Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity
Beth Reinke
(1, 2)
,
Hugo Cayuela
(3)
,
Fredric J. Janzen
(4, 5)
,
Jean-François Lemaître
(6)
,
Jean-Michel Gaillard
(6)
,
A. Michelle Lawing
(7)
,
John B. Iverson
(8)
,
Ditte Marie Christiansen
(9)
,
Iñigo Martínez-Solano
(10)
,
Gregorio Sánchez-Montes
(10)
,
Jorge Gutiérrez-Rodríguez
(10, 11)
,
Francis L.R. Rose
(12)
,
Nicola Nelson
(13)
,
Susan Keall
(13)
,
Alain J. Crivelli
(14)
,
Theodoros Nazirides
(15)
,
Annegret Grimm-Seyfarth
(16)
,
Klaus Henle
(16)
,
Emiliano Mori
(17)
,
Gaëtan Guiller
(18)
,
Rebecca Homan
(19)
,
Anthony Olivier
(14)
,
Erin Muths
(20)
,
Blake Hossack
(21)
,
Xavier Bonnet
(22)
,
David Pilliod
(23)
,
Marieke Lettink
(15)
,
Tony Whitaker
(15)
,
Benedikt R. Schmidt
(9, 24)
,
Michael G. Gardner
(25, 26)
,
Marc Cheylan
(27)
,
Françoise Poitevin
(27)
,
Ana Golubovic
(28)
,
Ljiljana Tomović
(28)
,
Dragan Arsovski
(29)
,
Richard A. Griffiths
(30)
,
Jan W. Arntzen
(31)
,
Jean-Pierre Baron
(32)
,
Jean-François Le Galliard
(32, 33)
,
Thomas Tully
(33)
,
Luca Luiselli
(34, 35, 36)
,
Massimo Capula
(37)
,
Lorenzo Rugiero
(34)
,
Rebecca McCaffery
(38)
,
Lisa A. Eby
(39)
,
Venetia Briggs-Gonzalez
(40)
,
Frank Mazzotti
(40)
,
David Pearson
(41)
,
Brad A. Lambert
(42)
,
David M. Green
(43)
,
Nathalie Jreidini
(43)
,
Claudio Angelini
(15)
,
Graham Pyke
(44, 45)
,
Jean-Marc Thirion
(46)
,
Pierre Joly
(47)
,
Jean-Paul Léna
(47)
,
Anton D. Tucker
(41)
,
Col Limpus
(48)
,
Pauline Priol
(49)
,
Aurelien Besnard
(50)
,
Pauline Bernard
(51)
,
Kristin Stanford
(52)
,
Richard King
(53)
,
Justin Garwood
(54)
,
Jaime Bosch
(10, 55)
,
Franco L. Souza
(56)
,
Jaime Bertoluci
(57)
,
Shirley Famelli
(58, 59)
,
Kurt Grossenbacher
(60)
,
Omar Lenzi
(9)
,
Kathleen Matthews
(61)
,
Sylvain Boitaud
(62)
,
Deanna H. Olson
(61)
,
Tim S. Jessop
(63)
,
Graeme R. Gillespie
(64)
,
Jean Clobert
(65)
,
Murielle Richard
(65)
,
Andrés Valenzuela-Sánchez
(66, 67)
,
Gary M. Fellers
(68)
,
Patrick Kleeman
(68)
,
Brian Halstead
(68)
,
Evan H. Campbell Grant
(69)
,
Phillip G. Byrne
(70)
,
Thierry Frétey
(15)
,
Bernard Le Garff
(71)
,
Pauline Levionnois
(72)
,
John C. Maerz
(73)
,
Julian Pichenot
(74)
,
Kurtuluş Olgun
(75)
,
Nazan Üzüm
(75)
,
Aziz Avcı
(75)
,
Claude Miaud
(27)
,
Johan Elmberg
(76)
,
Gregory Brown
(45)
,
Richard Shine
(45)
,
Nathan F. Bendik
(77)
,
Lisa O’Donnell
(15)
,
Courtney L. Davis
(78)
,
Michael J. Lannoo
(79)
,
Rochelle M. Stiles
(15)
,
Robert M. Cox
(80)
,
Aaron M. Reedy
(80, 81)
,
Daniel A. Warner
(81)
,
Eric Bonnaire
(72)
,
Kristine Grayson
(82)
,
Roberto Ramos-Targarona
(83)
,
Eyup Baskale
(84)
,
David Muñoz
(2)
,
John Measey
(85)
,
F. Andre de Villiers
(85)
,
Will Selman
(86)
,
Victor Ronget
(87)
,
Anne M. Bronikowski
(4, 5)
,
David A. W. Miller
(2)
1
Northeastern Illinois University
2 Penn State - Pennsylvania State University
3 Department of Ecology and Evolution [Lausanne]
4 ISU - Iowa State University
5 KBS - W. K. Kellogg Biological Station
6 LBBE - Laboratoire de Biométrie et Biologie Evolutive - UMR 5558
