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：针对相似选择压力环境（selective regimes）产生分化的重复种群对，可用于开展四项科学探究：(a) 表型性状（phenotypic traits）是否以相似且可预测的模式发生分化；(b) 表型分化是否存在梯度变异，以此反映种群间自然选择强度的差异；(c) 多种性状组合（即协同进化（concerted evolution））间的分化程度是否存在相关性；(d) 表型分化的梯度变异是否可预测生殖隔离（reproductive isolation）程度，进而揭示适应作用作为（生态物种形成（ecological speciation））驱动因子的角色。本研究以食蚊鱼属（Gambusia）和花鳉属（Poecilia）的花鳉科鱼类（poeciliid fishes）为研究对象，该类群多次演化出可耐受高浓度且持续暴露的有毒硫化氢（hydrogen sulfide, H₂S）的极端嗜极谱系（extremophile lineages），以此解答上述科学问题。
研究结果：本研究采用整合生活史、体型与种群遗传学（population genetics）关联的多变量分析方法（multivariate approach），探究了食蚊鱼属（Gambusia，次要分析花鳉属（Poecilia）类群）在硫化氢胁迫下的进化分化模式，其中以核微卫星（nuclear microsatellites，原文笔误为miscrosatellites）推断种群遗传分化，以此作为生殖隔离的替代指标。研究揭示了进化分化的共有与特有模式：多数嗜极食蚊鱼种群按照先验预测，演化出更大的头部与子代体型以适配硫化水环境；而成体生活史的变异则各具特异性。跨食蚊鱼属与花鳉属的整体分析显示，子代相关生活史与体型的分化在种群间呈正相关，但两类性状组合在个体水平的关联证据有限，提示遗传连锁（genetic linkage）、发育互作（developmental interdependencies）或多效性（pleiotropic effects）无法解释协同进化的模式。进一步分析发现，表型分化与环境硫化氢浓度、中性遗传分化（基因流（gene flow）的替代指标）均呈正相关。
研究结论：本研究结果表明，环境毒性越强则选择压力越大，且歧化选择（divergent selection）似乎会限制基因流，支持生态物种形成的演化场景。尽管如此，生态物种形成的进展存在差异，这部分源于歧化选择强度的变异，凸显了即使在看似受单一强选择因子主导的自然系统中，选择压力环境也具有复杂性。