Data from: RAD-sequencing highlights polygenic discrimination of habitat ecotypes in the panmictic American eel (Anguilla rostrata)

The two primary ways that species respond to heterogeneous environments is through local adaptation and phenotypic plasticity. The American eel (Anguilla rostrata) presents a paradox; despite inhabiting drastically different environments [ 1 ], the species is panmictic [ 2, 3 ]. Spawning takes place only in the southern Sargasso Sea in the Atlantic Ocean [ 1 ]. Then, the planktonic larvae (leptocephali) disperse to rearing locations from Cuba to Greenland, and juveniles colonize either freshwater or brackish/saltwater habitats, where they spend 3–25 years before returning to the Sargasso Sea to spawn as a panmictic species. Depending on rearing habitat, individuals exhibit drastically different ecotypes [ 4–6 ]. In particular, individuals rearing in freshwater tend to grow slowly and mature older and are more likely to be female in comparison to individuals that rear in brackish/saltwater [ 4, 6 ]. The hypothesis that phenotypic plasticity alone can account for all of the differences was not supported by three independent controlled experiments [ 7–10 ]. Here, we present a genome-wide association study that demonstrates a polygenic basis that discriminates these habitat-specific ecotypes belonging to the same panmictic population. We found that 331 co-varying loci out of 42,424 initially considered were associated with the divergent ecotypes, allowing a reclassification of 89.6%. These 331 SNPs are associated with 101 genes that represent vascular and morphological development, calcium ion regulation, growth and transcription factors, and olfactory receptors. Our results are consistent with divergent natural selection of phenotypes and/or genotype-dependent habitat choice by individuals that results in these genetic differences between habitats, occurring every generation anew in this panmictic species.物种应对异质环境的两种核心途径为局部适应（local adaptation）与表型可塑性（phenotypic plasticity）。美洲鳗鲡（Anguilla rostrata）却呈现出一个经典悖论：尽管其栖息环境差异悬殊[1]，该物种却属于泛交种群（panmictic）[2,3]。该物种仅在大西洋南部的马尾藻海产卵[1]，随后其浮游幼体（柳叶鳗幼体，leptocephali）会扩散至从古巴到格陵兰的各类育幼栖息地，幼体会定居于淡水或咸淡水/咸水环境中，并在此度过3至25年，之后返回马尾藻海产卵，始终以泛交种群的方式完成繁殖循环。依据育幼栖息地的不同，个体可展现出截然不同的生态型[4–6]。具体而言，相较于在咸淡水/咸水环境中育幼的个体，淡水育幼的个体生长速率更慢、成熟年龄更晚，且雌性占比更高[4,6]。仅有表型可塑性即可解释全部差异的假说，并未得到三项独立对照实验的支持[7–10]。本研究开展了全基因组关联分析（genome-wide association study），结果证实存在多基因基础（polygenic basis），可区分隶属于同一泛交种群的这些栖息地特异性生态型。我们在初始筛选的42424个位点中，发现331个协同变异位点与这些分化的生态型显著相关，该分类模型的准确率可达89.6%。这331个单核苷酸多态性（SNPs）位点与101个基因相关联，这些基因涉及血管与形态发育、钙离子调节、生长及转录因子，以及嗅觉受体。我们的研究结果与表型的趋异自然选择，以及/或个体的基因型依赖性栖息地选择相契合——正是这一过程在该泛交物种的每一代中，持续造就了不同栖息地间的遗传差异。