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Signatures of natural selection in a foundation tree along Mediterranean climatic gradients.

ABSTRACT: Temperature and precipitation regimes are rapidly changing, resulting in forest dieback and extinction events, particularly in Mediterranean-type climates (MTC). Forest management that enhance forests' resilience is urgently required, however adaptation to climates in heterogeneous landscapes with multiple selection pressures is complex. For widespread trees in MTC we hypothesized that: patterns of local adaptation are associated with climate; precipitation is a stronger factor of adaptation than temperature; functionally related genes show similar signatures of adaptation; and adaptive variants are independently sorting across the landscape. We sampled 28 populations across the geographic distribution of Eucalyptus marginata (jarrah), in South-west Western Australia, and obtained 13,534 independent single nucleotide polymorphic (SNP) markers across the genome. Three genotype-association analyses that employ different ways of correcting population structure were used to identify putatively adapted SNPs associated with independent climate variables. While overall levels of population differentiation were low (F_ST = 0.04), environmental association analyses found a total of 2336 unique SNPs associated with temperature and precipitation variables, with 1440 SNPs annotated to genic regions. Considerable allelic turnover was identified for SNPs associated with temperature seasonality and mean precipitation of the warmest quarter, suggesting that both temperature and precipitation are important factors in adaptation. SNPs with similar gene functions had analogous allelic turnover along climate gradients, while SNPs among temperature and precipitation variables had uncorrelated patterns of adaptation. These contrasting patterns provide evidence that there may be standing genomic variation adapted to current climate gradients, providing the basis for adaptive management strategies to bolster forest resilience in the future.

SUBMITTER: Filipe JC

PROVIDER: S-EPMC9305101 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Natural ecosystems are under pressure from increasing abiotic and biotic stressors, including climate change and novel pathogens, which are putting species at risk of local extinction, and altering community structure, composition and function. Here, we aim to assess adaptive variation in growth and fungal disease resistance within a foundation tree, Corymbia calophylla to determine local adaptation, trait heritability and genetic constraints in adapting to future environments. Two experimental planting sites were established in regions of contrasting rainfall with seed families from 18 populations capturing a wide range of climate origins (~4,000 individuals at each site). Every individual was measured in 2015 and 2016 for growth (height, basal diameter) and disease resistance to a recently introduced leaf blight pathogen (Quambalaria pitereka). Narrow-sense heritability was estimated along with trait covariation. Trait variation was regressed against climate-of-origin, and multivariate models were used to develop predictive maps of growth and disease resistance. Growth and blight resistance traits differed significantly among populations, and these differences were consistent between experimental sites and sampling years. Growth and blight resistance were heritable, and comparisons between trait differentiation (Q ST) and genetic differentiation (F ST) revealed that population differences in height and blight resistance traits are due to divergent natural selection. Traits were significantly correlated with climate-of-origin, with cool and wet populations showing the highest levels of growth and blight resistance. These results provide evidence that plants have adaptive growth strategies and pathogen defence strategies. Indeed, the presence of standing genetic variation and trait heritability of growth and blight resistance provide capacity to respond to novel, external pressures. The integration of genetic variation into adaptive management strategies, such as assisted gene migration and seed sourcing, may be used to provide greater resilience for natural ecosystems to both biotic and abiotic stressors.

Project description:Background and aimsThe effects of habitat fragmentation on quantitative genetic variation in plant populations are still poorly known. Saxifraga sponhemica is a rare endemic of Central Europe with a disjunct distribution, and a stable and specialized habitat of treeless screes and cliffs. This study therefore used S. sponhemica as a model species to compare quantitative and molecular variation in order to explore (1) the relative importance of drift and selection in shaping the distribution of quantitative genetic variation along climatic gradients; (2) the relationship between plant fitness, quantitative genetic variation, molecular genetic variation and population size; and (3) the relationship between the differentiation of a trait among populations and its evolvability.MethodsGenetic variation within and among 22 populations from the whole distribution area of S. sponhemica was studied using RAPD (random amplified polymorphic DNA) markers, and climatic variables were obtained for each site. Seeds were collected from each population and germinated, and seedlings were transplanted into a common garden for determination of variation in plant traits.Key resultsIn contrast to previous results from rare plant species, strong evidence was found for divergent selection. Most population trait means of S. sponhemica were significantly related to climate gradients, indicating adaptation. Quantitative genetic differentiation increased with geographical distance, even when neutral molecular divergence was controlled for, and QST exceeded FST for some traits. The evolvability of traits was negatively correlated with the degree of differentiation among populations (QST), i.e. traits under strong selection showed little genetic variation within populations. The evolutionary potential of a population was not related to its size, the performance of the population or its neutral genetic diversity. However, performance in the common garden was lower for plants from populations with reduced molecular genetic variation, suggesting inbreeding depression due to genetic erosion.ConclusionsThe findings suggest that studies of molecular and quantitative genetic variation may provide complementary insights important for the conservation of rare species. The strong differentiation of quantitative traits among populations shows that selection can be an important force for structuring variation in evolutionarily important traits even for rare endemic species restricted to very specific habitats.

Project description:Many theoretical models predict when genetic evolution and phenotypic plasticity allow adaptation to changing environmental conditions. These models generally assume stabilizing selection around some optimal phenotype. We however often ignore how optimal phenotypes change with the environment, which limit our understanding of the adaptive value of phenotypic plasticity. Here, we propose an approach based on our knowledge of the causal relationships between climate, adaptive traits, and fitness to further these questions. This approach relies on a sensitivity analysis of the process-based model phenofit, which mathematically formalizes these causal relationships, to predict fitness landscapes and optimal budburst dates along elevation gradients in three major European tree species. Variation in the overall shape of the fitness landscape and resulting directional selection gradients were found to be mainly driven by temperature variation. The optimal budburst date was delayed with elevation, while the range of dates allowing high fitness narrowed and the maximal fitness at the optimum decreased. We also found that the plasticity of the budburst date should allow tracking the spatial variation in the optimal date, but with variable mismatch depending on the species, ranging from negligible mismatch in fir, moderate in beech, to large in oak. Phenotypic plasticity would therefore be more adaptive in fir and beech than in oak. In all species, we predicted stronger directional selection for earlier budburst date at higher elevation. The weak selection on budburst date in fir should result in the evolution of negligible genetic divergence, while beech and oak would evolve counter-gradient variation, where genetic and environmental effects are in opposite directions. Our study suggests that theoretical models should consider how whole fitness landscapes change with the environment. The approach introduced here has the potential to be developed for other traits and species to explore how populations will adapt to climate change.

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Signatures of natural selection in a foundation tree along Mediterranean climatic gradients.

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