species. This article is protected by copyright. All rights reserved.
... Understanding plant phenotypic plasticity to the changing environment will be key to predicting and managing climate change effects on crops (Nicotra et al. 2010). Genome-wide analysis (GWA) 5 in the model plant species Arabidopsis thaliana 6 led to identifying genomic sites related to climatic adaptation (Savolainen 2011 An interdisciplinary perspective (which includes ecology, evolution, genetics, genomics, physiology and molecular biology, among others) will assist in further deepening the knowledge about plant phenotypic plasticity in a changing climate. Nicotra et al. (2010) list leaf mass per unit area, stomata size and density, height at maturity, flowering time plus size at maturity and phenology, and seed size and number among the key functional traits for investigating plant phenotypic plasticity to climate change. ...
... The considerable variation for temperature responses observed in MAGIC accessions corresponds to the adaptation to specific temperature conditions. Though many plant populations are locally adapted to native environmental conditions, the genetic basis of their adaptation is not well known (Savolainen, 2011). There are several ways of how this could be investigated. ...
Thesis
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Temperature is one of the most important abiotic environmental regulators of plant growth and development. The temperature-dependent elongation of the Arabidopsis thaliana hypocotyls (seedling stems) is a well-characterised environmental response. The aim of this study was to identify allelic variants underlying Quantitative Trait Loci (QTL) responsible for the natural genetic variation of hypocotyl length in response to ambient temperatures. The Arabidopsis thaliana accessions were phenotyped for hypocotyl length at 12°C, 17°C, 22°C and 27°C ambient temperature environments and substantial genetic variation was established. This facilitated a forward genetic approach by performing a QTL analysis to identify the genetic basis of thermal sensitivity. Firstly, fine-mapped QTL were identified for hypocotyl length in response to different temperatures. SMALL AUXIN UPREGULATED RNA 38 (SAUR38) is a novel candidate gene for a QTL. Another major-effect QTL ‘Temp22.2’ was also identified which harbours the candidate gene PHYTOCHROME B (PHYB). Secondly, fine-mapped ‘Environmental QTL’ were also discovered for the genotype by environment (G x E) interaction. PHYTOCHROME D (PHYD) is a candidate for a temperature-responsiveness QTL. For QTL cloning, functional characterisation of SAUR38 and PHYB was carried out by knockout analysis and transgenic allelic complementation. The results showed that SAUR38 controlled natural variation in the Tsu-0 accession by increasing elongation. The PHYB alleles of Ct-1, Sf-2 and Col-0 accessions explain the Temp22.2 QTL. Ct-1 and Sf-2 alleles are positive regulators increasing elongation, whereas Col-0 allele is a negative regulator. Temp22.2 QTL was cloned and novel alleles were discovered revealing the molecular basis of quantitative variation in hypocotyl length in response to temperature.
... Even if the processes causing the spatial genetic structuring in tree populations are well documented in temperate zones, tropical rainforests suffer from a lack of knowledge about the process of populations evolution and the genetic structuring of tree populations at intra-specific level (at a level of genetic differentiation more recent than the divergence between species), Savolainen et al. 2007. Many studies have already provided evidence of genetic differentiation in temperate plant populations caused by both neutral and adaptive processes involving a large variety of environmental gradients and subjacent ecological factors such as climatic factors (temperature, precipitation), edaphic factors (soil properties among which soil water availability, nutrients), and biotic interactions (competition, predation, mutualism etc…), Caisse & Antonovics 1978, Savolainen et al. 2007, Leimu & Fischer 2008, Siol et al. 2008, Savolainen et al. 2011, Strasburg et al. 2011. In the tropical rainforest of Amazonia, many studies have already addressed the question of neutral differentiation caused by restricted gene flow and local inbreeding (Ward et al. 2005, Hardy et al. 2006, Dick et al. 2008), but no study has yet integrated both neutral and adaptive aspects of populations evolution at intra-specific level in Amazonia. ...
Thesis
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In the tropical rainforest of Amazonia, the factors driving the evolution of tree species remain poorly understood, and the relative influence of neutral and adaptive processes is continuously debated. In particular, local habitat patchiness draws much attention, as profound changes in the structure and composition of forest communities occur among micro-habitats. Thus, micro-environmental variations related to topography have frequently been invoked as drivers of adaptive radiation leading to sympatric speciation in Neotropical trees. On one hand, the hypothesis of local adaptation has never been investigated at the intra-specific level, i.e. within species currently undergoing population differentiation; on the other hand, many tree species are genetically structured over local scales due to neutral processes, mainly limited gene flow (caused by restricted pollen and seed dispersal). In this study, I used populations of a common tree species of the Guiana Shield - Eperua falcata (Fabaceae) - to study how neutral and adaptive processes shape the distribution of genetic diversity across forest landscapes characterized by local micro-habitat patchiness. I asked three main questions by combining both phenotypic (quantitative genetics) and molecular (population genetics) approaches: 1) How is the genetic diversity structured in forest landscapes of French Guiana? 2) Which evolutionary drivers are relevant to explain the structure of genetic diversity at local scale? 3) Does local adaptation contribute to structure genetic diversity within continuous populations?
... To test the possibility that the observed differences in variation of reversion rates are due to a latitudinal cline of the sampling locations, we used Pearson analysis but found no significant correlation between reversion and latitude or between flowering time and latitude (data not shown). Several studies in the past have shown that flowering time in A. thaliana is correlated with latitude [35,36], however the latitudinal cline in our study was considerably smaller (59-65°) compared to that in similar studies in A. thaliana where flowering time increased with latitude from 40-65° [36][37][38]. ...
Article
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Angiosperm flowers are usually determinate structures that may produce seeds. In some species, flowers can revert from committed flower development back to an earlier developmental phase in a process called floral reversion. The allopolyploid Arabidopsis suecica displays photoperiod-dependent floral reversion in a subset of its flowers, yet little is known about the environmental conditions enhancing this phenotype, or the morphological processes leading to reversion. We have used light and electron microscopy to further describe this phenomenon. Additionally, we have further studied the phenology of flowering and floral reversion in A. suecica. In this study we confirm and expand upon our previous findings that floral reversion in the allopolyploid A. suecica is photoperiod-dependent, and show that its frequency is correlated with the timing for the onset of flowering. Our results also suggest that floral reversion in A. suecica displays natural variation in its penetrance between geographic populations of A. suecica.
