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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Boltzmann, L. The Second Law of Thermodynamics (Populare Schriften. Essay No. 3 (Address to Imperial Academy of Science in 1886)). Reprinted in English in Theoretical Physics and Philosophical Problems, Selected Writings of L. Boltzmann (D. Riedel, Dordrecht, 1905).
Lotka, A. J. Contribution to the energetics of evolution. Proc. Natl Acad. Sci. USA 8, 147–151 (1922).
Brody, S. Bioenergetics and Growth (Reinhold, New York, 1945).
Van Valen, L. Evolution as a zero-sum game for energy. Evol. Theor. 4, 289–300 (1980).
McNab, B. K. The Physiological Ecology of Vertebrates: A View from Energetics (Cornell Univ. Press, Ithaca, 2002).
Humphries, M. M. & McCann, K. S. Metabolic ecology. J. Anim. Ecol. 83, 7–19 (2014).
Judson, O. P. The energy expansions of evolution. Nat. Ecol. Evol. 1, 0138 (2017).
Peters, R. H. The Ecological Implications of Body Size (Cambridge Univ. Press, Cambridge, 1983).
Karasov, W. H. & del Rio, C. M. Physiological Ecology: How Animals Process Energy, Nutrients, and Toxins (Princeton Univ. Press, Princeton, 2007).
Sibly, R. M. et al. Representing the acquisition and use of energy by individuals in agent‐based models of animal populations. Methods Ecol. Evol. 4, 151–161 (2013).
Pearl, R. The Rate of Living (Knopf, New York, 1928).
Harman, D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11, 298–300 (1956).
Speakman, J. R. Body size, energy metabolism and lifespan. J. Exp. Biol. 208, 1717–1730 (2005).
Speakman, J. R. et al. Oxidative stress and life histories: unresolved issues and current needs. Ecol. Evol. 5, 5745–5757 (2015).
Calder, W. A. Size, Function, and Life History (Harvard Univ. Press, Cambridge, 1984).
Martin, A. P. & Palumbi, S. R. Body size, metabolic rate, generation time, and the molecular clock. Proc. Natl Acad. Sci. USA 90, 4087–4091 (1993).
Atanasov, A. T. The linear allometric relationship between total metabolic energy per life span and body mass of poikilothermic animals. Biosystems 82, 137–142 (2005).
Schmidt-Nielsen, K. Scaling: Why is Animal Size so Important? (Cambridge Univ. Press, Cambridge, 1984).
Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).
Kleiber, M. Body size and metabolism. Hilgardia 6, 315–353 (1932).
West, G. B., Brown, J. H. & Enquist, B. J. A general model for the origin of allometric scaling laws in biology. Science 276, 122–126 (1997).
Lindstedt, S. L. & Calder, W. A. III Body size, physiological time, and longevity of homeothermic animals. Quart. Rev. Biol. 56, 1–16 (1981).
Gillooly, J. F., Charnov, E. L., West, G. B., Savage, V. M. & Brown, J. H. Effects of size and temperature on developmental time. Nature 417, 70–73 (2002).
McCoy, M. W. & Gillooly, J. F. Predicting natural mortality rates of plants and animals. Ecol. Lett. 11, 710–716 (2008).
Hatton, I. A. et al. The predator–prey power law: biomass scaling across terrestrial and aquatic biomes. Science 349, 1070–1070 (2015).
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).
Sibly, R. M., Brown, J. H. & Kodric-Brown, A. Metabolic Ecology: A Scaling Approach (John Wiley-Blackwell, Chichester, 2012).
Cummins, K. W. & Wuychek, J. C. Calorific equivalents for studies in ecological energetics. Int. Assoc. Theor. Appl. Limnol. 18, 1–158 (1967).
Brey, T., Rumohr, H. & Ankar, S. Energy content of macrobenthic invertebrates: general conversion factors from weight to energy. J. Exp. Mar. Biol. Ecol. 117, 271–278 (1988).
Humphreys, W. F. Production and respiration in animal populations. J. Anim. Ecol. 48, 427–453 (1979).
May, R. M. Production and respiration in animal communities. Nature 282, 443–444 (1979).
Charnov, E. L. & Berrigan, D. Why do female primates have such long lifespans and so few babies? Or life in the slow lane. Evol. Anthropol. 1, 191–194 (1993).
DeLong, J. P., Okie, J. G., Moses, M. E., Sibly, R. M. & Brown, J. H. Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life. Proc. Natl Acad. Sci. USA 107, 12941–12945 (2010).
Lynch, M. & Marinov, G. K. The bioenergetic costs of a gene. Proc. Natl Acad. Sci. USA 112, 15690–15695 (2015).
Corkrey, R. et al The biokinetic spectrum for temperature. PLoS. ONE 11, e0153343 (2016).
Williams, G. C. Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am. Nat. 100, 687–690 (1966).
Stearns, S. C. The Evolution of Life Histories (Oxford Univ. Press, Oxford, 1992).
Charnov, E. L. Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology (Oxford Univ. Press, Oxford, 1993).
Charnov, E. L., Warne, R. & Moses, M. Lifetime reproductive effort. Am. Nat. 170, E129–E142 (2007).
Ginzburg, L. R., Burger, O. & Damuth, J. The May threshold and life-history allometry. Biol. Lett. 6, 850–853 (2010).
Odum, H. T. & Pinkerton, R. C. Time’s speed regulator: the optimum efficiency for maximum power output in physical and biological systems. Am. Sci. 43, 331–343 (1955).
Odum, H. T. Environment, Power, and Society (Wiley-Interscience, New York, 1971).
Hall, C. A. S. Maximum power: The Ideas and Applications of H.T. Odum (Univ. Press Colorado, Boulder, 1995).
Payne, J. L. et al. Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity. Proc. Natl. Acad. Sci. USA 106, 24–27 (2009).
Van Valen, L. A new evolutionary law. Evol. Theor. 1, 1–30 (1973).
Tolkamp, B., Wall, E., Roehe, R., Newbold, J. & Zaralis, K. Review of Nutrient Efficiency in Different Breeds of Farm Livestock Report to DEFRA IF0183 (Haymarket SAC Publishing, Mumbai, 2010).
Hutchinson, G. E. Concluding remarks. Cold Spring Harb. Symp. Quant. Biol. 22, 415–427 (1957).
Hall, C. A. S., Stanford, J. A. & Hauer, F. R. The distribution and abundance of organisms as a consequence of energy balances along multiple environmental gradients. Oikos 65, 377–390 (1992).
Hall, C. A. S. Energy Return on Investment: A Unifying Principle for Biology, Economics and Sustainability (Springer, New York, 2017).
Brett, J. R. in Behavioral Energetics: The Cost of Survival in Vertebrates Vol. 2 (eds Aspey, W. P. & Lustick, S. I.) 29–63 (Ohio State Univ. Press, Columbus, 1983).
Nagy, K. A. Field metabolic rate and body size. J. Exp. Biol. 208, 1621–1625 (2005).
Sibly, R. M. & Calow, P. Ecological compensation—a complication for testing life history theory. J. Theor. Biol. 125, 177–186 (1987).
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.
The authors declare no competing financial interests.
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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.
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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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