Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity

Beth A. Reinke; Hugo Cayuela; Fredric J. Janzen; Jean François Lemaître; Jean Michel Gaillard; A. Michelle Lawing; John B. Iverson; Ditte G. Christiansen; Iñigo Martínez-Solano; Gregorio Sánchez-Montes; Jorge Gutiérrez-Rodríguez; Francis L. Rose; Nicola Nelson; Susan Keall; Alain J. Crivelli; Theodoros Nazirides; Annegret Grimm-Seyfarth; Klaus Henle; Emiliano Mori; Gaëtan Guiller; Rebecca Homan; Anthony Olivier; Erin Muths; Blake R. Hossack; Xavier Bonnet; David S. Pilliod; Marieke Lettink; Tony Whitaker; Benedikt R. Schmidt; Michael G. Gardner; Marc Cheylan; Françoise Poitevin; Ana Golubović; Ljiljana Tomović; Dragan Arsovski; Richard A. Griffiths; Jan W. Arntzen; Jean Pierre Baron; Jean François Le Galliard; Thomas Tully; Luca Luiselli; Massimo Capula; Lorenzo Rugiero; Rebecca McCaffery; Lisa A. Eby; Venetia Briggs-Gonzalez; Frank Mazzotti; David Pearson; Brad A. Lambert; David M. Green; Nathalie Jreidini; Claudio Angelini; Graham Pyke; Jean Marc Thirion; Pierre Joly; Jean Paul Léna; Anton D. Tucker; Col Limpus; Pauline Priol; Aurélien Besnard; Pauline Bernard; Kristin Stanford; Richard King; Justin Garwood; Jaime Bosch; Franco L. Souza; Jaime Bertoluci; Shirley Famelli; Kurt Grossenbacher; Omar Lenzi; Kathleen Matthews; Sylvain Boitaud; Deanna H. Olson; Tim S. Jessop; Graeme R. Gillespie; Jean Clobert; Murielle Richard; Andrés Valenzuela-Sánchez; Gary M. Fellers; Patrick M. Kleeman; Brian J. Halstead; Evan H. Campbell Grant; Phillip G. Byrne; Thierry Frétey; Bernard Le Garff; Pauline Levionnois; John C. Maerz; Julian Pichenot; Kurtuluş Olgun; Nazan Üzüm; Aziz Avcı; Claude Miaud; Johan Elmberg; Gregory P. Brown; Richard Shine; Nathan F. Bendik; Lisa O'Donnell; Courtney L. Davis; Michael J. Lannoo; Rochelle M. Stiles; Robert M. Cox; Aaron M. Reedy; Daniel A. Warner; Eric Bonnaire; Kristine Grayson; Roberto Ramos-Targarona; Eyup Baskale; David Muñoz; John Measey; F. Andre de Villiers; Will Selman; Victor Ronget; Anne M. Bronikowski; David A.W. Miller

doi:10.1126/science.abm0151

Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity

Beth A. Reinke, Hugo Cayuela, Fredric J. Janzen, Jean François Lemaître, Jean Michel Gaillard, A. Michelle Lawing, John B. Iverson, Ditte G. Christiansen, Iñigo Martínez-Solano, Gregorio Sánchez-Montes, Jorge Gutiérrez-Rodríguez, Francis L. Rose, Nicola Nelson, Susan Keall, Alain J. Crivelli, Theodoros Nazirides, Annegret Grimm-Seyfarth, Klaus Henle, Emiliano Mori, Gaëtan GuillerRebecca Homan, Anthony Olivier, Erin Muths, Blake R. Hossack, Xavier Bonnet, David S. Pilliod, Marieke Lettink, Tony Whitaker, Benedikt R. Schmidt, Michael G. Gardner, Marc Cheylan, Françoise Poitevin, Ana Golubović, Ljiljana Tomović, Dragan Arsovski, Richard A. Griffiths, Jan W. Arntzen, Jean Pierre Baron, Jean François Le Galliard, Thomas Tully, Luca Luiselli, Massimo Capula, Lorenzo Rugiero, Rebecca McCaffery, Lisa A. Eby, Venetia Briggs-Gonzalez, Frank Mazzotti, David Pearson, Brad A. Lambert, David M. Green, Nathalie Jreidini, Claudio Angelini, Graham Pyke, Jean Marc Thirion, Pierre Joly, Jean Paul Léna, Anton D. Tucker, Col Limpus, Pauline Priol, Aurélien Besnard, Pauline Bernard, Kristin Stanford, Richard King, Justin Garwood, Jaime Bosch, Franco L. Souza, Jaime Bertoluci, Shirley Famelli, Kurt Grossenbacher, Omar Lenzi, Kathleen Matthews, Sylvain Boitaud, Deanna H. Olson, Tim S. Jessop, Graeme R. Gillespie, Jean Clobert, Murielle Richard, Andrés Valenzuela-Sánchez, Gary M. Fellers, Patrick M. Kleeman, Brian J. Halstead, Evan H. Campbell Grant, Phillip G. Byrne, Thierry Frétey, Bernard Le Garff, Pauline Levionnois, John C. Maerz, Julian Pichenot, Kurtuluş Olgun, Nazan Üzüm, Aziz Avcı, Claude Miaud, Johan Elmberg, Gregory P. Brown, Richard Shine, Nathan F. Bendik, Lisa O'Donnell, Courtney L. Davis, Michael J. Lannoo, Rochelle M. Stiles, Robert M. Cox, Aaron M. Reedy, Daniel A. Warner, Eric Bonnaire, Kristine Grayson, Roberto Ramos-Targarona, Eyup Baskale, David Muñoz, John Measey, F. Andre de Villiers, Will Selman, Victor Ronget, Anne M. Bronikowski, David A.W. Miller