... This statement is particularly important for the ability to withstand one to multi-year extreme events, which are already testing our forest species, leading to forest dieback in many regions around the globe (Allen et al., 2010;Choat et al., 2012). It was previously suggested that a rapid climate change requires fast adaptation which relies on existing natural variability rather than on selection of new mutations (Savolainen, 2011). The above considerations have led forestry organizations to consider in situ selection of forest trees based on their ability to withstand drought and thrive in environments whose aridity matches that predicted for coming generations (Joyce and Rehfeldt, 2013). ...
Article
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Climate change is increasing mean temperatures and in the eastern Mediterranean is expected to decrease annual precipitation. The resulting increase in aridity may be too rapid for adaptation of tree species unless their gene pool already possesses variation in drought resistance. Vulnerability to embolism, estimated by the pressure inducing 50% loss of xylem hydraulic conductivity (P50), is strongly associated with drought stress resistance in trees. Yet, previous studies on various tree species reported low intraspecific genetic variation for this trait, and therefore limited adaptive capacities to increasing aridity. Here we quantified differences in hydraulic efficiency (xylem hydraulic conductance) and safety (resistance to embolism) in four contrasting provenances of Pinus halepensis (Aleppo pine) in a provenance trial, which is indirect evidence for genetic differences. Results obtained with three techniques (bench dehydration, centrifugation and X-ray micro-CT) evidenced significant differentiation with similar ranking between provenances. Inter-provenance variation in P50 correlated with pit anatomical properties (torus overlap and pit aperture size). These results suggest that adaptation of P. halepensis to xeric habitats has been accompanied by modifications of bordered pit function driven by variation in pit aperture. This study thus provides evidence that appropriate exploitation of provenance differences will allow continued forestry with P. halepensis in future climates of the Eastern Mediterranean.
... In this study, to understand local diff erences in varieties of T. distichum , we sequenced 47 nuclear loci of 96 individuals, including those of the two varieties, using targeted amplicon sequencing (TAS) with an NGS approach ( Bybee et al., 2011 ). Th e objectives of this study were (1) to estimate the levels of genetic diff erentiation among the three regions (MRAV, Texas, and Florida) and between the two varieties (bald cypress and pond cypress) using our newly collected samples from bald cypress populations in Texas and samples of bald cypress and pond cypress populations in the MRAV and Florida from previous studies; (2) to identify candidate loci for local (habitat) adaptation showing higher levels of diff erentiation between varieties or geographical regions than the other loci; and (3) to infer the demographic history of the regional populations and varieties. We estimated demographical parameters (current and ancestral population sizes, migration rates and divergence time) assuming the "isolation with migration model" ( Nielsen and Wakeley, 2001 ) and estimated these parameters while paying attention to divergence times between geographical regions and between the varieties. ...
Article
Premise of the study: Studies of natural genetic variation can elucidate the genetic basis of phenotypic variation and the past population structure of species. Our study species, Taxodium distichum, is a unique conifer that inhabits the flood plains and swamps of North America. Morphological and ecological differences in two varieties, T. distichum var. distichum (bald cypress) and T. distichum var. imbricarium (pond cypress), are well known, but little is known about the level of genetic differentiation between the varieties and the demographic history of local populations. Methods: We analyzed nucleotide polymorphisms at 47 nuclear loci from 96 individuals collected from the Mississippi River Alluvial Valley (MRAV), and Gulf Coastal populations in Texas, Louisiana, and Florida using high-throughput DNA sequencing. Standard population genetic statistics were calculated, and demographic parameters were estimated using a composite-likelihood approach. Key results: Taxodium distichum in North America can be divided into at least three genetic groups, bald cypress in the MRAV and Texas, bald cypress in Florida, and pond cypress in Florida. The levels of genetic differentiation among the groups were low but significant. Several loci showed the signatures of positive selection, which might be responsible for local adaptation or varietal differentiation. Conclusions: Bald cypress was genetically differentiated into two geographical groups, and the boundary was located between the MRAV and Florida. This differentiation could be explained by population expansion from east to west. Despite the overlap of the two varieties' ranges, they were genetically differentiated in Florida. The estimated demographic parameters suggested that pond cypress split from bald cypress during the late Miocene.
... In nature, these species can inhabit latitudinal and altitudinal clines that span considerable temperature ranges [1]. Individuals from species with broad ecological amplitudes exhibit local adaptation when divergent selection is strong relative to the rate of gene flow [2,3]. Locally adapted individuals show higher fitness in their focal environment relative to immigrants. ...
Article
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Background Many fungal species occur across a variety of habitats. Particularly lichens, fungi forming symbioses with photosynthetic partners, have evolved remarkable tolerances for environmental extremes. Despite their ecological importance and ubiquity, little is known about the genetic basis of adaption in lichen populations. Here we studied patterns of genome-wide differentiation in the lichen-forming fungus Lasallia pustulata along an altitudinal gradient in the Mediterranean region. We resequenced six populations as pools and identified highly differentiated genomic regions. We then detected gene-environment correlations while controlling for shared population history and pooled sequencing bias, and performed ecophysiological experiments to assess fitness differences of individuals from different environments. Results We detected two strongly differentiated genetic clusters linked to Mediterranean and temperate-oceanic climate, and an admixture zone, which coincided with the transition between the two bioclimates. High altitude individuals showed ecophysiological adaptations to wetter and more shaded conditions. Highly differentiated genome regions contained a number of genes associated with stress response, local environmental adaptation, and sexual reproduction. Conclusions Taken together our results provide evidence for a complex interplay between demographic history and spatially varying selection acting on a number of key biological processes, suggesting a scenario of ecological speciation. Electronic supplementary material The online version of this article (doi:10.1186/s12862-017-0929-8) contains supplementary material, which is available to authorized users.
... Landscape genomic approaches associate genomic variation rather than phenotypes from common garden experiments with environmental gradients (Savolainen, 2011;Sork et al., 2013). The gradient forest (GF) model is one method for establishing such an association. ...
