Equal fitness paradigm explained by a trade-off between generation time and energy production rate

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Abstract

Most plant, animal and microbial species of widely varying body size and lifestyle are nearly equally fit as evidenced by their coexistence and persistence through millions of years. All organisms compete for a limited supply of organic chemical energy, derived mostly from photosynthesis, to invest in the two components of fitness: survival and production. All organisms are mortal because molecular and cellular damage accumulates over the lifetime; life persists only because parents produce offspring. We call this the equal fitness paradigm. The equal fitness paradigm occurs because: (1) there is a trade-off between generation time and productive power, which have equal-but-opposite scalings with body size and temperature; smaller and warmer organisms have shorter lifespans but produce biomass at higher rates than larger and colder organisms; (2) the energy content of biomass is essentially constant, ~22.4 kJ g−1 dry body weight; and (3) the fraction of biomass production incorporated into surviving offspring is also roughly constant, ~10–50%. As organisms transmit approximately the same quantity of energy per gram to offspring in the next generation, no species has an inherent lasting advantage in the struggle for existence. The equal fitness paradigm emphasizes the central importance of energy, biological scaling relations and power–time trade-offs in life history, ecology and evolution.

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Fig. 1: Energy balance of an individual organism.
Fig. 2: Generation time as a function of body mass plotted on logarithmic axes for a variety of organisms spanning more than 15 orders of magnitude in body mass.
Fig. 3: Mass-specific rate of biomass production as a function of dry body mass plotted on logarithmic axes for a variety of organisms spanning more than 20 orders of magnitude in body mass.
Fig. 4: Ash-free energy content of dry biomass, Q, as a function of body mass for a variety of animals, plants and microbes spanning about 18 orders of magnitude in body mass.
Fig. 5: The model for EFP parameterized with data from the text.

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Acknowledgements

We thank the following individuals for helpful discussions of ideas and/or comments on the manuscript: G. Boyle, J. R. Burger, K. Cummins, J. Damuth, B. J. Enquist, J. F. Gillooly, R. Hengeveld, C. Jordan, A. Kodric-Brown, C. Levitan, J. G. Okie and D. Storch.

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All three co-authors contributed to all aspects of the work.

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Correspondence to James H. Brown or Charles A. S. Hall.

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Supplementary Table 1

Data of Fig. 2 as an Excel file with columns giving taxon, genus, species, dry body mass, temperature in °C, uncorrected mortality rate, log10 dry body mass and log10 generation time at 20 °C, for 2,026 species.

Supplementary Table 2

Data of Fig. 4 as an Excel file with columns giving taxon, genus and species, dry body mass and ash-free energy content for 74 species.

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Brown, J.H., Hall, C.A.S. & Sibly, R.M. Equal fitness paradigm explained by a trade-off between generation time and energy production rate. Nat Ecol Evol 2, 262–268 (2018). https://doi.org/10.1038/s41559-017-0430-1

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