Imprints of Natural Selection Along Environmental Gradients in Phenology-Related Genes ofQuercus petraea

Abstract

We explored single nucleotide polymorphism (SNP) variation in candidate genes for bud burst from Quercus petraea populations sampled along gradients of latitude and altitude in Western Europe. SNP diversity was monitored for 106 candidate genes, in 758 individuals from 32 natural populations. We investigated whether SNP variation reflected the clinal pattern of bud burst observed in common garden experiments. We used different methods to detect imprints of natural selection (F ST outlier, clinal variation at allelic frequencies, association tests) and compared the results obtained for the two gradients. F ST outlier SNPs were found in 15 genes, 5 of which were common to both gradients. The type of selection differed between the two gradients (directional or balancing) for 3 of these 5. Clinal variations were observed for six SNPs, and one cline was conserved across both gradients. Association tests between the phenotypic or breeding values of trees and SNP genotypes identified 14 significant associations, involving 12 genes. The results of outlier detection on the basis of population differentiation or clinal variation were not very consistent with the results of association tests. The discrepancies between these approaches may reflect the different hierarchical levels of selection considered (inter-and intrapopulation selection). Finally, we obtained evidence for convergent selection (similar for gradients) and clinal variation for a few genes, suggesting that comparisons between parallel gradients could be used to screen for major candidate genes responding to natural selection in trees.L OCAL adaptation of temperate forest trees to environmental variation has been widely investigated in common garden experiments or provenance tests (Langlet 1971;Matyas 1996; König 2005 for reviews). Comparisons of populations sampled over wide ranges have revealed continuous patterns of differentiation along environmental gradients (Wright 1976;Morgenstern 1996). Clinal variation along geographic gradients (latitude, altitude, longitude) is frequently reported for phenological traits (see Alberto et al. 2013 for a review). Congruent clines have been identified across species and across experiments within species, suggesting the occurrence of directional selection in response to identical environmental gradients. For example, in northern temperate spruces and pines, populations from northern latitudes flush earlier than southern populations (Wright 1976;Morgenstern 1996) and steep clines have been observed in species extending over large ranges of latitude (Pinus sylvestris in Scandinavia, Giertych 1991; Picea sitchensis in North America, Mimura and Aitken 2007). Bud burst clines have also been observed in northern temperate broadleaved trees, but following the opposite trend. In beech (von Wuehlisch et al. 1995), birch (Worrell et al. 2000), and sessile oak (Liepe 1993;Deans and Harvey 1995;Ducousso et al. 1996), southern populations flush earlier than northern populations. Similar clinal variation has also been repo...

The population genomic signature of environmental selection in the widespread insect-pollinated tree species Frangula alnus at different geographical scales

“…However, the detection of the same outliers at different geographical scales, together with the association of most of our outliers with ecologically relevant functions and environmental variables, supports selective divergence of the corresponding loci (Limborg et al, 2012; Population and landscape genomics in F. alnus H De Kort et al Buehler et al, 2012;Alberto et al, 2013;Steane et al, 2014). Overall, these findings also render it unlikely that our outlier SNPs represent sequence assembling errors, which can be introduced during the de novo sequence assembly preceding SNP discovery in non-model organisms (Da Silva et al, 2014).…”

“…alnus (Table 2), this finding denotes locus a107 as a candidate target for natural selection induced by drought. Although the occurrence of the same outliers at different spatial scales may reflect excellent candidates for further research, selective loci may be different at different spatial scales because of variable selection pressures across scales, or because of correlations among loci underlying the same phenotypic trait (Nosil et al, 2009;Alberto et al, 2013). We therefore cannot exclude the potential adaptive value of outliers that do not appear consistently across all scales.…”

“…More specifically, a standard Bayesian population genomic outlier screen (BAYESCAN, Foll & Gaggiotti, 2008) was complemented with individual-based latent factor mixed modeling (LFMM, Frichot et al, 2013), and multivariate redundancy analyses (RDA, Borcard et al, 2011), to identify (i) SNPs putatively under selection and (ii) the main environmental drivers of population differentiation while accounting for spatial autocorrelation in allele frequencies. Although the use of candidate SNPs has been the standard method to find loci putatively under selection (for example, Namroud et al, 2008;Alberto et al, 2013;Guichoux et al, 2013;Olson et al, 2013), they may compromise the relevance of classical outlier detection methods due to overestimation of neutral distributions. This stresses the importance of integrating landscape genomic methods to reliably reveal loci putatively under selection and the selective agents underlying the observed patterns (De Villemereuil et al, 2014;Weinig et al, 2014).…”

Footprints of divergent selection in natural populations of Castanopsis fargesii (Fagaceae)

“…Identifying genes that are under selection in natural populations of tree species will facilitate our understanding of how these populations are adapted to their environment and responded to future climatic changes (Bradbury et al, 2013). Evidence for selection at the molecular genetic level has been demonstrated in some important tree species such as spruce (Namroud et al, 2008), pine (Eveno et al, 2008), oak (Alberto et al, 2013) and Eucalyptus (Bradbury et al, 2013).…”

Ecological and association genetics in two Mediterranean pine species

“…For example, in Arabidopsis thaliana, a model annual selfing plant, new advantageous mutations associated with fitness and local climate occur in such mosaics, together with more common and widely distributed favorable variants (Hancock et al 2011). On the other hand, evidence suggests that in widespread outcrossing species with long generation times, such as forest trees, local adaptations mostly develop from alleles already present in the gene pools (i.e., from standing genetic variation), which often results in the establishment of gene clines along environmental gradients Eckert et al 2010a;Prunier et al 2012;Alberto et al 2013b). Compared to well-studied selfing annuals, forest trees have to face highly variable selection pressures that result from environmental changes over long periods of time.…”