Ecosystem Science and Management

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Abstract

Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.

Original language	English (US)
Pages (from-to)	1459-1466
Number of pages	8
Journal	Science
Volume	376
Issue number	6600
DOIs	https://doi.org/10.1126/science.abm0151
State	Published - Jun 24 2022

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10.1126/science.abm0151

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Reinke, B. A., Cayuela, H., Janzen, F. J., Lemaître, J. F., Gaillard, J. M., Lawing, A. M., Iverson, J. B., Christiansen, D. G., Martínez-Solano, I., Sánchez-Montes, G., Gutiérrez-Rodríguez, J., Rose, F. L., Nelson, N., Keall, S., Crivelli, A. J., Nazirides, T., Grimm-Seyfarth, A., Henle, K., Mori, E., ... Miller, D. A. W. (2022). Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity. Science, 376(6600), 1459-1466. https://doi.org/10.1126/science.abm0151

@article{101f32b91b8647cbb0b9f0ee7b3e5906,

title = "Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity",

abstract = "Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.",

author = "Reinke, {Beth A.} and Hugo Cayuela and Janzen, {Fredric J.} and Lema{\^i}tre, {Jean Fran{\c c}ois} and Gaillard, {Jean Michel} and Lawing, {A. Michelle} and Iverson, {John B.} and Christiansen, {Ditte G.} and I{\~n}igo Mart{\'i}nez-Solano and Gregorio S{\'a}nchez-Montes and Jorge Guti{\'e}rrez-Rodr{\'i}guez and Rose, {Francis L.} and Nicola Nelson and Susan Keall and Crivelli, {Alain J.} and Theodoros Nazirides and Annegret Grimm-Seyfarth and Klaus Henle and Emiliano Mori and Ga{\"e}tan Guiller and Rebecca Homan and Anthony Olivier and Erin Muths and Hossack, {Blake R.} and Xavier Bonnet and Pilliod, {David S.} and Marieke Lettink and Tony Whitaker and Schmidt, {Benedikt R.} and Gardner, {Michael G.} and Marc Cheylan and Fran{\c c}oise Poitevin and Ana Golubovi{\'c} and Ljiljana Tomovi{\'c} and Dragan Arsovski and Griffiths, {Richard A.} and Arntzen, {Jan W.} and Baron, {Jean Pierre} and {Le Galliard}, {Jean Fran{\c c}ois} and Thomas Tully and Luca Luiselli and Massimo Capula and Lorenzo Rugiero and Rebecca McCaffery and Eby, {Lisa A.} and Venetia Briggs-Gonzalez and Frank Mazzotti and David Pearson and Lambert, {Brad A.} and Green, {David M.} and Nathalie Jreidini and Claudio Angelini and Graham Pyke and Thirion, {Jean Marc} and Pierre Joly and L{\'e}na, {Jean Paul} and Tucker, {Anton D.} and Col Limpus and Pauline Priol and Aur{\'e}lien Besnard and Pauline Bernard and Kristin Stanford and Richard King and Justin Garwood and Jaime Bosch and Souza, {Franco L.} and Jaime Bertoluci and Shirley Famelli and Kurt Grossenbacher and Omar Lenzi and Kathleen Matthews and Sylvain Boitaud and Olson, {Deanna H.} and Jessop, {Tim S.} and Gillespie, {Graeme R.} and Jean Clobert and Murielle Richard and Andr{\'e}s Valenzuela-S{\'a}nchez and Fellers, {Gary M.} and Kleeman, {Patrick M.} and Halstead, {Brian J.} and {Campbell Grant}, {Evan H.} and Byrne, {Phillip G.} and Thierry Fr{\'e}tey and {Le Garff}, Bernard and Pauline Levionnois and Maerz, {John C.} and Julian Pichenot and Kurtulu{\c s} Olgun and Nazan {\"U}z{\"u}m and Aziz Avcı and Claude Miaud and Johan Elmberg and Brown, {Gregory P.} and Richard Shine and Bendik, {Nathan F.} and Lisa O'Donnell and Davis, {Courtney L.} and Lannoo, {Michael J.} and Stiles, {Rochelle M.} and Cox, {Robert M.} and Reedy, {Aaron M.} and Warner, {Daniel A.} and Eric Bonnaire and Kristine Grayson and Roberto Ramos-Targarona and Eyup Baskale and David Mu{\~n}oz and John Measey and {de Villiers}, {F. Andre} and Will Selman and Victor Ronget and Bronikowski, {Anne M.} and Miller, {David A.W.}",

