Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

Nature volume 572, pages 651–654 (2019)Cite this article

Subjects

This article has been updated

Abstract

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

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.

Data availability

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.

References

  1. Clarke, A. Principles of Thermal Ecology. Temperature, Energy and Life (Oxford Univ. Press, 2017)

  2. 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).

    Article  ADS  CAS  Google Scholar 

  3. Clarke, A. & Pörtner, H.-O. Temperature, metabolic power and the evolution of endothermy. Biol. Rev. Camb. Philos. Soc. 85, 703–727 (2010).

    PubMed  Google Scholar 

  4. Kemp, T. S. The origin of mammalian endothermy: a paradigm for the evolution of complex biological structure. Zool. J. Linn. Soc. 147, 473–488 (2006).

    Article  Google Scholar 

  5. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Towards a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Article  Google Scholar 

  6. Lovegrove, B. G. The evolution of endothermy in Cenozoic mammals: a plesiomorphic–apomorphic continuum. Biol. Rev. Camb. Philos. Soc. 87, 128–162 (2012).

    Article  Google Scholar 

  7. Lovegrove, B. G. The evolution of mammalian body temperature: the Cenozoic supraendothermic pulses. J. Comp. Physiol. B 182, 579–589 (2012).

    Article  Google Scholar 

  8. Lovegrove, B. G. A phenology of the evolution of endothermy in birds and mammals. Biol. Rev. Camb. Philos. Soc. 92, 1213–1240 (2017).

    Article  Google Scholar 

  9. Fristoe, T. S. et al. Metabolic heat production and thermal conductance are mass-independent adaptations to thermal environment in birds and mammals. Proc. Natl Acad. Sci. USA 112, 15934–15939 (2015).

    Article  ADS  CAS  Google Scholar 

  10. Naya, D. E., Naya, H. & White, C. R. On the interplay among ambient temperature, basal metabolic rate, and body mass. Am. Nat. 192, 518–524 (2018).

    Article  Google Scholar 

  11. White, C. R., Blackburn, T. M., Martin, G. R. & Butler, P. J. Basal metabolic rate of birds is associated with habitat temperature and precipitation, not primary productivity. Proc. R. Soc. Lond. B 274, 287–293 (2007).

    Article  Google Scholar 

  12. Jetz, W., Freckleton, R. P. & McKechnie, A. E. Environment, migratory tendency, phylogeny and basal metabolic rate in birds. PLoS ONE 3, e3261 (2008).

    Article  ADS  Google Scholar 

  13. Venditti, C., Meade, A. & Pagel, M. Multiple routes to mammalian diversity. Nature 479, 393–396 (2011).

    Article  ADS  CAS  Google Scholar 

  14. Rabosky, D. L. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE 9, e89543 (2014).

    Article  ADS  Google Scholar 

  15. Baker, J., Meade, A., Pagel, M. & Venditti, C. Adaptive evolution toward larger size in mammals. Proc. Natl Acad. Sci. USA 112, 5093–5098 (2015).

    Article  ADS  CAS  Google Scholar 

  16. Clarke, A., Rothery, P. & Isaac, N. J. B. Scaling of basal metabolic rate with body mass and temperature in mammals. J. Anim. Ecol. 79, 610–619 (2010).

    Article  Google Scholar 

  17. Baker, J., Meade, A., Pagel, M. & Venditti, C. Positive phenotypic selection inferred from phylogenies. Zool. J. Linn. Soc. 118, 95–115 (2016).

    Article  Google Scholar 

  18. Zachos, J., Pagani, M., Sloan, L., Thomas, E. & Billups, K. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693 (2001).

    Article  ADS  CAS  Google Scholar 

  19. Rolland, J. et al. The impact of endothermy on the climatic niche evolution and the distribution of vertebrate diversity. Nat. Ecol. Evol. 2, 459–464 (2018).

    Article  Google Scholar 

  20. Swanson, D. L., McKechnie, A. E. & Vézina, F. How low can you go? An adaptive energetic framework for interpreting basal metabolic rate variation in endotherms. J. Comp. Physiol. B 187, 1039–1056 (2017).

    Article  Google Scholar 

  21. Körtner, G., Brigham, R. M. & Geiser, F. Winter torpor in a large bird. Nature 407, 318 (2000).

    Article  ADS  Google Scholar 

  22. Crompton, A. W., Taylor, C. R. & Jagger, J. A. Evolution of homeothermy in mammals. Nature 272, 333–336 (1978).

    Article  ADS  CAS  Google Scholar 

  23. Bozinovic, F. & Pörtner, H.-O. Physiological ecology meets climate change. Ecol. Evol. 5, 1025–1030 (2015).

    Article  Google Scholar 

  24. Lieberman, B. S. & Dudgeon, S. An evaluation of stabilizing selection as a mechanism for stasis. Palaeogeogr. Palaeoclimatol. Palaeoecol. 127, 229–238 (1996).

    Article  Google Scholar 

  25. Fritz, S. A., Bininda-Emonds, O. R. & Purvis, A. Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics. Ecol. Lett. 12, 538–549 (2009).

    Article  Google Scholar 

  26. Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).

    Article  ADS  CAS  Google Scholar 

  27. Clarke, A. & Rothery, P. Scaling of body temperature in mammals and birds. Funct. Ecol. 22, 58–67 (2008).

    Google Scholar 

  28. Raftery, A. E. in Markov Chain Monte Carlo in Practice (eds Gilks, W. R. et al.) 163–187 (Chapman & Hall, 1996).

  29. Pagel, M., Meade, A. & Barker, D. Bayesian estimation of ancestral character states on phylogenies. Syst. Biol. 53, 673–684 (2004).

    Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. School of Biological Sciences, University of Reading, Reading, UK

    Jorge Avaria-Llautureo & Chris Venditti

  2. Centro de Investigación en Biodiversidad y Ambientes Sustentables (CIBAS), Facultad de Ciencias, Universidad Católica de la Santísima Concepción (UCSC), Concepción, Chile

    Jorge Avaria-Llautureo

  3. Laboratorio de Ecología Evolutiva y Filoinformática, Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile

    Cristián E. Hernández

  4. Laboratorio de Mastozoología, Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile

    Enrique Rodríguez-Serrano

Authors
  1. Jorge Avaria-Llautureo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristián E. Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enrique Rodríguez-Serrano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chris Venditti
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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

Corresponding authors

Correspondence to Jorge Avaria-Llautureo or Chris Venditti.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Supplementary information

Supplementary Information

This file contains Supplementary Text and Data and Supplementary Tables 1-17.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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). https://doi.org/10.1038/s41586-019-1476-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-019-1476-9

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing