The long lives of primates and the ‘invariant rate of ageing’ hypothesis

Fernando Colchero; José Manuel Aburto; Elizabeth A. Archie; Christophe Boesch; Thomas Breuer; Fernando A. Campos; Anthony Collins; Dalia A. Conde; Marina Cords; Catherine Crockford; Melissa Emery Thompson; Linda M. Fedigan; Claudia Fichtel; Milou Groenenberg; Catherine Hobaiter; Peter M. Kappeler; Richard R. Lawler; Rebecca J. Lewis; Zarin P. Machanda; Marie L. Manguette; Martin N. Muller; Craig Packer; Richard J. Parnell; Susan Perry; Anne E. Pusey; Martha M. Robbins; Robert M. Seyfarth; Joan B. Silk; Johanna Staerk; Tara S. Stoinski; Emma J. Stokes; Karen B. Strier; Shirley C. Strum; Jenny Tung; Francisco Villavicencio; Roman M. Wittig; Richard W. Wrangham; Klaus Zuberbühler; James W. Vaupel; Susan C. Alberts

doi:10.1038/s41467-021-23894-3

The long lives of primates and the ‘invariant rate of ageing’ hypothesis

Fernando Colchero, José Manuel Aburto, Elizabeth A. Archie, Christophe Boesch, Thomas Breuer, Fernando A. Campos, Anthony Collins, Dalia A. Conde, Marina Cords, Catherine Crockford, Melissa Emery Thompson, Linda M. Fedigan, Claudia Fichtel, Milou Groenenberg, Catherine Hobaiter, Peter M. Kappeler, Richard R. Lawler, Rebecca J. Lewis, Zarin P. Machanda, Marie L. ManguetteMartin N. Muller, Craig Packer, Richard J. Parnell, Susan Perry, Anne E. Pusey, Martha M. Robbins, Robert M. Seyfarth, Joan B. Silk, Johanna Staerk, Tara S. Stoinski, Emma J. Stokes, Karen B. Strier, Shirley C. Strum, Jenny Tung, Francisco Villavicencio, Roman M. Wittig, Richard W. Wrangham, Klaus Zuberbühler, James W. Vaupel, Susan C. Alberts

Ecology, Evolution and Behavior

Research output: Contribution to journal › Article › peer-review

48 Scopus citations

Abstract

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the ‘invariant rate of ageing’ hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.

Original language	English (US)
Article number	3666
Journal	Nature communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-23894-3
State	Published - Dec 1 2021

Bibliographical note

Funding Information:
The governments of Botswana, Brazil, Costa Rica, Côte d’Ivoire, Kenya, Madagascar, Uganda, Republic of Congo, Rwanda and Tanzania provided permission for the primate field studies; all research complied with guidelines in the host countries. We thank the zoo and aquarium staff for manageing their animal records in Zoological Information Management System (ZIMS) and providing high quality demographic data for this project (Data Use Approval Number 82421). Duke University, Max Planck Institute of Demographic Research, and University of Southern Denmark provided logistical support. Annette Baudisch provided valuable feedback on the manuscript. This work was supported by NIA P01AG031719 to J.W.V. and S.C.A., with additional support provided by the Max Planck Institute of Demographic Research and the Duke University Population Research Institute.

Publisher Copyright:
© 2021, The Author(s).

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Colchero, F., Aburto, J. M., Archie, E. A., Boesch, C., Breuer, T., Campos, F. A., Collins, A., Conde, D. A., Cords, M., Crockford, C., Thompson, M. E., Fedigan, L. M., Fichtel, C., Groenenberg, M., Hobaiter, C., Kappeler, P. M., Lawler, R. R., Lewis, R. J., Machanda, Z. P., ... Alberts, S. C. (2021). The long lives of primates and the ‘invariant rate of ageing’ hypothesis. Nature communications, 12(1), Article 3666. https://doi.org/10.1038/s41467-021-23894-3

