Evidence for extensive parallelism but divergent genomic architecture of adaptation along altitudinal and latitudinal gradients in Populus trichocarpa

Abstract

SummaryAdaptation to climate across latitude and altitude reflects shared climatic constraints, which may lead to parallel adaptation. However, theory predicts that higher gene flow should favor more concentrated genomic architectures, which would lead to fewer locally maladapted recombinants.We used exome capture to resequence the gene space along a latitudinal and two altitudinal transects in the model tree Populus trichocapra. Adaptive trait phenotyping was coupled with F ST outlier tests and sliding window analysis to assess the degree of parallel adaptation as well as the genomic distribution of outlier loci.Up to 51% of outlier loci overlapped between transect pairs and up to 15% of these loci overlapped among all three transects. Genomic clustering of adaptive loci was more pronounced for altitudinal than latitudinal transects. In both altitudinal transects, there was a larger number of these 'islands of divergence', which were on average longer and included several of exceptional physical length.Our results suggest that recapitulation of genetic clines over latitude and altitude involves extensive parallelism, but that steep altitudinal clines generate islands of divergence. This suggests that physical proximity of genes in coadapted complexes may buffer against the movement of maladapted alleles from geographically proximal but climatically distinct populations.

Trait differentiation and adaptation of plants along elevation gradients

“…Holliday et al . () compared signatures of selection in populations of Populus trichocarpa in two mountain ranges in British Columbia and found evidence for convergent evolution in 23% of the SNPs under selection in loci generally involved in developmental and light‐mediated processes.…”

Population genomics of the eastern cottonwood (Populus deltoides)

“…A better understanding of the genetic regulation of adaptation is fundamental for the development of adequate management and conservation strategies under a changing climate (Porth et al., 2015). In recent years, population genomics has been used to study tree populations, identifying genes under selection involved in local adaptation (Evans et al., 2014; Geraldes et al., 2014; Holliday et al., 2016; Zhou et al., 2014). The great advantage of population genomics studies over smaller‐scale population genetics studies is that the former allow identifying and correcting for genomewide demographic effects, increasing the power to detect locus‐specific effects (Stinchcombe & Hoekstra, 2008).…”

“…The Populus trichocarpa genome, the first tree to be sequenced (Tuskan et al., 2006), created numerous opportunities for pioneering genomic studies in tree species. Several genomewide association, transcriptome, and population genomics studies have been reported for P. trichocarpa , contributing to the current knowledge about the species regulation of complex traits (McKown, Klápště, et al., 2014; Porth et al., 2013a, 2013b), extent of linkage disequilibrium (LD) and effective population size (Slavov et al., 2012; Zhou, Bawa, & Holliday, 2014), population structure (Geraldes et al., 2014; Slavov et al., 2012; Zhou et al., 2014), genetic diversity (Evans et al., 2014; Zhou et al., 2014), demographic history (Zhou et al., 2014), adaptation (Evans et al., 2014; Geraldes et al., 2014; Holliday, Zhou, Bawa, Zhang, & Oubida, 2016; Porth et al., 2015; Zhou et al., 2014), and sex determination (Geraldes et al., 2015). Studies in other poplar species (Stölting et al., 2013, 2015; Wang, Street, Scofield, & Ingvarsson, 2016a, 2016b) have significantly lagged behind.…”

“…Genetic structure is mainly driven by interspecific hybridization, isolation by distance, and natural selection (Evans et al., 2014; Geraldes et al., 2014; Slavov et al., 2012; Stölting et al., 2015; Wang et al., 2016b; Zhou et al., 2014). Adaptation has been shown to have a complex genetic architecture (Evans et al., 2014; Holliday et al., 2016; McKown, Guy, et al., 2014; McKown, Klápště, et al., 2014; Porth et al., 2015) and to be a driver of divergent evolution between species (Wang et al., 2016b). Contradictory estimates of LD decay have been reported for P. trichocarpa , with an early study on a reduced number of genes reporting fast LD decay below a threshold of 0.2 (200 bp, Wegrzyn et al., 2010).…”

Adaptive genomic divergence under high gene flow between freshwater and brackish‐water ecotypes of prickly sculpin (Cottus asper) revealed by Pool‐Seq

“…; Holliday et al . ), it becomes increasingly important to identify the targets of selection (‘candidate genes’) that can be functionally linked to ecological variables that likely affect the fitness of individuals. A promising approach is to focus on a priori determined candidate genes or gene families that are suspected to underlie important ecotypic traits, as has been demonstrated by Smadja et al .…”