Article
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Seed and breeding zones are traditionally delineated based on local adaptation of phenotypic traits associated with climate variables, an approach requiring long‐term field experiments. In this study, we applied a landscape genomics approach to delineate seed and breeding zones for lodgepole pine. We used gradient forest (GF) model to select environment‐associated single nucleotide polymorphisms (SNPs) using three SNP datasets (full, neutral and candidate) and 20 climate variables for 1906 lodgepole pine (Pinus contorta) individuals in British Columbia and Alberta, Canada. The two GF models built with the full (28,954) and candidate (982) SNPs were compared. The GF models identified winter‐related climate as major climatic factors driving genomic patterns of lodgepole pine’s local adaptation. Based on the genomic gradients predicted by the full and candidate GF models, lodgepole pine distribution range in British Columbia and Alberta was delineated into six seed and breeding zones. Our approach is a novel and effective alternative to traditional common‐garden approaches for delineating seed and breeding zone and could be applied to tree species lacking data from provenance trials or common garden experiments.
... Such a correlation provides a meaningful model for the investigation of thermal adaptation on all levels(Hereford, Hansen, & Houle, 2004). As our natural populations have been acclimatized to laboratory conditions for at most up to three generations, the differential response to thermal regimes in the experiments was most likely due to heritable differences among the natural populations, thus providing the necessary evidence to investigate the genomic footprint of this adaptation(Savolainen, 2011). 4.2 | Population genetic simulations underestimate neutral divergence in C. riparius Different evolutionary forces, that is selection, genetic drift, gene flow and mutation, simultaneously shape the evolution of populations(Savolainen et al., 2013). ...
Article
The gradual heterogeneity of climatic factors poses varying selection pressures across geographic distances that leave signatures of clinal variation in the genome. Separating signatures of clinal adaptation from signatures of other evolutionary forces, such as demographic processes, genetic drift, and adaptation to non-clinal conditions of the immediate local environment is a major challenge. Here, we examine climate adaptation in five natural populations of the harlequin fly Chironomus riparius sampled along a climatic gradient across Europe. Our study integrates experimental data, individual genome resequencing, Pool-Seq data, and population genetic modelling. Common-garden experiments revealed significantly different population growth rates at test temperatures corresponding to the population origin along the climate gradient, suggesting thermal adaptation on the phenotypic level. Based on a population genomic analysis, we derived empirical estimates of historical demography and migration. We used an FST outlier approach to infer positive selection across the climate gradient, in combination with an environmental association analysis. In total we identified 162 candidate genes as genomic basis of climate adaptation. Enriched functions among these candidate genes involved the apoptotic process and molecular response to heat, as well as functions identified in other studies of climate adaptation in other insects. Our results show that local climate conditions impose strong selection pressures and lead to genomic adaptation despite strong gene flow. Moreover, these results imply that selection to different climatic conditions seems to converge on a functional level, at least between different insect species.
... Adaptive genomics aims to understand the molecular basis of local adaptation in species experiencing a wide range of environmental gradients. This emerging research field may help predicting how a species will respond to future environmental changes [1] as well as delineating sustainable management units [2][3][4]. This important area of research has taken advantage of the arrival of next generation sequencing (NGS) with reduced sequencing costs, allowing thousands of markers, both potentially neutral and adaptive, to be sequenced in hundreds of individuals [5]. ...
Article
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Background: Adaptive genomics may help predicting how a species will respond to future environmental changes. Genomic signatures of local adaptation in marine organisms are often driven by environmental selective agents impacting the physiology of organisms. With one of the highest salinity level, the Mediterranean Sea provides an excellent model to investigate adaptive genomic divergence underlying salinity adaptation. In the present study, we combined six genome scan methods to detect potential genomic signal of selection in the striped red mullet (Mullus surmuletus) populations distributed across a wide salinity gradient. We then blasted these outlier sequences on published fish genomic resources in order to identify relevant potential candidate genes for salinity adaptation in this species. Results: Altogether, the six genome scan methods found 173 outliers out of 1153 SNPs. Using a blast approach, we discovered four candidate SNPs belonging to three genes potentially implicated in adaptation of M. surmuletus to salinity. The allele frequency at one of these SNPs significantly increases with salinity independently from the effect of longitude. The gene associated to this SNP, SOCS2, encodes for an inhibitor of cytokine and has previously been shown to be expressed under osmotic pressure in other marine organisms. Additionally, our results showed that genome scan methods not correcting for spatial structure can still be an efficient strategy to detect potential footprints of selection, when the spatial and environmental variation are confounded, and then, correcting for spatial structure in a second step represents a conservative method. Conclusion: The present outcomes bring evidences of potential genomic footprint of selection, which suggest an adaptive response of M. surmuletus to salinity conditions in the Mediterranean Sea. Additional genomic data such as sequencing of a full-genome and transcriptome analyses of gene expression would provide new insights regarding the possibility that some striped red mullet populations are locally adapted to their saline environment.
... Lastly, most plants have a wide range of variation in traits associated with fitness and are locally adapted to the environment in which they are found (Savolainen 2011). Though some variation in traits can be associated with genetic drift and gene flow, much of the trait variability is the product of natural selection from spatially varying environmental factors on traits beneficial to a specific environment, suggesting that the variation will differ across the species range (Sork 2018). ...
Chapter
Biogeography is a multifaceted field that integrates geography, geology, ecology, and biology to investigate both historical and ecological questions of how spatial and temporal patterns of varying environmental factors impact the distribution of species and their evolutionary history. Genomes contain imprints of these impacts and, when such genomic imprints are rightly deciphered and interpreted, can help us address these questions. In the past 10 years, incredible advances have been made with respect to acquiring and deciphering genome sequences. The advances in genomics and bioinformatics and the decreasing costs of nucleotide sequencing have reduced many of the barriers to using genomics in biogeography. Here, we introduce some of the strategies and approaches from population genomics that can be integrated into biogeography research. First, we introduce the field of biogeography and define the two well-established broad subdisciplines of ecological and historical biogeography along with the traditional methods that they use. Next, we present examples of how population genomics approaches can be used to address biogeographic questions. To illustrate how both ecological and historical biogeography can benefit from adopting a population genomics approach, we outline our own research on mountain hemlock as a case study. We also briefly discuss the application of biogeography in biological conservation. We conclude the chapter by discussing some of the remaining challenges and future research avenues that become possible by integrating population genomics into biogeography research.