Colchero, F, Aburto, JM, Archie, EA, Boesch, C, Breuer, T, Campos, FA, Collins, A, Conde, DA, Cords, M, Crockford, C, Thompson, ME, Fedigan, LM, Fichtel, C, Groenenberg, M, Hobaiter, C, Kappeler, PM, Lawler, RR, Lewis, RJ, Machanda, ZP, Manguette, ML, Muller, MN, Packer, C, Parnell, RJ, Perry, S, Pusey, AE, Robbins, MM, Seyfarth, RM, Silk, JB, Staerk, J, Stoinski, TS, Stokes, EJ, Strier, KB, Strum, SC, Tung, J, Villavicencio, F, Wittig, RM, Wrangham, RW, Zuberbühler, K, Vaupel, JW & Alberts, SC 2021, 'The long lives of primates and the ‘invariant rate of ageing’ hypothesis', Nature communications, vol. 12, no. 1, 3666. https://doi.org/10.1038/s41467-021-23894-3

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title = "The long lives of primates and the {\textquoteleft}invariant rate of ageing{\textquoteright} hypothesis",

abstract = "Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the {\textquoteleft}invariant rate of ageing{\textquoteright} hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.",

author = "Fernando Colchero and Aburto, {Jos{\'e} Manuel} and Archie, {Elizabeth A.} and Christophe Boesch and Thomas Breuer and Campos, {Fernando A.} and Anthony Collins and Conde, {Dalia A.} and Marina Cords and Catherine Crockford and Thompson, {Melissa Emery} and Fedigan, {Linda M.} and Claudia Fichtel and Milou Groenenberg and Catherine Hobaiter and Kappeler, {Peter M.} and Lawler, {Richard R.} and Lewis, {Rebecca J.} and Machanda, {Zarin P.} and Manguette, {Marie L.} and Muller, {Martin N.} and Craig Packer and Parnell, {Richard J.} and Susan Perry and Pusey, {Anne E.} and Robbins, {Martha M.} and Seyfarth, {Robert M.} and Silk, {Joan B.} and Johanna Staerk and Stoinski, {Tara S.} and Stokes, {Emma J.} and Strier, {Karen B.} and Strum, {Shirley C.} and Jenny Tung and Francisco Villavicencio and Wittig, {Roman M.} and Wrangham, {Richard W.} and Klaus Zuberb{\"u}hler and Vaupel, {James W.} and Alberts, {Susan C.}",

note = "Funding Information: The governments of Botswana, Brazil, Costa Rica, C{\^o}te d{\textquoteright}Ivoire, Kenya, Madagascar, Uganda, Republic of Congo, Rwanda and Tanzania provided permission for the primate field studies; all research complied with guidelines in the host countries. We thank the zoo and aquarium staff for manageing their animal records in Zoological Information Management System (ZIMS) and providing high quality demographic data for this project (Data Use Approval Number 82421). Duke University, Max Planck Institute of Demographic Research, and University of Southern Denmark provided logistical support. Annette Baudisch provided valuable feedback on the manuscript. This work was supported by NIA P01AG031719 to J.W.V. and S.C.A., with additional support provided by the Max Planck Institute of Demographic Research and the Duke University Population Research Institute. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

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AU - Aburto, José Manuel

AU - Archie, Elizabeth A.

AU - Boesch, Christophe

AU - Breuer, Thomas

AU - Campos, Fernando A.

AU - Collins, Anthony

AU - Conde, Dalia A.

AU - Cords, Marina

AU - Crockford, Catherine

AU - Thompson, Melissa Emery

AU - Fedigan, Linda M.

AU - Fichtel, Claudia

AU - Groenenberg, Milou

AU - Hobaiter, Catherine

AU - Kappeler, Peter M.

AU - Lawler, Richard R.

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AU - Machanda, Zarin P.

AU - Manguette, Marie L.

AU - Muller, Martin N.

AU - Packer, Craig

AU - Parnell, Richard J.

AU - Perry, Susan

AU - Pusey, Anne E.

AU - Robbins, Martha M.

AU - Seyfarth, Robert M.

AU - Silk, Joan B.

AU - Staerk, Johanna

AU - Stoinski, Tara S.

AU - Stokes, Emma J.

AU - Strier, Karen B.

AU - Strum, Shirley C.

AU - Tung, Jenny

AU - Villavicencio, Francisco

AU - Wittig, Roman M.

AU - Wrangham, Richard W.

AU - Zuberbühler, Klaus

AU - Vaupel, James W.

AU - Alberts, Susan C.

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The long lives of primates and the ‘invariant rate of ageing’ hypothesis

Abstract

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