note = "Publisher Copyright: Copyright {\textcopyright} 2022 The Authors",

year = "2022",

month = jun,

day = "24",

doi = "10.1126/science.abm0151",

language = "English (US)",

volume = "376",

pages = "1459--1466",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6600",

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Reinke, BA, Cayuela, H, Janzen, FJ, Lemaître, JF, Gaillard, JM, Lawing, AM, Iverson, JB, Christiansen, DG, Martínez-Solano, I, Sánchez-Montes, G, Gutiérrez-Rodríguez, J, Rose, FL, Nelson, N, Keall, S, Crivelli, AJ, Nazirides, T, Grimm-Seyfarth, A, Henle, K, Mori, E, Guiller, G, Homan, R, Olivier, A, Muths, E, Hossack, BR, Bonnet, X, Pilliod, DS, Lettink, M, Whitaker, T, Schmidt, BR, Gardner, MG, Cheylan, M, Poitevin, F, Golubović, A, Tomović, L, Arsovski, D, Griffiths, RA, Arntzen, JW, Baron, JP, Le Galliard, JF, Tully, T, Luiselli, L, Capula, M, Rugiero, L, McCaffery, R, Eby, LA, Briggs-Gonzalez, V, Mazzotti, F, Pearson, D, Lambert, BA, Green, DM, Jreidini, N, Angelini, C, Pyke, G, Thirion, JM, Joly, P, Léna, JP, Tucker, AD, Limpus, C, Priol, P, Besnard, A, Bernard, P, Stanford, K, King, R, Garwood, J, Bosch, J, Souza, FL, Bertoluci, J, Famelli, S, Grossenbacher, K, Lenzi, O, Matthews, K, Boitaud, S, Olson, DH, Jessop, TS, Gillespie, GR, Clobert, J, Richard, M, Valenzuela-Sánchez, A, Fellers, GM, Kleeman, PM, Halstead, BJ, Campbell Grant, EH, Byrne, PG, Frétey, T, Le Garff, B, Levionnois, P, Maerz, JC, Pichenot, J, Olgun, K, Üzüm, N, Avcı, A, Miaud, C, Elmberg, J, Brown, GP, Shine, R, Bendik, NF, O'Donnell, L, Davis, CL, Lannoo, MJ, Stiles, RM, Cox, RM, Reedy, AM, Warner, DA, Bonnaire, E, Grayson, K, Ramos-Targarona, R, Baskale, E, Muñoz, D, Measey, J, de Villiers, FA, Selman, W, Ronget, V, Bronikowski, AM & Miller, DAW 2022, 'Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity', Science, vol. 376, no. 6600, pp. 1459-1466. https://doi.org/10.1126/science.abm0151

TY - JOUR

T1 - Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity

AU - Reinke, Beth A.

AU - Cayuela, Hugo

AU - Janzen, Fredric J.

AU - Lemaître, Jean François

AU - Gaillard, Jean Michel

AU - Lawing, A. Michelle

AU - Iverson, John B.

AU - Christiansen, Ditte G.

AU - Martínez-Solano, Iñigo

AU - Sánchez-Montes, Gregorio

AU - Gutiérrez-Rodríguez, Jorge

AU - Rose, Francis L.

AU - Nelson, Nicola

AU - Keall, Susan

AU - Crivelli, Alain J.

AU - Nazirides, Theodoros

AU - Grimm-Seyfarth, Annegret

AU - Henle, Klaus

AU - Mori, Emiliano

AU - Guiller, Gaëtan

AU - Homan, Rebecca

AU - Olivier, Anthony

AU - Muths, Erin

AU - Hossack, Blake R.

AU - Bonnet, Xavier

AU - Pilliod, David S.

AU - Lettink, Marieke

AU - Whitaker, Tony

AU - Schmidt, Benedikt R.

AU - Gardner, Michael G.

AU - Cheylan, Marc

AU - Poitevin, Françoise

AU - Golubović, Ana

AU - Tomović, Ljiljana

AU - Arsovski, Dragan

AU - Griffiths, Richard A.

AU - Arntzen, Jan W.

AU - Baron, Jean Pierre

AU - Le Galliard, Jean François

AU - Tully, Thomas

AU - Luiselli, Luca

AU - Capula, Massimo

AU - Rugiero, Lorenzo

AU - McCaffery, Rebecca

AU - Eby, Lisa A.

AU - Briggs-Gonzalez, Venetia

AU - Mazzotti, Frank

AU - Pearson, David

AU - Lambert, Brad A.

AU - Green, David M.

AU - Jreidini, Nathalie

AU - Angelini, Claudio

AU - Pyke, Graham

AU - Thirion, Jean Marc

AU - Joly, Pierre

AU - Léna, Jean Paul

AU - Tucker, Anton D.

AU - Limpus, Col

AU - Priol, Pauline

AU - Besnard, Aurélien

AU - Bernard, Pauline

AU - Stanford, Kristin

AU - King, Richard

AU - Garwood, Justin

AU - Bosch, Jaime

AU - Souza, Franco L.

AU - Bertoluci, Jaime

AU - Famelli, Shirley

AU - Grossenbacher, Kurt

AU - Lenzi, Omar

AU - Matthews, Kathleen

AU - Boitaud, Sylvain

AU - Olson, Deanna H.

AU - Jessop, Tim S.

AU - Gillespie, Graeme R.

AU - Clobert, Jean

AU - Richard, Murielle

AU - Valenzuela-Sánchez, Andrés

AU - Fellers, Gary M.

AU - Kleeman, Patrick M.

AU - Halstead, Brian J.

AU - Campbell Grant, Evan H.

AU - Byrne, Phillip G.

AU - Frétey, Thierry

AU - Le Garff, Bernard

AU - Levionnois, Pauline

AU - Maerz, John C.

AU - Pichenot, Julian

AU - Olgun, Kurtuluş

AU - Üzüm, Nazan

AU - Avcı, Aziz

AU - Miaud, Claude

AU - Elmberg, Johan

AU - Brown, Gregory P.

AU - Shine, Richard

AU - Bendik, Nathan F.

AU - O'Donnell, Lisa

AU - Davis, Courtney L.

AU - Lannoo, Michael J.

AU - Stiles, Rochelle M.

AU - Cox, Robert M.

AU - Reedy, Aaron M.

AU - Warner, Daniel A.

AU - Bonnaire, Eric

AU - Grayson, Kristine

AU - Ramos-Targarona, Roberto

AU - Baskale, Eyup

AU - Muñoz, David

AU - Measey, John

AU - de Villiers, F. Andre

AU - Selman, Will

AU - Ronget, Victor

AU - Bronikowski, Anne M.

AU - Miller, David A.W.

PY - 2022/6/24

Y1 - 2022/6/24

N2 - Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.

AB - Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.

UR - http://www.scopus.com/inward/record.url?scp=85132684157&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85132684157&partnerID=8YFLogxK

U2 - 10.1126/science.abm0151

DO - 10.1126/science.abm0151

M3 - Article

C2 - 35737773

AN - SCOPUS:85132684157

SN - 0036-8075

VL - 376

SP - 1459

EP - 1466

JO - Science

JF - Science

IS - 6600

ER -

Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity

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