... Recently, several biologists have raised concerns about whether tree species with their long lifespan and adaptation to local environments will be able to survive rapid climate change (Aitken, Yeaman, Holliday, Wang, & Curtis-McLane, 2008;Rellstab et al., 2016;Sork et al., 2013). Thus, it is important to manage both plantations and natural populations with knowledge of the genetic basis of tree performance and how that variation is distributed in the natural landscape (Christmas, Breed, & Lowe, 2015;Savolainen, 2011;Sork et al., 2013). ...
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Local adaptation is a critical evolutionary process that allows plants to grow better in their local compared to nonnative habitat and results in species‐wide geographic patterns of adaptive genetic variation. For forest tree species with a long generation time, this spatial genetic heterogeneity can shape the ability of trees to respond to rapid climate change. Here, we identify genomic variation that may confer local environmental adaptations and then predict the extent of adaptive mismatch under future climate as a tool for forest restoration or management of the widely distributed high‐elevation oak species Quercus rugosa in Mexico. Using genotyping‐by‐sequencing, we identified 5354 single‐nucleotide polymorphisms (SNPs) genotyped from 103 individuals across 17 sites in the Trans‐Mexican Volcanic Belt, and, after controlling for neutral genetic structure, we detected 74 FST‐outlier SNPs and 97 SNPs associated with climate variation. Then, we deployed a nonlinear multivariate model, Gradient Forest (GF), to map turnover in allele frequencies along environmental gradients and predict areas most sensitive to climate change. We found that spatial patterns of genetic variation were most strongly associated with precipitation seasonality and geographical distance. We identified regions of contemporary genetic and climatic similarities, and predicted regions where future populations of Q. rugosa might be at risk due to high expected rate of climate change. Our findings provide preliminary details for future management strategies of Q. rugosa in Mexico and also illustrate how a landscape genomic approach can provide a useful tool for conservation and resource management strategies. This article is protected by copyright. All rights reserved.
... Long-lived tree species with large population size are typically locally adapted to different conditions within highly heterogeneous environments (Savolainen, 2011). Recent advances in ecological genomics of nonmodel species have started to unravel the molecular genetic basis for local adaptation in tree species (Sork et al., 2013). ...
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Long‐lived tree species are genetically differentiated and locally adapted with respect to fitness‐related traits, but the genetic basis of local adaptation remains largely unresolved. Recent advances in population genetics and landscape genomic analyses enable identification of putative adaptive loci and specific selective pressures acting on local adaptation. Here we sampled 60 evergreen oak (Quercus aquifolioides) populations throughout the species’ range and pool‐sequenced 587 individuals at drought stress candidate genes. We analyzed patterns of genetic diversity and differentiation for 381 single nucleotide polymorphisms (SNPs) from 65 candidate genes and eight microsatellites. Outlier loci were identified by genetic differentiation analysis and genome–environment associations. The response pattern of genetic variation to environmental gradient was assessed by linear isolation by distance/environment tests, redundancy analysis and non‐linear methods. SNPs and microsatellites revealed two genetic lineages: Tibet and Hengduan Mountains‐Western Sichuan Plateau (HDM‐WSP), with reduced genetic diversity in Tibet lineage. More outlier loci were detected in HDM‐WSP lineage than Tibet lineage. Among these, three SNPs in two genes responded to dry season precipitation in the HDM‐WSP lineage but not in Tibet. By contrast, genetic variation in the Tibet lineage was related to geographic distance instead of the environment. Furthermore, Risk of Non‐Adaptedness (RONA) analyses suggested HDM‐WSP lineage will have a better capacity to adapt in the predicted future climate compared to the Tibet lineage. We detected genetic imprints consistent with natural selection and molecular adaptation to drought on the Qinghai‐Tibet Plateau (QTP) over a range of long‐lived and widely distributed oak species in a changing environment. Our results suggest that different within‐species adaptation processes occur in species occurring in heterogeneous environments.
... Even if the processes causing the spatial genetic structuring in tree populations are well documented in temperate zones, tropical rainforests suffer from a lack of knowledge about the process of populations evolution and the genetic structuring of tree populations at intra-specific level (at a level of genetic differentiation more recent than the divergence between species), Savolainen et al. 2007. Many studies have already provided evidence of genetic differentiation in temperate plant populations caused by both neutral and adaptive processes involving a large variety of environmental gradients and subjacent ecological factors such as climatic factors (temperature, precipitation), edaphic factors (soil properties among which soil water availability, nutrients), and biotic interactions (competition, predation, mutualism etc…), Caisse & Antonovics 1978, Savolainen et al. 2007, Leimu & Fischer 2008, Siol et al. 2008, Savolainen et al. 2011, Strasburg et al. 2011. In the tropical rainforest of Amazonia, many studies have already addressed the question of neutral differentiation caused by restricted gene flow and local inbreeding (Ward et al. 2005, Hardy et al. 2006, Dick et al. 2008), but no study has yet integrated both neutral and adaptive aspects of populations evolution at intra-specific level in Amazonia. ...
Thesis
In the tropical rainforest of Amazonia, the factors driving the evolution of tree species remain poorly understood, and the relative influence of neutral and adaptive processes is continuously debated. In particular, local habitat patchiness draws much attention, as profound changes in the structure and composition of forest communities occur among micro-habitats. Thus, micro-environmental variations related to topography have frequently been invoked as drivers of adaptive radiation leading to sympatric speciation in Neotropical trees. On one hand, the hypothesis of local adaptation has never been investigated at the intra-specific level, i.e. within species currently undergoing population differentiation; on the other hand, many tree species are genetically structured over local scales due to neutral processes, mainly limited gene flow (caused by restricted pollen and seed dispersal). In this study, I used populations of a common tree species of the Guiana Shield - Eperua falcata (Fabaceae) - to study how neutral and adaptive processes shape the distribution of genetic diversity across forest landscapes characterized by local micro-habitat patchiness. I asked three main questions by combining both phenotypic (quantitative genetics) and molecular (population genetics) approaches: 1) How is the genetic diversity structured in forest landscapes of French Guiana? 2) Which evolutionary drivers are relevant to explain the structure of genetic diversity at local scale? 3) Does local adaptation contribute to structure genetic diversity within continuous populations?
