Data from: Genomic and functional approaches reveal a case of adaptive introgression from Populus balsamifera (balsam poplar) in P. trichocarpa (black cottonwood)

Natural hybrid zones in forest trees provide systems to study the transfer of adaptive genetic variation by introgression. Previous landscape genomic studies in Populus trichocarpa, a keystone tree species, indicated genomic footprints of admixture with its sister species P. balsamifera and identified candidate genes for local adaptation. Here, we explored patterns of introgression and signals of local adaptation in P. trichocarpa and P. balsamifera, employing genome resequencing data from three chromosomes in pure species and admixed individuals from wild populations. Local ancestry analysis in admixed P. trichocarpa revealed a telomeric region in chromosome 15 with P. balsamifera ancestry, containing several candidate genes for local adaptation. Genomic analyses revealed signals of selection in certain genes in this region (e.g. PRR5, COMT1), and functional analyses based on gene expression variation and correlations with adaptive phenotypes suggest distinct functions of the introgressed alleles. In contrast, a block of genes in chromosome 12 paralogous to the introgressed region showed no signs of introgression or signatures of selection. We hypothesize that the introgressed region in chromosome 15 has introduced modular, or cassette-like variation into P. trichocarpa. These linked adaptive mutations are associated with a block of genes in chromosome 15 that appear to have undergone neo- or sub-functionalization relative to paralogs in a duplicated region on chromosome 12 that show no signatures of adaptive variation. The association between P. balsamifera introgressed alleles with the expression of adaptive traits in P. trichocarpa supports the hypothesis that this is a case of adaptive introgression in an ecologically important foundation species.

林木天然杂交带为研究渐渗（introgression）介导的适应性遗传变异传递提供了研究体系。此前针对关键树种毛果杨（Populus trichocarpa）开展的景观基因组学研究，已检测到其与姊妹种香脂杨（Populus balsamifera，下文简称P. balsamifera）的基因混合基因组印记，并鉴定出若干局域适应候选基因。本研究利用野生种群中纯合物种与杂交个体的三条染色体基因组重测序数据，对毛果杨与P. balsamifera的渐渗模式及局域适应信号展开探究。对杂交背景毛果杨的本地祖先成分分析显示，其15号染色体存在一段携带P. balsamifera祖先成分的端粒区域，该区域包含若干局域适应候选基因。基因组分析检测到该区域部分基因（如PRR5、COMT1）存在选择信号；基于基因表达变异及与适应性表型的相关性开展的功能分析表明，渐渗等位基因具有独特功能。与之相反，12号染色体上与该渐渗区域存在旁系同源关系的基因簇，未表现出任何渐渗或选择信号。我们提出假说：15号染色体上的渐渗区域为毛果杨引入了模块化（或称盒式）变异。这些连锁的适应性突变，与15号染色体上的一段基因簇相关；相较于12号染色体重复区域中未表现出适应性变异的旁系同源基因，该基因簇似乎经历了新功能化或亚功能化过程。香脂杨渐渗等位基因与毛果杨适应性性状表达之间的关联，支持了这一假说：即在这一具有重要生态意义的建群物种中存在适应性渐渗现象。