Microgeographic adaptation and the effect of pollen flow on the adaptive potential of a temperate tree species

Recent interest for microgeographic adaptation, i.e. adaptation at spatial scales compatible with substantial amount of gene dispersal, offers to reconsider the scale at which evolution occurs (Richardson et al. 2014). Whether gene flow is constraining or facilitating local adaptation at this fine spatial scale remains an unresolved question. Too important gene flow would overwhelm the effects of natural selection and decrease local adaptation along environmental gradients. Conversely, gene flow, and particularly long-distance dispersal events, could play a major role in resupplying the genetic variation of populations and favouring the spread of beneficial alleles (Kremer et al. 2012). Hence, the high dispersal capacities of trees are often assumed to be the main process maintaining the large levels of genetic variation measured in their natural populations. However, evidences for microgeographic adaptation and the quantitative assessment of the impact of gene flow on adaptive genetic variation are still limited in most temperate trees. Here, we sampled 60 open-pollinated families of European beech (Fagus sylvatica L.) from three natural plots, spreading along a short elevation gradient (∼1.5 km) at the warm margin of this species distribution. We analysed the phenotypic and genotypic data of ∼2,300 seedlings grown in a common garden. We focused on 11 potentially adaptive traits with significant heritabilities (Gauzere et al. 2016) and tested for signature of local selection on quantitative trait differentiation. We then identified the offspring likely originating from local or distant pollen immigration events and quantified the role of gene flow in increasing locally the additive variance of traits under selection. We found a significant signal of adaptive differentiation among plots separated by less than one kilometre, with local selection acting on growth and phenological traits. We found that trees in the plots at high elevation, experiencing the lowest temperature conditions, flushed earlier and had a higher height and diameter growth in our common garden than trees from the plot at low elevation. Beech populations originating from higher longitude or elevation have also been shown to be genetically earlier in provenance tests, suggesting that these populations evolved phenological traits promoting a longer vegetation period. At this southern margin of the species, the reduced allocation to stem growth at the low elevation plot is likely an adaptive response to drought, which has previously been described by comparing marginal vs central beech populations. Consistently with theoretical expectations, our results suggest a beneficial effect of pollen dispersal by increasing the genetic diversity for these locally differentiated traits. These effects were quantitatively high, with more than twice higher genetic variance for immigrant than local offspring, although with large standard errors around estimates. Our results highlight that local selection is an important evolutionary force in natural tree populations, and provide a strong evidence that adaptive genetic differentiation can occur despite high gene flow. For the two genetically differentiated traits, our analyses suggested a beneficial effect of pollen dispersal by increasing genetic diversity after one episode of reproduction. The findings suggest that conservation and management interventions to facilitate movement of gametes along short ecological gradients would boost genetic diversity of individual tree populations, and thereby enhance their adaptive potential

Detecting short spatial scale local adaptation and epistatic selection in climate-related candidate genes in European beech (Fagus sylvatica) populations

Detecting signatures of selection in tree populations threatened by climate change is currently a major research priority. Here, we investigated the signature of local adaptation over a short spatial scale using 96 European beech (Fagus sylvatica L.) individuals originating from two pairs of populations on the northern and southern slopes of Mont Ventoux (south-eastern France). We performed both single and multi-locus analysis of selection based on 53 climate-related candidate genes containing 546 SNPs. FST outlier methods at the SNP level revealed a weak signal of selection, with three marginally significant outliers in the northern populations. At the gene-level, considering haplotypes as alleles, two additional marginally significant outliers were detected, one on each slope. To account for the uncertainty of haplotype inference, we averaged the Bayes Factors over many possible phase reconstructions. Epistatic selection offers a realistic multi-locus model of selection in natural populations. Here, we used a test suggested by Ohta based on the decomposition of the variance of linkage disequilibrium. Over all populations, 0.23% of the SNP pairs (haplotypes) showed evidence of epistatic selection, with nearly 80% of them being within genes. One of the between gene epistatic selection signals arose between an FST outlier and a non-synonymous mutation in a drought response gene. Additionally, we identified haplotypes containing selectively advantageous allele combinations which were unique to high or low-elevations and northern or southern populations. Several haplotypes contained non-synonymous mutations situated in genes with known functional importance for adaptation to climatic factor

Looking for local adaptation:Convergent microevolution in aleppo pine (pinus halepensis)

Finding outlier loci underlying local adaptation is challenging and is best approached by suitable sampling design and rigorous method selection. In this study, we aimed to detect outlier loci (single nucleotide polymorphisms, SNPs) at the local scale by using Aleppo pine (Pinus halepensis), a drought resistant conifer that has colonized many habitats in the Mediterranean Basin, as the model species. We used a nested sampling approach that considered replicated altitudinal gradients for three contrasting sites. We genotyped samples at 294 SNPs located in genomic regions selected to maximize outlier detection. We then applied three different statistical methodologies-Two Bayesian outlier methods and one latent factor principal component method-To identify outlier loci. No SNP was an outlier for all three methods, while eight SNPs were detected by at least two methods and 17 were detected only by one method. From the intersection of outlier SNPs, only one presented an allelic frequency pattern associated with the elevational gradient across the three sites. In a context of multiple populations under similar selective pressures, our results underline the need for careful examination of outliers detected in genomic scans before considering them as candidates for convergent adaptation

Comprendre la réponse adaptative de populations d’arbres aux variations climatiques : modélisation des processus éco-évolutifs à des échelles locales

