Data from: Adaptive evolution and segregating load contribute to the genomic landscape of divergence in two tree species connected by episodic gene flow

Speciation often involves repeated episodes of genetic contact between divergent populations before reproductive isolation (RI) is complete. Whole genome sequencing (WGS) holds great promise for unravelling the genomic bases of speciation. We have studied two ecologically divergent, hybridizing species of the ‘model tree’ genus Populus (poplars, aspens, cottonwoods), Populus alba and P. tremula, using >8.6 million Single Nucleotide Polymorphisms (SNPs) from WGS of population pools. We used the genomic data to (1) scan these species’ genomes for regions of elevated and reduced divergence, (2) assess key aspects of their joint demographic history based on genome-wide site frequency spectra (SFS), (3) infer the potential roles of adaptive and deleterious coding mutations in shaping the genomic landscape of divergence. We identified numerous small, unevenly distributed genome regions without fixed polymorphisms despite high overall genomic differentiation. The joint SFS was best explained by ancient and repeated gene flow and allowed pinpointing candidate interspecific migrant tracts. The direction of selection (DoS) differed between genes in putative migrant tracts and the remainder of the genome, thus indicating the potential roles of adaptive divergence and segregating deleterious mutations on the evolution and breakdown of RI. Genes affected by positive selection during divergence were enriched for several functionally interesting groups, including well known candidate ‘speciation genes’ involved in plant innate immunity. Our results suggest that adaptive divergence affects RI in these hybridizing species mainly through intrinsic and demographic processes. Integrating genomic with molecular data holds great promise for revealing the effects of particular genetic pathways on speciation.

物种形成过程中，生殖隔离（reproductive isolation, RI）完全建立前，分化种群间往往会反复发生遗传接触。全基因组测序（Whole Genome Sequencing, WGS）为解析物种形成的基因组基础提供了重要契机。我们以“模式树木”类群杨属（Populus）的两个生态分化且存在杂交的物种——银白杨（Populus alba）和欧洲山杨（P. tremula）为研究对象，利用基于种群混样全基因组测序得到的超860万个单核苷酸多态性（Single Nucleotide Polymorphisms, SNPs）开展研究。我们依托基因组数据开展了三项分析：（1）扫描两个物种基因组中分化程度升高与降低的区域；（2）基于全基因组位点频率频谱（site frequency spectra, SFS）解析二者联合人口统计学历史的关键特征；（3）推断适应性与有害编码突变在塑造分化基因组景观中的潜在作用。
研究发现，尽管整体基因组分化程度较高，但存在大量小型、分布不均的基因组区域未出现固定多态性。联合位点频率频谱的最优解释模型为古老且反复的基因流，同时可精准定位候选种间基因渐渗片段。推定渐渗片段内的基因与基因组其余区域的选择方向（direction of selection, DoS）存在差异，这表明适应性分化和分离的有害突变可能对生殖隔离的演化与瓦解发挥作用。分化过程中受正向选择影响的基因富集于多个具有重要功能的基因类群，包括已知参与植物先天免疫的经典“物种形成基因”候选位点。
研究结果表明，在这两个杂交物种中，适应性分化主要通过内在遗传与人口统计学过程影响生殖隔离。将基因组数据与分子生物学数据相结合，有望揭示特定遗传通路对物种形成的调控效应。