Data from: Putative chromosomal rearrangements are associated primarily with ecotype divergence rather than geographic separation in an intertidal, poorly-dispersing snail

Littorina saxatilis is becoming a model system for understanding the genomic basis of ecological speciation. The parallel formation of crab-adapted ecotypes that exhibit partial reproductive isolation from wave-adapted ecotypes has enabled genomic investigation of conspicuous shell traits. Recent genomic studies suggest that chromosomal rearrangements may enable ecotype divergence by reducing gene flow. However, the genomic architecture of traits that are divergent between ecotypes remains poorly understood. Here, we use 11,504 single nucleotide polymorphism (SNP) markers called using the recently-released L. saxatilis genome to genotype 462 crab ecotype, wave ecotype, and phenotypically-intermediate L. saxatilis individuals with scored phenotypes. We used redundancy analysis to study the genetic architecture of loci associated with shell shape, shape corrected for size, shell size, and shell ornamentation, and to compare levels of co-association among different traits. We discovered 341 SNPs associated with shell traits. Loci associated with trait divergence between ecotypes were often located inside putative chromosomal rearrangements recently characterized in Swedish L. saxatilis. In contrast, we found that shell shape corrected for size varied primarily by site rather than by ecotype and showed little association with these putative rearrangements. Together, these results reveal that genomic regions of elevated divergence with putative rearrangements are associated with divergence along steep environmental axes in L. saxatilis ecotypes, consistent with models of adaptation with gene flow, but these regions are distinct from genomic architecture associated with site-specific variation. Our findings here further support predictions from models indicating the importance of genomic regions of reduced recombination allowing co-association of loci during ecological speciation with ongoing gene flow.

滨螺（Littorina saxatilis）现已成为解析生态物种形成基因组基础的模式研究系统。适应蟹类捕食的生态型与适应波浪冲击的生态型之间存在部分生殖隔离，二者的平行演化形成了该系统的核心特征，为探究显著壳表性状的基因组机制提供了理想契机。近期基因组研究表明，染色体重排可通过降低基因流推动生态型分化，但生态型间分化性状的基因组架构仍不甚明晰。本研究基于新近发布的滨螺参考基因组，利用11504个单核苷酸多态性（SNP）标记，对462个适应蟹类捕食的生态型、适应波浪冲击的生态型以及表型中间型滨螺个体进行基因分型，所有个体均带有已量化的表型数据。本研究采用冗余分析，探究与壳形、校正体型后的壳形、壳体大小以及壳表纹饰相关的位点遗传架构，并比较不同性状间的共关联水平。研究共鉴定出341个与壳类性状相关的SNP位点。与生态型间性状分化相关的位点，大多位于瑞典滨螺中已被表征的推定染色体重排区域内。与之相反，校正体型后的壳形主要随采样位点分化，而非随生态型分化，且与上述推定重排区域几乎无关联。综合来看，本研究结果表明，滨螺生态型中伴随推定重排的高分化基因组区域，与陡峭环境梯度下的性状分化相关，这与存在基因流的适应性演化模型相符，但此类区域与介导位点特异性变异的基因组架构截然不同。本研究结果进一步支持相关模型的预测：在存在持续基因流的生态物种形成过程中，重组率降低的基因组区域可促进位点间的共关联，这一机制具有重要意义。