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The decoupled nature of basal metabolic rate and body temperature in endotherm evolution


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The origins of endothermy in birds and mammals are important events in vertebrate evolution. Endotherms can maintain their body temperature (Tb) over a wide range of ambient temperatures primarily using the heat that is generated continuously by their high basal metabolic rate (BMR)1. There is also an important positive feedback loop as Tb influences BMR1,2,3. Owing to this interplay between BMRs and Tb, many ecologists and evolutionary physiologists posit that the evolution of BMR and Tb must have been coupled during the radiation of endotherms3,4,5, changing with similar trends6,7,8. However, colder historical environments might have imposed strong selective pressures on BMR to compensate for increased rates of heat loss and to keep Tb constant9,10,11,12. Thus, adaptation to cold ambient temperatures through increases in BMR could have decoupled BMR from Tb and caused different evolutionary routes to the modern diversity in these traits. Here we show that BMR and Tb were decoupled in approximately 90% of mammalian phylogenetic branches and 36% of avian phylogenetic branches. Mammalian BMRs evolved with rapid bursts but without a long-term directional trend, whereas Tb evolved mostly at a constant rate and towards colder bodies from a warmer-bodied common ancestor. Avian BMRs evolved predominantly at a constant rate and without a long-term directional trend, whereas Tb evolved with much greater rate heterogeneity and with adaptive evolution towards colder bodies. Furthermore, rapid shifts that lead to both increases and decreases in BMRs were linked to abrupt changes towards colder ambient temperatures—although only in mammals. Our results suggest that natural selection effectively exploited the diversity in mammalian BMRs under diverse, often-adverse historical thermal environments.

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Fig. 1: Possible evolutionary scenarios for BMR and Tb given their branch-wise rates in a bivariate space.
Fig. 2: Branch-wise rates of BMR, Tb and Ta on the mammalian and avian phylogeny.
Fig. 3: Branch-wise rates of BMR, Tb and Ta in bivariate space for mammals and birds.
Fig. 4: Mammals and birds evolved towards both colder Tb and Ta over their evolutionary history.

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No new data were generated for this study. The data used for this paper are available from the original sources cited in the Methods and Supplementary Information.

Change history

  • 23 August 2019

    Owing to a technical error, this Letter was not published online on 14 August 2019, as originally stated, and was instead first published online on 15 August 2019. The Letter has been corrected online.


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We thank C. O’Donovan, J. Baker, M. Sakamoto and A. N. Campoy for helpful discussion of the manuscript. A. Clarke supplied data for mammals and birds. This work is part of the PhD thesis of J.A.-L., supported by the CONICYT Doctoral Fellowship 21130943. C.V. was supported by the Leverhulme Trust (RPG-2013-185 and RPG-2017-071). C.E.H. and E.R.-S. were supported by FONDECYT grants 1170815 and 1170486.

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J.A.-L., C.E.H., E.R.-S. and C.V. contributed to all aspects of this work.

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Correspondence to Jorge Avaria-Llautureo or Chris Venditti.

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Peer review information Nature thanks Olaf Bininda-Emonds, Isabella Capellini and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Avaria-Llautureo, J., Hernández, C.E., Rodríguez-Serrano, E. et al. The decoupled nature of basal metabolic rate and body temperature in endotherm evolution. Nature 572, 651–654 (2019).

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