7 Texas A&M University [College Station]
8 Earlham College
9 Department of Evolutionary Biology and Environmental Studies
10 MNCN - Museo Nacional de Ciencias Naturales [Madrid]
11 CSIC - Centro de Investigaciones Biológicas
12 Department of Biological Sciences [Lubbock]
13 School of Biological Sciences [Wellington, New Zealand]
14 Tour du Valat, Research Institute for the conservation of Mediterranean Wetlands
15 Auteur indépendant
16 Department of Conservation Biology [UFZ Leipzig]
17 IRET - Research Institute on Terrestrial Ecosystems [CNR, Italy]
18 Le Grand Momesson, Bouvron, France
19 Denison University
20 FORT - Fort Collins Science Center
21 University of Montana
22 CEBC - Centre d'Études Biologiques de Chizé - UMR 7372
23 FRESC - Forest and Rangeland Ecosystem Science Center
24 Info Fauna Karch 2000
25 Flinders University [Adelaide, Australia]
26 Evolutionary Biology Unit
27 UPVM - Université Paul-Valéry - Montpellier 3
28 University of Belgrade [Belgrade]
29 Macedonian Ecological Society
30 University of Kent [Canterbury]
31 Naturalis Biodiversity Center [Leiden]
32 CEREEP-Ecotron Ile de France (UMS 3194)
33 iEES Paris - Institut d'écologie et des sciences de l'environnement de Paris
34 Institute for Development, Ecology, Conservation and Cooperation [Rome, Italy]
35 Rivers State University of Science and Technology
36 Université de Lomé [Togo]
37 Museo Civico di Zoologia
38 U.S. Geological Survey
39 Wildlife Biology Program
40 Department of Wildlife Ecology and Conservation, University of Florida
41 Department of Biodiversity, Conservation and Attractions [Australia]
42 CSU - Colorado State University [Fort Collins]
43 Redpath Museum
44 KIB - Kunming Institute of Botany [CAS]
45 Macquarie University
46 OBIOS - Association Objectifs Biodiversités
47 E2C - Équipe 4 - Écophysiologie, Comportement, Conservation
48 CSIRO, EcoSciences Precinct
49 StatiPOP, scientific consulting
50 CEFE - Centre d’Ecologie Fonctionnelle et Evolutive
51 Conservatoire d'Espaces Naturels de Nouvelle-Aquitaine
52 OSU - Ohio State University [Columbus]
53 Northern Illinois University
54 California Department of Fish and Wildlife
55 Universidad de Oviedo [Oviedo]
56 Department of Biology [Mato Grosso]
57 ESALQ - Escola Superior de Agricultura "Luiz de Queiroz"
58 RMIT University - Royal Melbourne Institute of Technology University
59 UHI - University of the Highlands and Islands
60 Naturhistorisches Museum [Bern]
61 USDA Forest Service Rocky Mountain Forest and Range Experiment Station
62 LEHNA - Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés
63 Deakin University [Waurn Ponds]
64 Palmerston North Research Centre
65 SETE - Station d'écologie théorique et expérimentale
66 Universidad Austral de Chile
67 ONG Ranita de Darwin
68 U.S Geological Survey
69 U.S. Geological Survey
70 School of Earth and Environmental Sciences [Wollongong]
71 UR - Université de Rennes
72 ONF - Office national des forêts
73 University of Georgia [USA]
74 2C2A-CERFE - Centre de Recherche et de Formation en Eco-éthologie
75 Adnan Menderes Üniversitesi
