Shi Yue, Bouska Kristen L, McKinney Garrett J, Dokai William, Bartels Andrew, McPhee Megan V, Larson Wesley A
College of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Juneau, Alaska, USA.
Wisconsin Cooperative Fishery Research Unit, College of Natural Resources, University of Wisconsin-Stevens Point, Stevens Point, Wisconsin, USA.
Mol Ecol. 2023 Apr;32(7):1549-1566. doi: 10.1111/mec.16317. Epub 2021 Dec 27.
Understanding how gene flow influences adaptive divergence is important for predicting adaptive responses. Theoretical studies suggest that when gene flow is high, clustering of adaptive genes in fewer genomic regions would protect adaptive alleles from recombination and thus be selected for, but few studies have tested it with empirical data. Here, we used restriction site-associated sequencing to generate genomic data for six fish species with contrasting life histories from six reaches of the Upper Mississippi River System, USA. We used four differentiation-based outlier tests and three genotype-environment association analyses to define neutral single nucleotide polymorphisms (SNPs) and outlier SNPs that were putatively under selection. We then examined the distribution of outlier SNPs along the genome and investigated whether these SNPs were found in genomic islands of differentiation and inversions. We found that gene flow varied among species, and outlier SNPs were clustered more tightly in species with higher gene flow. The two species with the highest overall F (0.0303-0.0720) and therefore lowest gene flow showed little evidence of clusters of outlier SNPs, with outlier SNPs in these species spreading uniformly across the genome. In contrast, nearly all outlier SNPs in the species with the lowest F (0.0003) were found in a single large putative inversion. Two other species with intermediate gene flow (F ~ 0.0025-0.0050) also showed clustered genomic architectures, with most islands of differentiation clustered on a few chromosomes. Our results provide important empirical evidence to support the hypothesis that increasingly clustered architecture of local adaptation is associated with high gene flow.
了解基因流如何影响适应性分化对于预测适应性反应至关重要。理论研究表明，当基因流较高时，适应性基因在较少基因组区域的聚集会保护适应性等位基因不发生重组，从而被选择保留，但很少有研究用实证数据对其进行验证。在此，我们利用限制性位点关联测序技术，为来自美国密西西比河上游水系六个河段、具有不同生活史的六种鱼类生成基因组数据。我们使用了四种基于分化的离群值检验和三种基因型 - 环境关联分析来定义中性单核苷酸多态性（SNP）和可能受到选择的离群SNP。然后，我们检查了离群SNP在基因组中的分布，并研究这些SNP是否存在于分化基因组岛和倒位中。我们发现，不同物种间基因流存在差异，离群SNP在基因流较高的物种中聚集得更紧密。总体F值最高（0.0303 - 0.0720）因而基因流最低的两个物种几乎没有离群SNP聚集的证据，这些物种中的离群SNP在基因组中均匀分布。相反，F值最低（0.0003）的物种中，几乎所有离群SNP都存在于一个单一的大型假定倒位中。另外两个基因流中等（F约为0.0025 - 0.0050）的物种也表现出聚集的基因组结构，大多数分化岛聚集在少数几条染色体上。我们的结果提供了重要的实证证据，支持局部适应性的聚集结构增加与高基因流相关这一假说。