... Such a correlation provides a meaningful model for the investigation of thermal adaptation on all levels (Hereford et al. 2004). Since our natural populations have been acclimatised to laboratory conditions for at most up to three generations, the differential response to thermal regimes in the experiments was most likely due to heritable differences among the natural populations, thus providing the necessary evidence to investigate the genomic footprint of this adaptation (Savolainen 2011). ...
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The gradual heterogeneity of climatic factors pose varying selection pressures across geographic distances that leave signatures of clinal variation in the genome. Separating signatures of clinal adaptation from signatures of other evolutionary forces, such as demographic processes, genetic drift, and adaptation to non-clinal conditions of the immediate local environment is a major challenge. Here, we examine climate adaptation in five natural populations of the harlequin fly Chironomus riparius sampled along a climatic gradient across Europe. Our study integrates experimental data, individual genome resequencing, Pool-Seq data, and population genetic modelling. Common-garden experiments revealed a positive correlation of population growth rates corresponding to the population origin along the climate gradient, suggesting thermal adaptation on the phenotypic level. Based on a population genomic analysis, we derived empirical estimates of historical demography and migration. We used an F ST outlier approach to infer positive selection across the climate gradient, in combination with an environmental association analysis. In total we identified 162 candidate genes as genomic basis of climate adaptation. Enriched functions among these candidate genes involved the apoptotic process and molecular response to heat, as well as functions identified in other studies of climate adaptation in other insects. Our results show that local climate conditions impose strong selection pressures and lead to genomic adaptation despite strong gene flow. Moreover, these results imply that selection to different climatic conditions seems to converge on a functional level, at least between different insect species.
... The Asian cultivated rice is an economically important crop and is extremely diverse, with a large number of landraces that are cultivated in different ecogeographical regions. These varieties contain vital genetic variants that are important for their adaptation to their local environment (including soil fertility), which provides valuable genetic resource for breeding [7][8][9] . Although several genetic variants that confer NUE variation have previously been identified in rice [10][11][12] , the genetic basis of NUE in a more diverse and inclusive population remains largely unexplored. ...
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The intensive application of inorganic nitrogen underlies marked increases in crop production, but imposes detrimental effects on ecosystems1,2: it is therefore crucial for future sustainable agriculture to improve the nitrogen-use efficiency of crop plants. Here we report the genetic basis of nitrogen-use efficiency associated with adaptation to local soils in rice (Oryza sativa L.). Using a panel of diverse rice germplasm collected from different ecogeographical regions, we performed a genome-wide association study on the tillering response to nitrogen—the trait that is most closely correlated with nitrogen-use efficiency in rice—and identified OsTCP19 as a modulator of this tillering response through its transcriptional response to nitrogen and its targeting to the tiller-promoting gene DWARF AND LOW-TILLERING (DLT)3,4. A 29-bp insertion and/or deletion in the OsTCP19 promoter confers a differential transcriptional response and variation in the tillering response to nitrogen among rice varieties. The allele of OsTCP19 associated with a high tillering response to nitrogen is prevalent in wild rice populations, but has largely been lost in modern cultivars: this loss correlates with increased local soil nitrogen content, which suggests that it might have contributed to geographical adaptation in rice. Introgression of the allele associated with a high tillering response into modern rice cultivars boosts grain yield and nitrogen-use efficiency under low or moderate levels of nitrogen, which demonstrates substantial potential for rice breeding and the amelioration of negative environment effects by reducing the application of nitrogen to crops. OsTCP19 is a modulator of the tillering response to nitrogen in rice, and introgression of an allele of OsTCP19 associated with a high tillering response into modern rice cultivars markedly improves their nitrogen-use efficiency.
Chapter
Inbred lines are nearly homozygous due to long inbreeding by forced self-pollination or sib-mating. These inbred lines can be used in genetic research (e.g., mapping genes and quantitative trait loci), allele discovery, and directly as cultivars in selfing species or as parents of hybrids and synthetic cultivars. Microsatellites and single-nucleotide polymorphisms are today among the most widely used DNA marker systems, while new generation sequencing starts providing access to more DNA landmarks for plant breeding. DNA markers allow us selecting genes directly or indirectly rather than solely based on phenotypes, and may reduce the time for assembling favorable alleles in doubled haploids (DHs), near-isogenic lines, or recombinant-inbred lines. DHs along with DNA marker-aided breeding offer a shortcut for backcrossing because they are fertile and homozygous at all loci in a single step. Model species such as Arabidopsis thaliana provides genetic resources to find genomic sites related to climatic adaptation, whose genetic basis remains mostly unknown. Plant breeding for local adaptation seems to be best in stressful environments where stable genotypes derived from broad-based germplasm can be selected. Local adaptation by various genetic mechanisms will also facilitate a flexible response to the changing climate. Decentralized and end-user participatory plant breeding provides further means to ensure impacts, particularly for low-input agriculture and farming systems in marginal environments.
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Local adaptation arises as a result of selection by the local environment favoring phenotypes that enhance fitness. Geographic patterns of phenotypic variation are in part due to this selective process. Classically, the genetic basis of those phenotypes has been studied in plant populations using a quantitative genetic approach in which plants from different source populations are grown in common environments, in reciprocal transplant experiments, or in studies across a wide geographic and environmentally heterogeneous area. Limitations of these approaches to understanding the genetic basis of phenotypic variation can now be addressed with next generation sequencing, gene expression profiles, and epigenetic analysis. In this paper, I summarize contemporary genomic research on local adaptation by comparing findings from the Arabidopsis annual plant model system with long-lived tree species in four kinds of local adaptation studies: (i) genomic studies of transplant experiments; (ii) landscape genomic studies; (iii) gene expression studies; (iv) epigenetic studies of local adaptation. Although the basic study designs of common garden, reciprocal transplants, and geographic variation have remained constant, the inclusion of contemporary genomic approaches has provided substantive advances in our understanding of the genetic underpinnings of local adaptation, including the impact of climate, the identification of candidate genes involved in genotype by environment interactions, and evidence for the potential role of epigenetic modification. Despite these advances, new questions are arising and key areas for future research include more exploration of gene networks in response to biotic and abiotic stressors and improved statistical tools for traits with polygenic inheritance.
