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Synopsis 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” (OD) 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 OD. 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 was 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 OD 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.
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A Unifying Framework for Understanding Biological Structures and Functions Across Levels of Biological Organization
Abstract The relationship between structure and function is a major constituent of the rules of life. Structures and functions occur across all levels of biological organization. Current efforts to integrate conceptual frameworks and approaches to address new and old questions promise to allow a more holistic and robust understanding of how different biological functions are achieved across levels of biological organization. Here, we provide unifying and generalizable definitions of both structure and function that can be applied across all levels of biological organization. However, we find differences in the nature of structures at the organismal level and below as compared to above the level of the organism. We term these intrinsic and emergent structures, respectively. Intrinsic structures are directly under selection, contributing to the overall performance (fitness) of the individual organism. Emergent structures involve interactions among aggregations of organisms and are not directly under selection. Given this distinction, we argue that while the functions of many intrinsic structures remain unknown, functions of emergent structures are the result of the aggregate of processes of individual organisms. We then provide a detailed and unified framework of the structure–function relationship for intrinsic structures to explore how their unknown functions can be defined. We provide examples of how these scalable definitions applied to intrinsic structures provide a framework to address questions on structure–function relationships that can be approached simultaneously from all subdisciplines of biology. We propose that this will produce a more holistic and robust understanding of how different biological functions are achieved across levels of biological organization.
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- Award ID(s):
- 2105167
- PAR ID:
- 10331037
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 61
- Issue:
- 6
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 2038 to 2047
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/icb/icab167
