Linking transcriptional responses to organismal tolerance reveals mechanisms of thermal sensitivity in a mesothermal endangered fish

Forecasting species' responses to climate change requires understanding the underlying mechanisms governing environmental stress tolerance, including acclimation capacity and acute stress responses. Current knowledge of these physiological processes in aquatic ectotherms is largely drawn from eurythermal or extreme stenothermal species. Yet many species of conservation concern exhibit tolerance windows and acclimation capacities in between these extremes. We linked transcriptome profiles to organismal tolerance in a mesothermal endangered fish, the delta smelt (Hypomesus transpacificus), to quantify the cellular processes, sublethal thresholds and effects of thermal acclimation on acute stress responses. Delta smelt initiated rapid molecular changes in line with expectations of theoretical thermal limitation models, but also exhibited diminished capacity to modify the expression of some genes and cellular mechanisms key to coping with acute thermal stress found in eurytherms. Sublethal critical thresholds occurred 4–6 °C below their upper tolerance limits, and thermal acclimation shifted the onset of acute thermal stress and tolerance as predicted. However, we found evidence that delta smelt's limited thermal plasticity may be partially due to an inability of individuals to effectively make physiological adjustments to truly achieve new homoeostasis under heightened temperatures, resulting in chronic thermal stress. These findings provide insight into the physiological basis of the diverse patterns of thermal tolerances observed in nature. Moreover, understanding how underlying molecular mechanisms shape thermal acclimation capacity, acute stress responses and ultimately differential phenotypes contributes to a predictive framework to deduce species' responses in situ to changes in selective pressures due to climate change.

预测物种对气候变化的响应，需阐明调控环境胁迫耐受性的内在机制，涵盖驯化能力与急性胁迫响应过程。目前学界对水生变温动物此类生理过程的认知，大多源自广温性或极端狭温性物种的研究。然而诸多具有保育价值的物种，其耐受窗口与驯化能力恰好处于这两类极端物种之间。本研究以中温性濒危鱼类三角洲胡瓜鱼（Hypomesus transpacificus）为对象，将其转录组表达谱与机体耐受性进行关联分析，以量化细胞生理过程、亚致死临界阈值，以及热驯化对急性胁迫响应的调控效应。三角洲胡瓜鱼的快速分子变化符合理论热限制模型的预测，但同时也表现出调控部分基因表达的能力减弱——此类基因与细胞机制是广温性物种应对急性热胁迫的关键。亚致死临界阈值较其最高耐受极限低4~6℃，且热驯化可如预期般改变急性热胁迫与耐受性的触发节点。但本研究发现，三角洲胡瓜鱼有限的热可塑性，可能部分源于个体无法在高温环境下有效完成生理调整以真正建立新的内稳态，进而引发慢性热胁迫。本研究结果为自然界中多样的热耐受模式提供了生理层面的阐释。此外，阐明内在分子机制如何调控热驯化能力、急性胁迫响应，并最终塑造差异化表型，可为推演物种在气候变化引发的选择压力变化下的原位响应提供预测性框架。