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Environmental heterogeneity is one of the main actors of biodiversity and species adaptation as it exerts a selective pressure on observable characteristics of living organisms. Consequently, local adaptation favours certain genetic variants and, by doing so, leaves a footprint in the genetic heritage across populations. The identification of these adaptive genetic variations is the main objective of landscape genomics and allows, among other things, to study the role of specific regions of the genome in evolutionary processes. Landscape genomics studies also provide essential information for species conservation and for the prediction of migrations due to environmental changes. To identify these adaptations to the environment, it is necessary to define a study area where the populations are sampled. However, defining the scale of the study area is not a trivial task. In fact, whether the work is carried out at a local or at a broad scale determines the relevance of environmental factors and the type of signature of selection that will be observed. In addition, the concept of scale in ecology takes into account not only the extent of the study area but also the pattern and density of the geographic distribution of observations, and the spatial resolution of predictors (environmental variables), which is intrinsically linked to the extent. However, a priori indications about the relevance of any resolution over another are rare in the literature and it is therefore essential to question this issue. In this thesis, we propose a multi-scale landscape genomic framework to identify signatures of adaptation to the environment. This multidisciplinary framework lies at the interface between geographic information systems, spatial analysis, environmental modelling, population genetics and computer science. Specifically, we focus on the relevance of variables derived from Digital Elevation Models (DEMs) and on the application of multi-scale analysis aiming to detect signatures of selection. We applied this analytical framework to three case studies, comprising four species: Biscutella laevigata sampled at a local scale, Plantago major at a regional scale, sheep and goats at a large scale. In particular, the case of B. laevigata allowed us to evaluate the role of topographic features based on Very High Resolution DEMs and to include DEM-derived variables as predictors in association models to study the adaptation of species to their local environment. On the other hand, the case of Moroccan sheep and goats permitted to include for the first time whole genome sequence data within landscape genomic models. The results revealed several important findings. We showed that micro-climate variability is highly dependent on topographic factors at a local scale and that therefore, DEMs are relevant for understanding species adaptation to a mountainous environment. We also demonstrated that it is essential to consider the scale of spatial representativeness by assessing DEM-derived variables at various spatial resolutions. Indeed, two out of three case studies showed that the models involving topographic variables were sensitive to changes in resolution. In summary, we used several landscape genetics approaches to understand the role of environmental factors in the local adaptation of various species. Our findings mainly provide an important contribution to the understanding and use of scale in landscape genomics, also useful in landscape ecology.
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Unlabelled: • Premise of study: Understanding the relationship between climate, adaptation, and population structure is of fundamental importance to botanists because these factors are crucial for the evolution of biodiversity and the response of species to future climate change. Panicum hallii is an emerging model system for perennial grass and bioenergy research, yet very little is known about the relationship between climate and population structure in this system. • Methods: We analyzed geographic population differentiation across 39 populations of P. hallii along a longitudinal transect from the savannas of central Texas through the deserts of Arizona and New Mexico. A combination of morphological and genetic (microsatellite) analysis was used to explore patterns of population structure. • Key results: We found strong differentiation between high elevation western desert populations and lower elevation eastern populations of P. hallii, with a pronounced break in structure occurring in western Texas. In addition, we confirmed that there are high levels of morphological and genetic structure between previous recognized varieties (var. hallii and var. filipes) within this species. • Conclusions: The results of this study suggest that patterns of population structure within P. hallii may be driven by climatic variation over space. Overall, this study lays the groundwork for future studies on the genetics of local adaptation and reproductive isolation in this system.
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Arabidopsis thaliana is now a model system, not just for plant biology but also for comparative genomics. The completion of the sequences of two closely related species, Arabidopsis lyrata and Brassica rapa, is complemented by genomic comparisons among A. thaliana accessions and mutation accumulation lines. Together these genomic data document the birth of new genes via gene duplication, transposon exaptation and de novo formation of new genes from noncoding sequence. Most novel loci exhibit low expression, and are undergoing pseudogenization or subfunctionalization. Comparatively, A. thaliana has lost large amounts of sequence through deletion, particularly of transposable elements. Intraspecific genomic variation indicates high rates of deletion mutations and deletion polymorphisms across accessions, shedding light on the history of Arabidopsis genome architecture.
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Local adaptation is critical for species persistence in the face of rapid environmental change, but its genetic basis is not well understood. Growing the model plant Arabidopsis thaliana in field experiments in four sites across the species’ native range, we identified candidate loci for local adaptation from a genome-wide association study of lifetime fitness in geographically diverse accessions. Fitness-associated loci exhibited both geographic and climatic signatures of local adaptation. Relative to genomic controls, high-fitness alleles were generally distributed closer to the site where they increased fitness, occupying specific and distinct climate spaces. Independent loci with different molecular functions contributed most strongly to fitness variation in each site. Independent local adaptation by distinct genetic mechanisms may facilitate a flexible evolutionary response to changing environment across a species range.
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Understanding the genetic bases and modes of adaptation to current climatic conditions is essential to accurately predict responses to future environmental change. We conducted a genome-wide scan to identify climate-adaptive genetic loci and pathways in the plant Arabidopsis thaliana. Amino acid–changing variants were significantly enriched among the loci strongly correlated with climate, suggesting that our scan effectively detects adaptive alleles. Moreover, from our results, we successfully predicted relative fitness among a set of geographically diverse A. thaliana accessions when grown together in a common environment. Our results provide a set of candidates for dissecting the molecular bases of climate adaptations, as well as insights about the prevalence of selective sweeps, which has implications for predicting the rate of adaptation.
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Author Summary Classical studies that examined the global distributions of human physiological traits such as pigmentation, basal metabolic rate, and body shape and size suggested that natural selection related to climate has been important during recent human evolutionary history. We scanned the human genome using data for about 650,000 variants in 61 worldwide populations to look for correlations between allele frequencies and 9 climate variables and found evidence for adaptations to climate at the genome-wide level. In addition, we detected compelling signals for individual SNPs involved in pigmentation and immune response, as well as for pathways related to UV radiation, infection and immunity, and cancer. A particularly appealing aspect of this approach is that we identify a set of candidate advantageous SNPs associated with specific biological hypotheses, which will be useful for follow-up testing. We developed an online resource to browse the results of our data analyses, allowing researchers to quickly assess evidence for selection in a particular genomic region and to compare it across several studies.
