Temperature is one of the most important environmental factors driving the genome-to-phenome relationship. Metabolic rates and related biological processes are predicted to increase with temperature due to the biophysical laws of chemical reactions. However, selection can also act on these processes across scales of biological organization, from individual enzymes to whole organisms. Although some studies have examined thermal responses across multiple scales, there is no general consensus on how these responses vary depending on the level of organization, or whether rates actually follow predicted theoretical patterns such as Arrhenius-like exponential responses or thermal performance curves (TPCs) that show peak responses. Here, we performed a meta-analysis on studies of ectotherms where biological rates were measured across the same set of temperatures, but at multiple levels of biological organization: enzyme activities, mitochondrial respiration, and/or whole-animal metabolic rates. Our final dataset consisted of 235 pairwise comparisons between levels of organization from 13 publications. Thermal responses differed drastically across levels of biological organization, sometimes showing completely opposite patterns. We developed a new effect size metric, 'organizational disagreement', to quantify the difference in responses among levels of biological organization. Overall, rates at higher levels of biological organization (e.g., whole animal metabolic rates) increased more quickly with temperature than rates at lower levels, contrary to our predictions. Responses may differ across levels due to differing consequences of biochemical laws with increasing organization or due to selection for different responses. However, taxa and tissues examined generally did not affect organizational disagreement. Theoretical TPCs, where rates increase to a peak value and then drop, were only rarely observed (12%), possibly because a broad range of test temperatures were rarely investigated. Exponential increases following Arrhenius predictions were more common (29%). This result suggests a classic assumption about thermal responses in biological rates is rarely observed in empirical datasets, although our results should be interpreted cautiously due to the lack of complete thermal profiles. We advocate for authors to explicitly address organizational disagreement in their interpretations and to measure thermal responses across a wider, more incremental range of temperatures. These results further emphasize the complexity of connecting the genome to the phenome when environmental plasticity is incorporated: the impact of the environment on the phenotype can depend on the scale of organization considered.

中文翻译：

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不同生物组织水平的热反应不同

温度是驱动基因组与现象关系的最重要的环境因素之一。由于化学反应的生物物理定律，预计代谢率和相关的生物过程会随着温度的升高而增加。然而，选择也可以在生物组织的各个尺度上对这些过程起作用，从单个酶到整个生物体。尽管一些研究已经研究了多个尺度的热响应，但对于这些响应如何根据组织水平而变化，或者速率是否实际遵循预测的理论模式，如阿伦尼乌斯指数响应或热性能曲线 (TPC)，尚未达成普遍共识。显示峰值响应。这里，我们对变温动物的研究进行了荟萃分析，其中生物速率是在同一组温度下测量的，但在生物组织的多个层面：酶活性、线粒体呼吸和/或全动物代谢率。我们的最终数据集由来自 13 篇出版物的组织级别之间的 235 个成对比较组成。不同生物组织水平的热反应差异很大，有时表现出完全相反的模式。我们开发了一个新的效应大小度量，“组织分歧”，以量化生物组织水平之间反应的差异。总体而言，与我们的预测相反，较高水平的生物组织（例如，整个动物的代谢率）随温度升高的速率比较低水平的速率增加得更快。由于随着组织的增加或由于对不同反应的选择而产生的生化规律的不同后果，反应可能因水平而异。然而，检查的分类群和组织通常不会影响组织分歧。理论 TPC，其中速率增加到峰值然后下降，很少被观察到 (12%)，可能是因为很少研究广泛的测试温度。Arrhenius 预测后的指数增长更为常见（29%）。这一结果表明，在经验数据集中很少观察到关于生物速率热响应的经典假设，尽管由于缺乏完整的热剖面，我们的结果应该谨慎解释。我们提倡作者在他们的解释中明确解决组织上的分歧，并在更广泛、更增量的温度范围内测量热响应。这些结果进一步强调了当环境可塑性被纳入时将基因组连接到表型的复杂性：环境对表型的影响可能取决于所考虑的组织规模。