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The origin and maintenance of metabolic allometry in animals

Abstract

Organisms vary widely in size, from microbes weighing 0.1 pg to trees weighing thousands of megagrams — a 1021-fold range similar to the difference in mass between an elephant and the Earth. Mass has a pervasive influence on biological processes, but the effect is usually non-proportional; for example, a tenfold increase in mass is typically accompanied by just a four- to sevenfold increase in metabolic rate. Understanding the cause of allometric scaling has been a long-standing problem in biology. Here, we examine the evolution of metabolic allometry in animals by linking microevolutionary processes to macroevolutionary patterns. We show that the genetic correlation between mass and metabolic rate is strong and positive in insects, birds and mammals. We then use these data to simulate the macroevolution of mass and metabolic rate, and show that the interspecific relationship between these traits in animals is consistent with evolution under persistent multivariate selection on mass and metabolic rate over long periods of time.

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Fig. 1: Phylogenetic distribution of the genetic correlation (rG) between Rm and M.
Fig. 2: Relationship between Rm and M predicted by random evolution.
Fig. 3: Empirical and simulated distributions of metabolic scaling exponents and mass-independent variation in Rm.
Fig. 4: Metabolic scaling relationships are not consistent with random evolution under a genetic constraint alone.
Fig. 5: Phylogenetic diversity of Rm and M.

Data availability

All data generated or analysed during this study are included within the article and its supplementary Information files.

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Acknowledgements

This research was supported by the Australian Research Council (projects DP110101776, FT130101493, DP170101114 and DP180103925).

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Contributions

C.R.W., D.O.-B. and D.J.M. designed the study. C.R.W., L.A.A., P.A.A., J.E.B., C.L.B., C.C., T.S.C., A.J., E.P., H.S.W.-S., M.J.A., S.F.C., C.E.F., L.G.H., M.R.K. and S.J.P. collected the data. C.R.W. analysed the data. C.R.W. and D.O.-B. wrote the first version of the manuscript. All authors contributed to and approved the final version.

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Correspondence to Craig R. White.

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Supplementary Methods, Supplementary References, Supplementary Tables 1–7 and Supplementary Figures 1–4

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White, C.R., Marshall, D.J., Alton, L.A. et al. The origin and maintenance of metabolic allometry in animals. Nat Ecol Evol 3, 598–603 (2019). https://doi.org/10.1038/s41559-019-0839-9

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