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In Drosophila, multiple lines of evidence converge in suggesting that beneficial substitutions to the genome may be common. All suffer from confounding factors, however, such that the interpretation of the evidence-in particular, conclusions about the rate and strength of beneficial substitutions-remains tentative. Here, we use genome-wide polymorphism data in D. simulans and sequenced genomes of its close relatives to construct a readily interpretable characterization of the effects of positive selection: the shape of average neutral diversity around amino acid substitutions. As expected under recurrent selective sweeps, we find a trough in diversity levels around amino acid but not around synonymous substitutions, a distinctive pattern that is not expected under alternative models. This characterization is richer than previous approaches, which relied on limited summaries of the data (e.g., the slope of a scatter plot), and relates to underlying selection parameters in a straightforward way, allowing us to make more reliable inferences about the prevalence and strength of adaptation. Specifically, we develop a coalescent-based model for the shape of the entire curve and use it to infer adaptive parameters by maximum likelihood. Our inference suggests that ∼13% of amino acid substitutions cause selective sweeps. Interestingly, it reveals two classes of beneficial fixations: a minority (approximately 3%) that appears to have had large selective effects and accounts for most of the reduction in diversity, and the remaining 10%, which seem to have had very weak selective effects. These estimates therefore help to reconcile the apparent conflict among previously published estimates of the strength of selection. More generally, our findings provide unequivocal evidence for strongly beneficial substitutions in Drosophila and illustrate how the rapidly accumulating genome-wide data can be leveraged to address enduring questions about the genetic basis of adaptation.
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Efforts to identify the genetic basis of human adaptations from polymorphism data have sought footprints of "classic selective sweeps" (in which a beneficial mutation arises and rapidly fixes in the population).Yet it remains unknown whether this form of natural selection was common in our evolution. We examined the evidence for classic sweeps in resequencing data from 179 human genomes. As expected under a recurrent-sweep model, we found that diversity levels decrease near exons and conserved noncoding regions. In contrast to expectation, however, the trough in diversity around human-specific amino acid substitutions is no more pronounced than around synonymous substitutions. Moreover, relative to the genome background, amino acid and putative regulatory sites are not significantly enriched in alleles that are highly differentiated between populations. These findings indicate that classic sweeps were not a dominant mode of human adaptation over the past ~250,000 years.
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Natural populations of forest trees exhibit striking phenotypic adaptations to diverse environmental gradients, thereby making them appealing subjects for the study of genes underlying ecologically relevant phenotypes. Here, we use a genome-wide data set of single nucleotide polymorphisms genotyped across 3059 functional genes to study patterns of population structure and identify loci associated with aridity across the natural range of loblolly pine (Pinus taeda L.). Overall patterns of population structure, as inferred using principal components and Bayesian cluster analyses, were consistent with three genetic clusters likely resulting from expansions out of Pleistocene refugia located in Mexico and Florida. A novel application of association analysis, which removes the confounding effects of shared ancestry on correlations between genetic and environmental variation, identified five loci correlated with aridity. These loci were primarily involved with abiotic stress response to temperature and drought. A unique set of 24 loci was identified as F(ST) outliers on the basis of the genetic clusters identified previously and after accounting for expansions out of Pleistocene refugia. These loci were involved with a diversity of physiological processes. Identification of nonoverlapping sets of loci highlights the fundamental differences implicit in the use of either method and suggests a pluralistic, yet complementary, approach to the identification of genes underlying ecologically relevant phenotypes.
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Although pioneered by human geneticists as a potential solution to the challenging problem of finding the genetic basis of common human diseases, genome-wide association (GWA) studies have, owing to advances in genotyping and sequencing technology, become an obvious general approach for studying the genetics of natural variation and traits of agricultural importance. They are particularly useful when inbred lines are available, because once these lines have been genotyped they can be phenotyped multiple times, making it possible (as well as extremely cost effective) to study many different traits in many different environments, while replicating the phenotypic measurements to reduce environmental noise. Here we demonstrate the power of this approach by carrying out a GWA study of 107 phenotypes in Arabidopsis thaliana, a widely distributed, predominantly self-fertilizing model plant known to harbour considerable genetic variation for many adaptively important traits. Our results are dramatically different from those of human GWA studies, in that we identify many common alleles of major effect, but they are also, in many cases, harder to interpret because confounding by complex genetics and population structure make it difficult to distinguish true associations from false. However, a-priori candidates are significantly over-represented among these associations as well, making many of them excellent candidates for follow-up experiments. Our study demonstrates the feasibility of GWA studies in A. thaliana and suggests that the approach will be appropriate for many other organisms.
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Many plants flower in response to seasonal changes in daylength. This response often varies between accessions of a single species. We studied the variation in photoperiod response found in the model species Arabidopsis (Arabidopsis thaliana). Seventy-two accessions were grown under six daylengths varying in 2-h intervals from 6 to 16 h. The typical response was sigmoidal, so that plants flowered early under days longer than 14 h, late under days shorter than 10 h, and at intermediate times under 12-h days. However, many accessions diverged from this pattern and were clustered into groups showing related phenotypes. Thirty-one mutants and transgenic lines were also scored under the same conditions. Statistical comparisons demonstrated that some accessions show stronger responses to different daylengths than are found among the mutants. Genetic analysis of two such accessions demonstrated that different quantitative trait loci conferred an enhanced response to shortening the daylength from 16 to 14 h. Our data illustrate the spectrum of daylength response phenotypes present in accessions of Arabidopsis and demonstrate that similar phenotypic variation in photoperiodic response can be conferred by different combinations of loci.
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Like many species, the model plant Arabidopsis thaliana exhibits multiple different life histories in natural environments. We grew mutants impaired in different signaling pathways in field experiments across the species' native European range in order to dissect the mechanisms underlying this variation. Unexpectedly, mutational loss at loci implicated in the cold requirement for flowering had little effect on life history except in late-summer cohorts. A genetically informed photothermal model of progression toward flowering explained most of the observed variation and predicted an abrupt transition from autumn flowering to spring flowering in late-summer germinants. Environmental signals control the timing of this transition, creating a critical window of acute sensitivity to genetic and climatic change that may be common for seasonally regulated life history traits.
