Data from: Targeted sequence capture and resequencing implies a predominant role of regulatory regions in the divergence of a sympatric lake whitefish species pair (Coregonus clupeaformis)

Latest technological developments in evolutionary biology bring new challenges in documenting the intricate genetic architecture of species in the process of divergence. Sympatric populations of lake whitefish represent one of the key systems to investigate this issue. Despite the value of random genotype-by-sequencing methods and decreasing cost of sequencing technologies, it remains challenging to investigate variation in coding regions, especially in the case of recently duplicated genomes as in salmonids, as this greatly complicates whole genome resequencing. We thus designed a sequence capture array targeting 2773 annotated genes to document the nature and the extent of genomic divergence between sympatric dwarf and normal whitefish. Among the 2728 genes successfully captured, a total of 2182 coding and 10 415 noncoding putative single-nucleotide polymorphisms (SNPs) were identified after applying a first set of basic filters. A genome scan with a quality-refined selection of 2203 SNPs identified 267 outlier SNPs in 210 candidate genes located in genomic regions potentially involved in whitefish divergence and reproductive isolation. We found highly heterogeneous FST estimates among SNP loci. There was an overall low level of coding polymorphism, with a predominance of noncoding mutations among outliers. The heterogeneous patterns of divergence among loci confirm the porous nature of genomes during speciation with gene flow. Considering that few protein-coding mutations were identified as highly divergent, our results, along with previous transcriptomic studies, imply that changes in regulatory regions most likely had a greater role in the process of whitefish population divergence than protein-coding mutations. This study is the first to demonstrate the efficiency of large-scale targeted resequencing for a nonmodel species with such a large and unsequenced genome.进化生物学领域的最新技术进展，为解析正处于物种分化进程中的复杂遗传结构带来了全新挑战。湖白鲑的同域种群正是研究该问题的关键模式系统之一。尽管随机基因型测序（genotype-by-sequencing, GBS）方法具有重要应用价值，且测序技术成本持续降低，但对编码区变异的解析仍存在诸多难点；尤其对于鲑科这类近期发生全基因组复制的类群，全基因组重测序的复杂度会大幅提升，进一步加剧了这一困境。为此，我们设计了靶向2773个已注释基因的序列捕获阵列，以解析同域分布的矮型与普通型湖白鲑之间的基因组分化特征与分化程度。在成功捕获的2728个基因中，经首轮基础过滤后，共鉴定出2182个编码区推定单核苷酸多态性（single-nucleotide polymorphisms, SNPs）与10415个非编码区推定SNPs。通过对经过质量优化筛选的2203个SNPs进行全基因组扫描，在210个候选基因中鉴定出267个异常SNPs，这些基因所在的基因组区域可能与湖白鲑的分化及生殖隔离密切相关。我们发现SNP位点间的固定指数（fixation index, FST）估计值存在高度异质性。整体而言，编码区多态性水平较低，异常位点中非编码突变占主导地位。位点间分化模式的异质性，证实了存在基因流的物种形成过程中基因组的多孔性特征。鉴于仅有少量蛋白质编码突变被鉴定为高度分化，我们的研究结果结合此前的转录组学研究表明，与蛋白质编码突变相比，调控区域的变异极有可能在湖白鲑种群分化进程中发挥了更为关键的作用。本研究首次证实了，针对这类基因组庞大且尚未完成测序的非模式物种开展大规模靶向重测序的有效性与可行性。