Understanding adaptive genetic responses to climate change is a main challenge for preserving biological diversity. Successful predictive models for climate-driven range shifts of species depend on the integration of information on adaptation, including that derived from genomic studies. Long-lived forest trees can experience substantial environmental change across generations, which results in a much more prominent adaptation lag than in annual species. Here, we show that candidate-gene SNPs (single nucleotide polymorphisms) can be used as predictors of maladaptation to climate in maritime pine (Pinus pinaster Aiton), an outcrossing long-lived keystone tree. A set of 18 SNPs potentially associated with climate, 5 of them involving amino acid-changing variants, were retained after performing logistic regression, latent factor mixed models, and Bayesian analyses of SNP-climate correlations. These relationships identified temperature as an important adaptive driver in maritime pine and highlighted that selective forces are operating differentially in geographically discrete gene pools. The frequency of the locally advantageous alleles at these selected loci was strongly correlated with survival in a common garden under extreme (hot and dry) climate conditions, which suggests that candidate-gene SNPs can be used to forecast the likely destiny of natural forest ecosystems under climate change scenarios. Differential levels of forest decline are anticipated for distinct maritime pine gene pools. Geographically defined molecular proxies for climate adaptation will thus critically enhance the predictive power of range-shift models and help establish mitigation measures for long-lived keystone forest trees in the face of impending climate change.KEYWORDS climate adaptation; environmental associations; genetic lineages; single nucleotide polymorphisms; fitness estimates P AST and present climate changes are major drivers of species displacements and range-size variation (Hughes 2000;Franks and Hoffmann 2012). Current predictions indicate that the impact of climate change will intensify over the next 20-100 years (Loarie et al. 2009;Bellard et al. 2012), with concomitant phenotypic and genetic effects on wild populations (Gamache and Payette 2004;Franks and Hoffmann 2012;Alberto et al. 2013a). The capability of species to respond to such alterations will rely on phenotypic plasticity, potential for in situ adaptation, and/or migration to more suitable habitats (Aitken et al. 2008). While phenotypic plasticity and migration might be insufficient to cope with these changes (Mclachlan et al. 2005;Malcom et al. 2011;Zhu et al. 2011), successful in situ adaptation will depend on the amount of standing genetic variation and the rate at which new alleles arise, are maintained, and/or get to fixation within populations (Hancock et al. 2011). Thus, our ability to detect present adaptive polymorphisms and to integrate them in predictive models of future maladaptation might be decisive to ensure the persistence of natural p...
Maritime pine provides essential ecosystem services in the south-western Mediterranean basin, where it covers around 4 million ha. Its scattered distribution over a range of environmental conditions makes it an ideal forest tree species for studies of local adaptation and evolutionary responses to climatic change. Highly multiplexed single nucleotide polymorphism (SNP) genotyping arrays are increasingly used to study genetic variation in living organisms and for practical applications in plant and animal breeding and genetic resource conservation. We developed a 9k Illumina Infinium SNP array and genotyped maritime pine trees from (i) a three-generation inbred (F2) pedigree, (ii) the French breeding population and (iii) natural populations from Portugal and the French Atlantic coast. A large proportion of the exploitable SNPs (2052/8410, i.e. 24.4%) segregated in the mapping population and could be mapped, providing the densest ever gene-based linkage map for this species. Based on 5016 SNPs, natural and breeding populations from the French gene pool exhibited similar level of genetic diversity. Population genetics and structure analyses based on 3981 SNP markers common to the Portuguese and French gene pools revealed high levels of differentiation, leading to the identification of a set of highly differentiated SNPs that could be used for seed provenance certification. Finally, we discuss how the validated SNPs could facilitate the identification of ecologically and economically relevant genes in this species, improving our understanding of the demography and selective forces shaping its natural genetic diversity, and providing support for new breeding strategies.
Preserving intraspecific genetic diversity is essential for long-term forest sustainability in a climate change scenario. Despite that, genetic information is largely neglected in conservation planning, and how conservation units should be defined is still heatedly debated. Here, we use maritime pine (Pinus pinaster Ait.), an outcrossing long-lived tree with a highly fragmented distribution in the Mediterranean biodiversity hotspot, to prove the importance of accounting for genetic variation, of both neutral molecular markers and quantitative traits, to define useful conservation units. Six gene pools associated to distinct evolutionary histories were identified within the species using 12 microsatellites and 266 single nucleotide polymorphisms (SNPs). In addition, height and survival standing variation, their genetic control, and plasticity were assessed in a multisite clonal common garden experiment (16 544 trees). We found high levels of quantitative genetic differentiation within previously defined neutral gene pools. Subsequent cluster analysis and post hoc trait distribution comparisons allowed us to define 10 genetically homogeneous population groups with high evolutionary potential. They constitute the minimum number of units to be represented in a maritime pine dynamic conservation program. Our results uphold that the identification of conservation units below the species level should account for key neutral and adaptive components of genetic diversity, especially in species with strong population structure and complex evolutionary histories. The environmental zonation approach currently used by the pan-European genetic conservation strategy for forest trees would be largely improved by gradually integrating molecular and quantitative trait information, as data become available.