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Local adaptation is of fundamental importance in evolutionary, population, conservation, and global-change biology. The generality of local adaptation in plants and whether and how it is influenced by specific species, population and habitat characteristics have, however, not been quantitatively reviewed. Therefore, we examined published data on the outcomes of reciprocal transplant experiments using two approaches. We conducted a meta-analysis to compare the performance of local and foreign plants at all transplant sites. In addition, we analysed frequencies of pairs of plant origin to examine whether local plants perform better than foreign plants at both compared transplant sites. In both approaches, we also examined the effects of population size, and of the habitat and species characteristics that are predicted to affect local adaptation. We show that, overall, local plants performed significantly better than foreign plants at their site of origin: this was found to be the case in 71.0% of the studied sites. However, local plants performed better than foreign plants at both sites of a pair-wise comparison (strict definition of local adaption) only in 45.3% of the 1032 compared population pairs. Furthermore, we found local adaptation much more common for large plant populations (>1000 flowering individuals) than for small populations (<1000 flowering individuals) for which local adaptation was very rare. The degree of local adaptation was independent of plant life history, spatial or temporal habitat heterogeneity, and geographic scale. Our results suggest that local adaptation is less common in plant populations than generally assumed. Moreover, our findings reinforce the fundamental importance of population size for evolutionary theory. The clear role of population size for the ability to evolve local adaptation raises considerable doubt on the ability of small plant populations to cope with changing environments.
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We model selection at a locus affecting a quantitative trait (QTL) in the presence of genetic variance due to other loci. The dynamics at the QTL are related to the initial genotypic value and to the background genetic variance of the trait, assuming that background genetic values are normally distributed, under three different forms of selection on the trait. Approximate dynamics are derived under the assumption of small mutation effect. For similar strengths of selection on the trait (i.e, gradient of directional selection beta) the way background variation affects the dynamics at the QTL critically depends on the shape of the fitness function. It generally causes the strength of selection on the QTL to decrease with time. The resulting neutral heterozygosity pattern resembles that of a selective sweep with a constant selection coefficient corresponding to the early conditions. The signature of selection may also be blurred by mutation and recombination in the later part of the sweep. We also study the race between the QTL and its genetic background toward a new optimum and find the conditions for a complete sweep. Overall, our results suggest that phenotypic traits exhibiting clear-cut molecular signatures of selection may represent a biased subset of all adaptive traits.
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FRIGIDA (FRI) is a major gene involved in the regulation of flowering time in Arabidopsis thaliana. Nucleotide variation at this gene was investigated by sequencing 25 field ecotypes collected from western Europe. Genetic diversity at FRI was characterized by a high number of haplotypes and an excess of low-frequency polymorphisms. A large excess of intraspecific nonsynonymous variation associated with low synonymous variation was detected along the first exon in the FRI gene. In contrast, no excess of nonsynonymous divergence was detected between A. thaliana and A. lyrata. The Tajima and McDonald and Kreitman tests, however, suggested that this gene has evolved in a nonneutral fashion. Nonsynonymous variation included eight loss-of-function mutations that have probably arisen recently and independently in several locations. A phenotypic evaluation of the sequenced ecotypes confirmed that these loss-of-function mutations were associated with an early-flowering phenotype. Taken together, our results suggest that DNA polymorphism at the FRI gene in A. thaliana from western Europe has been shaped by recent positive selection for earliness in a set of isolated populations.
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Populations are locally adapted when populations have the highest relative fitness at their home sites, and lower fitness in other parts of the range. Results from the extensive experimental plantations of populations of forest trees from different parts of the range show that populations can survive and grow in broad areas outside the home site. However, intra- and interspecific competition limit the distribution of genotypes. For populations from large parts of the range, relative fitness, compared with the local population, is often highest at the home site. At the edges of the range, this local adaptation may break down. The extent of local adaptation is determined by the balance between gene flow and selection. Genetic differentiation and strong natural selection occur over a range of tens or hundreds of kilometers, but reliable measurements of gene flow are available only for much shorter distances. Current models of spatially varying selection could be made more realistic by the incorporation of st...
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Plants provide unique opportunities to study the mechanistic basis and evolutionary processes of adaptation to diverse environmental conditions. Complementary laboratory and field experiments are important for testing hypotheses reflecting long-term ecological and evolutionary history. For example, these approaches can infer whether local adaptation results from genetic tradeoffs (antagonistic pleiotropy), where native alleles are best adapted to local conditions, or if local adaptation is caused by conditional neutrality at many loci, where alleles show fitness differences in one environment, but not in a contrasting environment. Ecological genetics in natural populations of perennial or outcrossing plants can also differ substantially from model systems. In this review of the evolutionary genetics of plant adaptation, we emphasize the importance of field studies for understanding the evolutionary dynamics of model and nonmodel systems, highlight a key life history trait (flowering time) and discuss emerging conservation issues.
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Selection for local adaptation results in genetic differentiation in ecologically important traits. In a perennial, outcrossing model plant Arabidopsis lyrata, several differentiated phenotypic traits contribute to local adaptation, as demonstrated by fitness advantage of the local population at each site in reciprocal transplant experiments. Here we compared fitness components, hierarchical total fitness and differentiation in putatively ecologically important traits of plants from two diverged parental populations from different continents in the native climate conditions of the populations in Norway and in North Carolina (NC, U.S.A.). Survival and number of fruits per inflorescence indicated local advantage at both sites and aster life-history models provided additional evidence for local adaptation also at the level of hierarchical total fitness. Populations were also differentiated in flowering start date and floral display. We also included reciprocal experimental F(1) and F(2) hybrids to examine the genetic basis of adaptation. Surprisingly, the F(2) hybrids showed heterosis at the study site in Norway, likely because of a combination of beneficial dominance effects from different traits. At the NC site, hybrid fitness was mostly intermediate relative to the parental populations. Local cytoplasmic origin was associated with higher fitness, indicating that cytoplasmic genomes also may contribute to the evolution of local adaptation.
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