76 University College of Kristianstad
77 Watershed Protection Department
78 Cornell Laboratory of Ornithology
79 Indiana University School of Medicine
80 University of Virginia
81 AU - Auburn University
82 University of Richmond
83 CITMA - Ministerio de Ciencia, Tecnología y Medio Ambiente
84 Pamukkale University
85 Stellenbosch University
86 Millsaps College
87 EA - Éco-Anthropologie
2 Penn State - Pennsylvania State University
3 Department of Ecology and Evolution [Lausanne]
4 ISU - Iowa State University
5 KBS - W. K. Kellogg Biological Station
6 LBBE - Laboratoire de Biométrie et Biologie Evolutive - UMR 5558
7 Texas A&M University [College Station]
8 Earlham College
9 Department of Evolutionary Biology and Environmental Studies
10 MNCN - Museo Nacional de Ciencias Naturales [Madrid]
11 CSIC - Centro de Investigaciones Biológicas
12 Department of Biological Sciences [Lubbock]
13 School of Biological Sciences [Wellington, New Zealand]
14 Tour du Valat, Research Institute for the conservation of Mediterranean Wetlands
15 Auteur indépendant
16 Department of Conservation Biology [UFZ Leipzig]
17 IRET - Research Institute on Terrestrial Ecosystems [CNR, Italy]
18 Le Grand Momesson, Bouvron, France
19 Denison University
20 FORT - Fort Collins Science Center
21 University of Montana
22 CEBC - Centre d'Études Biologiques de Chizé - UMR 7372
23 FRESC - Forest and Rangeland Ecosystem Science Center
24 Info Fauna Karch 2000
25 Flinders University [Adelaide, Australia]
26 Evolutionary Biology Unit
27 UPVM - Université Paul-Valéry - Montpellier 3
28 University of Belgrade [Belgrade]
29 Macedonian Ecological Society
30 University of Kent [Canterbury]
31 Naturalis Biodiversity Center [Leiden]
32 CEREEP-Ecotron Ile de France (UMS 3194)
33 iEES Paris - Institut d'écologie et des sciences de l'environnement de Paris
34 Institute for Development, Ecology, Conservation and Cooperation [Rome, Italy]
35 Rivers State University of Science and Technology
36 Université de Lomé [Togo]
37 Museo Civico di Zoologia
38 U.S. Geological Survey
39 Wildlife Biology Program
40 Department of Wildlife Ecology and Conservation, University of Florida
41 Department of Biodiversity, Conservation and Attractions [Australia]
42 CSU - Colorado State University [Fort Collins]
43 Redpath Museum
44 KIB - Kunming Institute of Botany [CAS]
45 Macquarie University
46 OBIOS - Association Objectifs Biodiversités
47 E2C - Équipe 4 - Écophysiologie, Comportement, Conservation
48 CSIRO, EcoSciences Precinct
49 StatiPOP, scientific consulting
50 CEFE - Centre d’Ecologie Fonctionnelle et Evolutive
51 Conservatoire d'Espaces Naturels de Nouvelle-Aquitaine
52 OSU - Ohio State University [Columbus]
53 Northern Illinois University
54 California Department of Fish and Wildlife
55 Universidad de Oviedo [Oviedo]
56 Department of Biology [Mato Grosso]
57 ESALQ - Escola Superior de Agricultura "Luiz de Queiroz"
58 RMIT University - Royal Melbourne Institute of Technology University
59 UHI - University of the Highlands and Islands
