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The Evolution of Brain Size in Ectothermic Tetrapods: Large Brain Mass Trades-Off with Lifespan in Reptiles

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Abstract

The evolution of brain size is constrained by the trade-off between the energetic costs allocated towards its maintenance and the cognitive advantages that come with a larger brain, leading to a paradox. The cognitive benefits of larger brains (e.g., high behavioural flexibility) mitigate extrinsic mortality factors, which may indirectly select for slower ageing that prolongs lifespan (“cognitive buffer hypothesis”). However, substantial energetic costs imposed by the maintenance of neural tissue is expected to compromise the energetic budget of large-brained organisms, and their investment in somatic maintenance and repair, thus accelerating ageing that shortens lifespan (the “disposable soma theory”). The relationship between lifespan and brain size has mostly been investigated in birds and mammals. Thus, whether these trade-offs express across ectothermic vertebrates remains to be addressed on a large-scale. Our study presents the first large-scale analysis of the brain size-lifespan relationship in ectothermic tetrapods (amphibians and reptiles). Using a dataset spanning 265 species, we performed phylogenetic linear models to investigate the predicted trade-off between variation in brain size and longevity. Our findings revealed a negative relationship between brain size and lifespan across reptiles, whereas no association was observed across amphibians. Thus, the relationship between life history and brain evolution in ectotherms does not follow the general pattern found across other vertebrates. Among ectotherms, the high metabolic cost of producing neural tissue seems to transcend the cognitive benefits of evolving a larger brain. Consequently, our findings suggest that natural selection favours optimization of the energetic economy over the fitness-advantages that cognitive benefits may offer.

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Data Accessibility Statement

All data used in the analyses and the associated metadata are available in Appendix S1. All codes used in the analyses are available in Appendix S3. Both data and codes in R software will be stored in Dryad and data DOI will be included at the end of the article.

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Acknowledgements

We are grateful to Rachel Schwarz Stark and Simon Jamison for constructive discussion. We are also enormously grateful to Naomi Paz for English editing on an earlier draft of the manuscript.

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  1. School of Zoology, Faculty of Life Sciences, Tel Aviv University, 6997801, Tel Aviv, Israel

    Gavin Stark

  2. School of Biological Sciences, Queen’s University Belfast, 19 Chlorine Gardens, BT9 5DL, Belfast, United Kingdom

    Daniel Pincheira-Donoso

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GS and DPD conceived the idea, outlined the hypotheses to be addressed and collected the data; GS led the preparation of the manuscript, devise the hypotheses, and performed most of the statistical analysis. DPD contributed at all stages of manuscript preparation.

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Stark, G., Pincheira-Donoso, D. The Evolution of Brain Size in Ectothermic Tetrapods: Large Brain Mass Trades-Off with Lifespan in Reptiles. Evol Biol 49, 180–188 (2022). https://doi.org/10.1007/s11692-022-09562-4

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