Data from: Clines on the seashore: the genomic architecture underlying rapid divergence in the face of gene flow

Adaptive divergence and speciation may happen despite opposition by gene flow. Identifying the genomic basis underlying divergence with gene flow is a major task in evolutionary genomics. Most approaches (e.g. outlier scans) focus on genomic regions of high differentiation. However, not all genomic architectures potentially underlying divergence are expected to show extreme differentiation. Here, we develop an approach that combines hybrid zone analysis (i.e. focuses on spatial patterns of allele frequency change) with system-specific simulations to identify loci inconsistent with neutral evolution. We apply this to a genome-wide SNP set from an ideally-suited study organism, the intertidal snail Littorina saxatilis, which shows primary divergence between ecotypes associated with different shore habitats. We detect many SNPs with clinal patterns, most of which are consistent with neutrality. Among non-neutral SNPs, most are located within three large putative inversions differentiating ecotypes. Many non-neutral SNPs show relatively low levels of differentiation. We discuss potential reasons for this pattern, including loose linkage to selected variants, polygenic adaptation and a component of balancing selection within populations (which may be expected for inversions). Our work is in line with theory predicting a role for inversions in divergence, and emphasises that genomic regions contributing to divergence may not always be accessible with methods purely based on allele frequency differences. These conclusions call for approaches that take spatial patterns of allele frequency change into account in other systems.

尽管存在基因流（gene flow）的拮抗作用，适应性分化与物种形成仍可能发生。解析存在基因流情况下的分化背后的基因组基础，是进化基因组学领域的核心研究任务之一。多数分析方法（如异常位点扫描（outlier scans））均聚焦于分化程度较高的基因组区域。然而，并非所有潜在参与分化的基因组架构都将呈现极端分化水平。本研究开发了一种整合杂交带分析（hybrid zone analysis，即聚焦等位基因频率变化的空间模式）与类群特异性模拟的分析方法，用于识别不符合中性进化（neutral evolution）模式的位点。我们将该方法应用于一种理想研究生物——潮间带滨螺（Littorina saxatilis）的全基因组单核苷酸多态性（Single Nucleotide Polymorphism，简称SNP）数据集，该物种的不同生态型（ecotype）因栖息于不同海岸生境而呈现初级分化。我们检测到大量呈现渐变模式（clinal pattern）的SNP，其中多数符合中性进化预期。在非中性SNP中，多数位于三个可区分生态型的大型推定倒位（putative inversion）区域内。许多非中性SNP的分化程度相对较低。我们探讨了该模式的潜在成因，包括与受选择变异的松散连锁、多基因适应性（polygenic adaptation），以及种群内存在的平衡选择（balancing selection）组分（倒位区域常出现此类选择模式）。本研究结果与“倒位在分化过程中发挥作用”的理论预测相符，并强调：仅基于等位基因频率差异的分析方法，并非总能检测到参与分化的基因组区域。上述结论呼吁在其他类群研究中，采用纳入等位基因频率变化空间模式的分析方法。