60 Naturhistorisches Museum [Bern]
61 USDA Forest Service Rocky Mountain Forest and Range Experiment Station
62 LEHNA - Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés
63 Deakin University [Waurn Ponds]
64 Palmerston North Research Centre
65 SETE - Station d'écologie théorique et expérimentale
66 Universidad Austral de Chile
67 ONG Ranita de Darwin
68 U.S Geological Survey
69 U.S. Geological Survey
70 School of Earth and Environmental Sciences [Wollongong]
71 UR - Université de Rennes
72 ONF - Office national des forêts
73 University of Georgia [USA]
74 2C2A-CERFE - Centre de Recherche et de Formation en Eco-éthologie
75 Adnan Menderes Üniversitesi
76 University College of Kristianstad
77 Watershed Protection Department
78 Cornell Laboratory of Ornithology
79 Indiana University School of Medicine
80 University of Virginia
81 AU - Auburn University
82 University of Richmond
83 CITMA - Ministerio de Ciencia, Tecnología y Medio Ambiente
84 Pamukkale University
85 Stellenbosch University
86 Millsaps College
87 EA - Éco-Anthropologie
Beth Reinke
Connectez-vous pour contacter l'auteur
- Function : Correspondent author
- PersonId : 1144714
- ORCID : 0000-0002-9620-001X
Connectez-vous pour contacter l'auteur
Hugo Cayuela
- Function : Author
- PersonId : 995434
- ORCID : 0000-0002-3529-0736
Jean-François Lemaître
- Function : Author
- PersonId : 21692
- IdHAL : jean-francois-lemaitre
- ORCID : 0000-0001-9898-2353
- IdRef : 199291675
Jean-Michel Gaillard
- Function : Author
- PersonId : 178430
- IdHAL : jean-michel-gaillard
- ORCID : 0000-0003-0174-8451
- IdRef : 033762406
Ditte Marie Christiansen
- Function : Author
- PersonId : 797305
- ORCID : 0000-0002-7020-5082
Iñigo Martínez-Solano
- Function : Author
- PersonId : 805092
- ORCID : 0000-0002-2260-226X
Alain J. Crivelli
- Function : Author
- PersonId : 855725
Annegret Grimm-Seyfarth
- Function : Author
- PersonId : 1016791
Emiliano Mori
- Function : Author
- PersonId : 781203
- ORCID : 0000-0001-8108-7950
Erin Muths
- Function : Author
- PersonId : 799923
- ORCID : 0000-0002-5498-3132
Xavier Bonnet
- Function : Author
- PersonId : 843791
- IdHAL : xavier-bonnet
- ORCID : 0000-0001-6150-8199
David Pilliod
- Function : Author
- PersonId : 797053
- ORCID : 0000-0003-4207-3518
Marc Cheylan
- Function : Author
- PersonId : 762516
- ORCID : 0000-0001-7594-571X
Jean-François Le Galliard
- Function : Author
- PersonId : 175128
- IdHAL : jean-francois-le-galliard
- ORCID : 0000-0002-5965-9868
- IdRef : 081800185
Frank Mazzotti
- Function : Author
- PersonId : 1019602
David Pearson
- Function : Author
- PersonId : 839806
Pierre Joly
- Function : Author
- PersonId : 952919
Kurt Grossenbacher
- Function : Author
- PersonId : 818029
- ORCID : 0000-0003-3844-2720
Jean Clobert
- Function : Author
- PersonId : 756795
- ORCID : 0000-0001-5238-4331
Murielle Richard
- Function : Author
- PersonId : 756768
- ORCID : 0000-0003-2135-8194
Andrés Valenzuela-Sánchez
- Function : Author
- PersonId : 1044223
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.