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：针对响应相似选择压力情境（selective regimes）发生趋异分化的重复种群对，可开展四类科学探究：(a) 表型性状（phenotypic traits）的趋异是否以相似且可预测的模式展开；(b) 表型趋异是否存在渐进变异，以此反映不同种群间自然选择强度的差异；(c) 该趋异程度是否在多个性状组（character suites，即协同进化（concerted evolution））之间存在相关性；(d) 表型趋异的渐进变异能否预测生殖隔离（reproductive isolation）的程度，进而揭示适应在（生态）物种形成（ecological speciation）中的驱动作用。本研究以食蚊鱼属（Gambusia）和花鳉属（Poecilia）的花鳉科鱼类为研究材料，该类群多次演化出能够耐受高浓度且持续存在的有毒硫化氢（H₂S）的极端嗜极谱系（extremophile lineages），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、体型与种群遗传学（population genetics）的相互作用，探究了食蚊鱼属物种（Gambusia spp.，花鳉属物种（Poecilia spp.）的分析占比相对较低）对硫化氢响应的演化趋异。其中，种群遗传学分析借助核微卫星（nuclear microsatellites）标记推断种群遗传分化，将其作为生殖隔离的替代指标。本研究揭示了兼具共有与特异的演化模式：多数极端嗜极的食蚊鱼属类群按照先验预测，演化出更大的头部与后代体型，这与适应硫化物水域的预期相符；而成体生活史的变异则呈现物种特异性。在对两个属（食蚊鱼属与花鳉属）的整体模式进行分析时，我们发现种群间与后代相关的生活史趋异与体型趋异呈显著正相关，但两个性状组之间的个体水平关联证据有限，这表明遗传连锁、发育互作或多效性效应（pleiotropic effects）无法解释协同进化的格局。此外，我们还发现表型趋异与环境硫化氢浓度以及中性遗传分化（基因流（gene flow）的替代指标）均呈显著正相关。
研究结论：本研究结果显示，更高的毒性会施加更强的选择压力，而歧化选择似乎会限制基因流，这支持了生态物种形成的演化情景假说。尽管如此，生态物种形成的进程存在差异，这部分源于歧化选择强度的变异，这也凸显了即使在看似受单一强选择因子调控的自然系统中，选择压力情境也具有复杂性。