Park Jane, Brown Charles, Hess Chelsea, Armstrong Madison, Rocke David M, Galvez Fernando, Whitehead Andrew
Department of Environmental Toxicology University of California Davis Davis California USA.
Department of Biological Sciences Louisiana State University Baton Rouge Louisiana USA.
Evol Appl. 2025 May 15;18(5):e70112. doi: 10.1111/eva.70112. eCollection 2025 May.
Persistence of wild species in human-altered environments is difficult, in part because challenges to fitness are complex when multiple environmental changes occur simultaneously, which is common in the Anthropocene. This complexity is difficult to conceptualize because the nature of environmental change is often highly context specific. A mechanism-guided approach may help to shape intuition and predictions about complexity; fitness challenges posed by co-occurring stressors with similar mechanisms of action may be less severe than for those with different mechanisms of action. We approach these considerations within the context of ecotoxicology because this field is built upon a rich mechanistic foundation. We hypothesized that evolved resistance to one class of common toxicants would afford resilience to the fitness impacts of another class of common toxicants that shares mechanisms of toxicity. killifish populations in urban estuaries have repeatedly evolved resistance to persistent organic pollutants including PCBs. Since PCBs and some of the toxicants that constitute crude oil (e.g., high molecular weight PAHs) exert toxicity through perturbation of AHR signaling, we predicted that PCB-resistant populations would also be resilient to crude oil toxicity. Common garden comparative oil exposure experiments, including killifish populations with different exposure histories, showed that most killifish populations were sensitive to fitness impacts (reproduction and development) caused by oil exposure, but that fish from the PCB-resistant population were insensitive. Population differences in toxic outcomes were not compatible with random-neutral expectations. Transcriptomics revealed that the molecular mechanisms that contributed to population variation in PAH resilience were shared with those that contribute to evolved variation in PCB resilience. We conclude that the fitness challenge posed by environmental pollutants is effectively reduced when those chemicals share mechanisms that affect fitness. Mechanistic considerations may help to scale predictions regarding the fitness challenges posed by stressors that may co-occur in human-altered environments.
野生物种在人类改变的环境中持续生存很困难，部分原因是当多种环境变化同时发生时，对适应性的挑战很复杂，而这在人类世很常见。这种复杂性难以概念化，因为环境变化的性质往往高度依赖具体情境。一种基于机制的方法可能有助于形成对复杂性的直觉和预测；具有相似作用机制的同时出现的应激源所带来的适应性挑战，可能不如具有不同作用机制的应激源那么严重。我们在生态毒理学的背景下探讨这些问题，因为该领域建立在丰富的机制基础之上。我们假设，对一类常见毒物的进化抗性会使对另一类具有相同毒性机制的常见毒物的适应性影响具有恢复力。城市河口的鳉鱼种群已多次进化出对包括多氯联苯在内的持久性有机污染物的抗性。由于多氯联苯和构成原油的一些毒物（如高分子量多环芳烃）通过干扰芳烃受体（AHR）信号传导发挥毒性，我们预测对多氯联苯有抗性的种群对原油毒性也具有恢复力。包括具有不同暴露历史的鳉鱼种群在内的普通园圃比较油暴露实验表明，大多数鳉鱼种群对油暴露引起的适应性影响（繁殖和发育）敏感，但来自对多氯联苯有抗性种群的鱼不敏感。毒性结果的种群差异不符合随机中性预期。转录组学显示，导致多环芳烃恢复力种群差异的分子机制与导致多氯联苯恢复力进化差异的机制相同。我们得出结论，当这些化学物质具有影响适应性的相同机制时，环境污染物带来的适应性挑战会有效降低。基于机制的考虑可能有助于扩大对人类改变的环境中可能同时出现的应激源所带来的适应性挑战的预测。
