Data from: Fine-grained adaptive divergence in an amphibian: genetic basis of phenotypic divergence and the role of non-random gene flow in restricting effective migration among wetlands

Adaptive ecological differentiation among sympatric populations is promoted by environmental heterogeneity, strong local selection and restricted gene flow. High gene flow, on the other hand, is expected to homogenize genetic variation among populations and therefore prevent local adaptation. Understanding how local adaptation can persist at the spatial scale at which gene flow occurs has remained an elusive goal, especially for wild vertebrate populations. Here, we explore the roles of natural selection and nonrandom gene flow (isolation by breeding time and habitat choice) in restricting effective migration among local populations and promoting generalized genetic barriers to neutral gene flow. We examined these processes in a network of 17 breeding ponds of the moor frog Rana arvalis, by combining environmental field data, a common garden experiment and data on variation in neutral microsatellite loci and in a thyroid hormone receptor (TRβ) gene putatively under selection. We illustrate the connection between genotype, phenotype and habitat variation and demonstrate that the strong differences in larval life history traits observed in the common garden experiment can result from adaptation to local pond characteristics. Remarkably, we found that haplotype variation in the TRβ gene contributes to variation in larval development time and growth rate, indicating that polymorphism in the TRβ gene is linked with the phenotypic variation among the environments. Genetic distance in neutral markers was correlated with differences in breeding time and environmental differences among the ponds, but not with geographical distance. These results demonstrate that while our study area did not exceed the scale of gene flow, ecological barriers constrained gene flow among contrasting habitats. Our results highlight the roles of strong selection and nonrandom gene flow created by phenological variation and, possibly, habitat preferences, which together maintain genetic and phenotypic divergence at a fine-grained spatial scale.

同域种群（sympatric populations）间的适应性生态分化，可由环境异质性、强局域选择以及受限基因流（gene flow）所推动。反之，高基因流则会使种群间的遗传变异趋于同质化，进而阻碍局域适应过程。探究在基因流发生的空间尺度下，局域适应如何得以维持，一直是一项颇具挑战性的研究目标，针对野生脊椎动物种群而言尤其如此。本研究旨在探究自然选择与非随机基因流（nonrandom gene flow，即基于繁殖时间与生境选择的隔离）在限制局域种群间有效迁移、推动中性基因流（neutral gene flow）的广义遗传屏障形成过程中所发挥的作用。我们以17处田野林蛙（Rana arvalis）繁殖水塘组成的研究网络为对象，结合野外环境调查数据、同质园实验（common garden experiment）数据，以及中性微卫星位点（neutral microsatellite loci）与推测处于选择压力下的甲状腺激素受体β（TRβ）基因的变异数据，对上述过程展开了分析。本研究阐明了基因型、表型与生境变异之间的关联，并证实同质园实验中观测到的幼虫生活史性状显著差异，可归因于对当地水塘环境特征的适应。值得注意的是，我们发现TRβ基因的单倍型变异（haplotype variation）会影响幼虫发育时长与生长速率，这表明TRβ基因多态性（polymorphism）与不同生境间的表型变异存在关联。中性标记的遗传距离与水塘间的繁殖时间差异及环境差异呈显著相关，但与地理距离并无关联。上述结果表明，尽管本研究区域未超出基因流发生的尺度，但生态屏障仍限制了不同生境间的基因流。本研究结果凸显了强选择与由物候变异及潜在生境偏好所介导的非随机基因流的作用，二者共同在精细空间尺度上维持了遗传与表型分化。