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Developmental cost theory predicts thermal environment and vulnerability to global warming

Abstract

Metazoans must develop from zygotes to feeding organisms. In doing so, developing offspring consume up to 60% of the energy provided by their parent. The cost of development depends on two rates: metabolic rate, which determines the rate that energy is used; and developmental rate, which determines the length of the developmental period. Both development and metabolism are highly temperature-dependent such that developmental costs should be sensitive to the local thermal environment. Here, we develop, parameterize and test developmental cost theory, a physiologically explicit theory that reveals that ectotherms have narrow thermal windows in which developmental costs are minimized (Topt). Our developmental cost theory-derived estimates of Topt predict the natural thermal environment of 71 species across seven phyla remarkably well (R2 ~0.83). Developmental cost theory predicts that costs of development are much more sensitive to small changes in temperature than classic measures such as survival. Warming-driven changes to developmental costs are predicted to strongly affect population replenishment and developmental cost theory provides a mechanistic foundation for determining which species are most at risk. Developmental cost theory predicts that tropical aquatic species and most non-nesting terrestrial species are likely to incur the greatest increase in developmental costs from future warming.

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Fig. 1: Graphical representation of temperature-dependent developmental cost theory.
Fig. 2: Development costs across temperatures for developing ectotherms.
Fig. 3: Effect of developmental environment on mismatch between Topt and Tmid for 71 ectotherms.
Fig. 4: Change in performance associated with a 20% increase (relative to the range experienced by that species) in temperature relative to the thermal optimum.

Data availability

The data used in these meta-analyses are available from Dryad: https://doi.org/10.5061/dryad.zw3r2284x.

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Acknowledgements

We thank B. Comerford, M. Parascandalo and L. Morris for assistance. This work was supported by funding to the Centre for Geometric Biology, Monash University.

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D.J.M. conceived the study, collected and analysed the data and wrote the first draft. M.B. developed the mathematical theory. D.J.M. and A.K.P. collected the data. D.J.M. and C.R.W. analysed the data. All authors contributed to subsequent drafts.

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Correspondence to Dustin J. Marshall.

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The authors declare no competing interests.

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Supplementary Information

Supplementary text 1–3, Tables 1–4, Figs. 1–3 and references.

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Marshall, D.J., Pettersen, A.K., Bode, M. et al. Developmental cost theory predicts thermal environment and vulnerability to global warming. Nat Ecol Evol 4, 406–411 (2020). https://doi.org/10.1038/s41559-020-1114-9

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