27Results from a decade of association studies in different organisms suggest that most complex 28 traits are polygenic, that is, their genetic architectures are determined by numerous causal loci 29 distributed across the genome each with small effect-size. Thus, determining the degree of 30 polygenicity is a central goal to understand the genetic basis of phenotypic variation. 31Recently, multi-loci methods able to detect variants associated with a phenotype of interest 32 despite the subtle allele frequency changes between populations usually observed have been 33 developed. In this study, we applied two multi-loci methods to estimate the degree of 34 polygenicity of fitness-related traits in a long-lived plant species (maritime pine) and to 35 analyze how polygenicity changes across years and environments. For this purpose, we 36 evaluated five categories of fitness related traits, such as, height, survival, phenology-related, 37 biotic-stress resistance and functional traits in a clonal common garden network planted in 38 contrasted environments. Most of the analyzed traits showed evidences of local adaptation. 39We observed a remarkably stable degree of polygenicity (average 6%) across traits, 40 environments and years. Additionally, some of the measured traits showed evidences of 41 negative selection that could explain the observed degree of polygenicity, as previously 42 suggested in humans. The observed genetic architecture of fitness-related traits in maritime 43 pine is in accordance with the polygenic adaptation model. Because polygenic adaptation can 44 take place rapidly, our results can contribute to improve the predictions about the capacity of 45
Heterozygosity-fitness correlations (HFCs) have been used to understand the complex interactions between inbreeding, genetic diversity and evolution. Although frequently reported for decades, evidence for HFCs was often based on underpowered studies or inappropriate methods, and hence their underlying mechanisms are still under debate. Here, we used 6100 genome-wide single nucleotide polymorphisms (SNPs) to test for general and local effect HFCs in maritime pine (Pinus pinaster Ait.), an iconic Mediterranean forest tree. Survival was used as a fitness proxy, and HFCs were assessed at a four-site common garden under contrasting environmental conditions (total of 16 288 trees). We found no significant correlations between genome-wide heterozygosity and fitness at any location, despite variation in inbreeding explaining a substantial proportion of the total variance for survival. However, four SNPs (including two non-synonymous mutations) were involved in significant associations with survival, in particular in the common gardens with higher environmental stress, as shown by a novel heterozygosity-fitness association test at the species-wide level. Fitness effects of SNPs involved in significant HFCs were stable across maritime pine gene pools naturally growing in distinct environments. These results led us to dismiss the general effect hypothesis and suggested a significant role of heterozygosity in specific candidate genes for increasing fitness in maritime pine. Our study highlights the importance of considering the species evolutionary and demographic history and different spatial scales and testing environments when assessing and interpreting HFCs.
A decade of genetic association studies in multiple organisms suggests that most complex traits are polygenic; that is, they have a genetic architecture determined by numerous loci, each with small effect‐size. Thus, determining the degree of polygenicity and its variation across traits, environments and time is crucial to understand the genetic basis of phenotypic variation. We applied multilocus approaches to estimate the degree of polygenicity of fitness‐related traits in a long‐lived plant (Pinus pinaster Ait., maritime pine) and to analyse this variation across environments and years. We evaluated five categories of fitness‐related traits (survival, height, phenology, functional, and biotic‐stress response) in a clonal common‐garden network planted in contrasted environments (over 20,500 trees). Most of the analysed traits showed evidence of local adaptation based on Qst–Fst comparisons. We further observed a remarkably stable degree of polygenicity, averaging 6% (range of 0%–27%), across traits, environments and years. We detected evidence of negative selection, which could explain, at least partially, the high degree of polygenicity. Because polygenic adaptation can occur rapidly, our results suggest that current predictions on the capacity of natural forest tree populations to adapt to new environments should be revised, especially in the current context of climate change.
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SummaryForest ecosystems are increasingly challenged by extreme events, e.g. pest and pathogen outbreaks, causing severe ecological and economical losses. Understanding the genetic basis of adaptive traits in tree species is of key importance to preserve forest ecosystemsAdaptive phenotypes, including susceptibility to two fungal pathogens (Diplodia sapinea and Armillaria ostoyae) and an insect pest (Thaumetopoea pityocampa), height and needle phenology were assessed in a range-wide common garden of maritime pine (Pinus pinaster Aiton), a widespread conifer in the western Mediterranean Basin and parts of the Atlantic coast.Broad-sense heritability was significant for height (0.497), needle phenology (0.231-0.468) and pathogen symptoms (0.413 for D. sapinea and 0.066 for A. ostoyae) measured after inoculation under controlled conditions, but not for pine processionary moth incidence assessed in the common garden. Genetic correlations between traits revealed contrasting trends for pathogen susceptibility to D. sapinea and A. ostoyae. Maritime pine populations from areas with high summer temperatures and frequent droughts were less susceptible to D. sapinea but more susceptible to A. ostoyae. An association study using 4,227 genome-wide SNPs revealed several loci significantly associated to each trait.This study provides important insights to develop genetic conservation and breeding strategies integrating tree responses to pathogens.
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