Data from: Extremophile Poeciliidae: multivariate insights into the complexity of speciation along replicated ecological gradients

Background: Replicate population pairs that diverge in response to similar selective regimes allow for an investigation of (a) whether phenotypic traits diverge in a similar and predictable fashion, (b) whether there is gradual variation in phenotypic divergence reflecting variation in the strength of natural selection among populations, (c) whether the extent of this divergence is correlated between multiple character suites (i.e., concerted evolution), and (d) whether gradual variation in phenotypic divergence predicts the degree of reproductive isolation, pointing towards a role for adaptation as a driver of (ecological) speciation. Here, we use poeciliid fishes of the genera Gambusia and Poecilia that have repeatedly evolved extremophile lineages able to tolerate high and sustained levels of toxic hydrogen sulfide (H2S) to answer these questions. Results: We investigated evolutionary divergence in response to H2S in Gambusia spp. (and to a lesser extent Poecilia spp.) using a multivariate approach considering the interplay of life history, body shape, and population genetics (nuclear miscrosatellites to infer population genetic differentiation as a proxy for reproductive isolation). We uncovered both shared and unique patterns of evolution: most extremophile Gambusia predictably evolved larger heads and offspring size, matching a priori predictions for adaptation to sulfidic waters, while variation in adult life histories was idiosyncratic. When investigating patterns for both genera (Gambusia and Poecilia), we found that divergence in offspring-related life histories and body shape were positively correlated across populations, but evidence for individual-level associations between the two character suites was limited, suggesting that genetic linkage, developmental interdependencies, or pleiotropic effects do not explain patterns of concerted evolution. We further found that phenotypic divergence was positively correlated with both environmental H2S-concentration and neutral genetic differentiation (a proxy for gene flow). Conclusions: Our results suggest that higher toxicity exerts stronger selection, and that divergent selection appears to constrain gene flow, supporting a scenario of ecological speciation. Nonetheless, progress toward ecological speciation was variable, partially reflecting variation in the strength of divergent selection, highlighting the complexity of selective regimes even in natural systems that are seemingly governed by a single, strong selective agent.研究背景：对响应相似选择压力发生分化的重复种群对开展研究，可用于探讨如下科学问题：(a) 表型性状是否以相似且可预测的方式发生分化；(b) 表型分化是否存在梯度变异，以此反映不同种群间自然选择强度的差异；(c) 该分化程度是否在多个性状组合（即协同进化）间存在相关性；(d) 表型分化的梯度变异是否能够预测生殖隔离的程度，从而揭示适应在（生态）物种形成过程中的驱动作用。本研究以花鳉科（poeciliid）鱼类中的食蚊鱼属（Gambusia）和花鳉属（Poecilia）为研究对象，这类鱼类多次演化出可耐受高浓度且持续存在的毒性硫化氢（H₂S）的嗜极端环境类群，以此解答上述科学问题。 研究结果：本研究采用多变量分析方法，综合考量生活史、体型形态与种群遗传学的相互关联，利用核微卫星标记推断种群遗传分化，将其作为生殖隔离的替代指标，探讨了食蚊鱼属（以及占比相对较少的花鳉属）鱼类在响应硫化氢环境时的进化分化模式。本研究揭示了进化过程中兼具共性与独特性的模式：多数嗜极端环境的食蚊鱼可预测地演化出更大的头部与子代体型，这与适应硫化水体的先验预测相符，而成体生活史的变异则各具特异性。在整合分析食蚊鱼属与花鳉属两类群的模式时，本研究发现子代相关生活史性状的分化与体型形态的分化在种群间呈正相关，但两类性状组合在个体水平上的关联证据有限，这表明遗传连锁、发育相互依存性或多效性效应并不能解释协同进化的模式。进一步研究发现，表型分化程度与环境硫化氢浓度以及中性遗传分化（即基因流的替代指标）均呈正相关。 研究结论：本研究结果表明，更高的毒性硫化氢施加了更强的选择压力，且分化选择似乎限制了基因流，支持了生态物种形成的理论假说。尽管如此，生态物种形成的进程存在差异，这部分反映了分化选择强度的变异，凸显了即使在看似仅受单一强选择因子调控的自然系统中，选择压力的复杂性。