Understanding how and how fast populations adapt to their environment is a major issue of evolutionary ecology, which is currently gaining a renewed interest in the context of climate change (CC). Phenotypic variation in life history traits, through which adaptation acts, results both from genetic variation between individuals and environmental variation in space or time. Forest trees are generally considered to have good adaptation abilities, because of their high levels of genetic diversity, their large population sizes, the strong gene flow between populations, and the high plasticity of their adaptive traits. However, the rhythm of observed and predicted CC, much higher than that of past climatic oscillations, raises the issue of how fast tree populations can respond. On these topics, the originality of my research relies on estimating "real time" eco-evolutionary processes contributing to adaptation, using an inter-disciplinary approach, and combining experimental and modeling approaches. I first developed innovative methods based on genetic markers to characterize plant mating system and gene flow by pollen and seed across a generation, and reveal their sensitivity to various environmental and anthropogenic factors in different populations of trees. I also used these methods in combination with quantitative genetic and ecophysiology approaches to measure the available genetic variability and the selection due to the abiotic environment on functional traits involved in climate response in beech populations along an altitudinal gradient. The significant adaptive potential of beech populations highlighted by this approach is corroborated by other experimental approaches, which reveal a small but significant adaptive genetic differentiation between populations separated by ~ 1km, both in terms of functional traits and candidate genes involved in these traits. Finally, I develop mechanistic simulation models to integrate eco-physiological, demographic and genetic processes, understand their effects and interactions, and predict future dynamics of trees population in response to CCPrédire le rythme et comprendre les mécanismes de l’adaptation des populations à leur environnement est une question majeure de l’écologie évolutive, qui connait actuellement un regain d’intérêt dans le contexte du changement climatique (CC) et global. La variation phénotypique des traits d’histoire de vie, à travers laquelle se manifeste l’adaptation, résulte à la fois de la variation génétique entre individus et de la variation environnementale dans l’espace ou dans le temps. Les arbres forestiers sont généralement considérés comme dotés de bonnes capacités d’adaptation, de par leurs hauts niveaux de diversité génétique, leurs grandes tailles de population, les forts flux de gènes entre populations, et la plasticité importante de leur traits adaptatifs. Cependant, le rythme observé et prédit du CC, bien supérieur à celui des oscillations climatiques passées, soulève la question de la rapidité de la réponse adaptative future des populations d’arbres. Sur cette question, l’originalité de mes travaux de recherche repose sur l’estimation « en temps réel » des processus éco-évolutifs contribuant à l’adaptation, dans une démarche inter-disciplinaire, et par la combinaison d’approches expérimentales et de modélisation. J’ai tout d’abord développé des méthodes innovantes basées sur des marqueurs génétiques pour caractériser le régime de reproduction et les flux de gènes par pollen et par graine à l’échelle d’une génération, et en révéler la sensibilité à différents facteurs écologiques et anthropiques dans différentes populations d’arbres. J’ai aussi utilisé ces méthodes, en association avec des approches de génétique quantitative et d’écophysiologie, pour mesurer la variabilité génétique disponible et la sélection exercée par l’environnement abiotique sur des traits fonctionnels impliqués dans la réponse au climat dans des populations de Hêtre le long de gradient altitudinaux. Le potentiel adaptatif non négligeable des populations de Hêtre ainsi mis en évidence est corroboré par d’autres approches expérimentales, qui révèlent une différenciation génétique adaptative faible mais significative entre populations séparées de ~1km, aussi bien au niveau des traits fonctionnels que des gènes candidats impliqués dans ces traits. Enfin, je développe des modèles de simulation mécanistes pour intégrer les processus écophysiologiques, démographiques et génétiques, comprendre leurs effets et leur interactions, et prédire la dynamique future des populations d’arbres en réponse au C

Simulating local adaptation to climate of forest trees with a physio-demo-genetics model

One challenge of evolutionary ecology is to predict the rate and mechanisms of population adaptation to environmental variations. The variations in most life-history traits are shaped both by individual genotypic and environmental variation. Forest trees exhibit high levels of genetic diversity, large population sizes, and gene flow, and they also show a high level of plasticity for life-history traits. We developed a new Physio-Demo-Genetics model (denoted PDG) coupling (1) a physiological module simulating individual tree responses to the environment; (2) a demographic module simulating tree survival, reproduction and pollen and seed dispersal; and (3) a quantitative genetics module controlling the heritability of key life history traits. We used this model to investigate the plastic and genetic components of the variations of the timing of budburst along an elevational gradient of Fagus sylvatica (the European beech). We used a repeated five years climatic sequence to show that five generations of natural selection were sufficient to develop non-monotonic genetic differentiation in the timing of budburst along the local climatic gradient but also that plastic variation among different elevations and years was higher than genetic variation. PDG complements theoretical models and provides testable predictions to understand the adaptive potential of tree population

Comparing direct vs. indirect estimates of gene flow within a population of a scattered tree species

The comparison between historical estimates of gene flow, using variance in allelic frequencies, and contemporary estimates of gene flow, using parentage assignment, is expected to provide insights into ecological and evolutionary processes at work within and among populations. Genetic variation at six microsatellite loci was used to quantify genetic structure in the insect-pollinated, animal-dispersed, low-density tree Sorbus torminalis L. Crantz, and to derive historical estimates of gene flow. The neighbourhood size and root-mean-squared dispersal distance inferred from seedling genotypes (Nb = 70 individuals, σe = 417 m) were similar to those inferred from adult genotypes (Nb = 114 individuals, σe = 472 m). We also used parentage analyses and a neighbourhood model approach after an evaluation of the statistical properties of this method on simulated data. From our data, we estimated even contributions of seed- and pollen-mediated dispersal to the genetic composition of established seedlings, with both fat-tailed pollen and seed dispersal kernels, and slightly higher mean distance of pollen dispersal (248 m) as compared to seed dispersal (135 m). The resulting contemporary estimate of gene dispersal distance (σc = 211 m) was ~twofold smaller than the historical estimates. Besides different assumptions and st