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
,
Rebecca Homan
(18)
,
Anthony Olivier
(14)
,
Erin Muths
(19)
,
Blake Hossack
(20)
,
Xavier Bonnet
(21)
,
David Pilliod
(22)
,
Marieke Lettink
(15)
,
Tony Whitaker
(15)
,
Benedikt R. Schmidt
(9)
,
Michael G. Gardner
(23, 24)
,
Marc Cheylan
(25)
,
Françoise Poitevin
(25)
,
Ana Golubovic
(26)
,
Ljiljana Tomović
(26)
,
Dragan Arsovski
(27)
,
Richard A. Griffiths
(28)
,
Jan W. Arntzen
(29)
,
Jean-Pierre Baron
(30)
,
Jean-François Le Galliard
(30, 31)
,
Thomas Tully
(31)
,
Luca Luiselli
(32, 33, 34)
,
Massimo Capula
(35)
,
Lorenzo Rugiero
(32)
,
Rebecca McCaffery
(36)
,
Lisa A. Eby
(37)
,
Venetia Briggs-Gonzalez
(38)
,
Frank Mazzotti
(39)
,
David Pearson
(40)
,
Brad A. Lambert
(41)
,
David M. Green
(42)
,
Nathalie Jreidini
(42)
,
Claudio Angelini
(15)
,
Graham Pyke
(43, 44)
,
Jean-Marc Thirion
(45)
,
Pierre Joly
(46)
,
Jean-Paul Léna
(46)
,
Anton D. Tucker
(40)
,
Col Limpus
(47)
,
Pauline Priol
(48)
,
Aurelien Besnard
(25)
,
Pauline Bernard
(49)
,
Kristin Stanford
(50)
,
Richard King
(51)
,
Justin Garwood
(52)
,
Jaime Bosch
(10, 53)
,
Franco L. Souza
(54)
,
Jaime Bertoluci
(55)
,
Shirley Famelli
(56, 57)
,
Kurt Grossenbacher
(58)
,
Omar Lenzi
(9)
,
Kathleen Matthews
(59)
,
Sylvain Boitaud
(60)
,
Deanna H. Olson
(59)
,
Tim S. Jessop
(61)
,
Graeme R. Gillespie
(62)
,
Jean Clobert
(63)
,
Murielle Richard
(63)
,
Andrés Valenzuela-Sánchez
(64, 65)
,
Gary M. Fellers
(66)
,
Patrick Kleeman
(66)
,
Brian Halstead
(66)
,
Evan H. Campbell Grant
(67)
,
Phillip G. Byrne
(68)
,
Thierry Frétey
(15)
,
Bernard Le Garff
(69)
,
Pauline Levionnois
(70)
,
John C. Maerz
(71)
,
Julian Pichenot
(72)
,
Kurtuluş Olgun
(73)
,
Nazan Üzüm
(73)
,
Aziz Avcı
(73)
,
Claude Miaud
(25)
,
Johan Elmberg
(74)
,
Gregory Brown
(44)
,
Richard Shine
(44)
,
Nathan F. Bendik
(75)
,
Lisa O’Donnell
(15)
,
Courtney L. Davis
(76)
,
Michael J. Lannoo
(77)
,
Rochelle M. Stiles
(15)
,
Robert M. Cox
(78)
,
Aaron M. Reedy
(78, 79)
,
Daniel A. Warner
(79)
,
Eric Bonnaire
(70)
,
Kristine Grayson
(80)
,
Roberto Ramos-Targarona
(81)
,
Eyup Baskale
(82)
,
David Muñoz
(2)
,
John Measey
(83)
,
F. Andre de Villiers
(83)
,
Will Selman
(84)
,
Victor Ronget
(85)
,
Anne M. Bronikowski
(4, 5)
,
David A. W. Miller
(2)
1
Northeastern Illinois University
2 Penn State - Pennsylvania State University
3 DEE - Department of Ecology and Evolution [UNIL, Lausanne] = Département d'écologie et évolution
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 IEU - 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 Denison University
19 US Geological Survey Lincoln]
20 University of Montana
21 CEBC - Centre d'Études Biologiques de Chizé - UMR 7372
22 FRESC - Forest and Rangeland Ecosystem Science Center
23 Flinders University [Adelaide, Australia]
24 SAM - South Australian Museum
25 CEFE - Centre d’Ecologie Fonctionnelle et Evolutive
26 University of Belgrade [Belgrade]
27 Macedonian Ecological Society
28 University of Kent [Canterbury]
29 Naturalis Biodiversity Center [Leiden]
30 CEREEP-Ecotron Ile de France (UMS 3194)
31 iEES Paris - Institut d'écologie et des sciences de l'environnement de Paris
32 Institute for Development, Ecology, Conservation and Cooperation [Rome, Italy]
33 Rivers State University of Science and Technology
34 Université de Lomé [Togo]
35 Museo Civico di Zoologia
36 U.S. Geological Survey
37 Wildlife Biology Program
38 UF - University of Florida [Gainesville]
39 Department of Wildlife Ecology and Conservation, University of Florida
40 Department of Biodiversity, Conservation and Attractions [Australia]
41 CSU - Colorado State University [Fort Collins]
42 Redpath Museum
43 KIB - Kunming Institute of Botany [CAS]
44 Macquarie University
45 OBIOS - Association Objectifs Biodiversités
46 E2C - Équipe 4 - Écophysiologie, Comportement, Conservation
47 CSIRO, EcoSciences Precinct
48 StatiPOP, scientific consulting
49 Conservatoire d'Espaces Naturels de Nouvelle-Aquitaine
50 OSU - Ohio State University [Columbus]
51 Northern Illinois University
52 California Department of Fish and Wildlife
53 Universidad de Oviedo = University of Oviedo
54 Department of Biology [Mato Grosso]
55 ESALQ - Escola Superior de Agricultura "Luiz de Queiroz"
56 RMIT University - Royal Melbourne Institute of Technology University
57 UHI - University of the Highlands and Islands
58 Naturhistorisches Museum [Bern]
59 USDA Forest Service Rocky Mountain Forest and Range Experiment Station
60 LEHNA - Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés
61 Deakin University [Waurn Ponds]
62 Palmerston North Research Centre
63 SETE - Station d'écologie théorique et expérimentale
64 Universidad Austral de Chile
65 ONG Ranita de Darwin
66 U.S Geological Survey
67 U.S. Geological Survey
68 School of Earth and Environmental Sciences [Wollongong]
69 UR - Université de Rennes
70 ONF - Office national des forêts
71 University of Georgia [USA]
72 2C2A-CERFE - Centre de Recherche et de Formation en Eco-éthologie
73 Adnan Menderes Üniversitesi
74 University College of Kristianstad
75 Watershed Protection Department
76 Cornell Laboratory of Ornithology
77 Indiana University School of Medicine
78 University of Virginia
79 AU - Auburn University
80 University of Richmond
81 CITMA - Ministerio de Ciencia, Tecnología y Medio Ambiente
82 Pamukkale University
83 Stellenbosch University
84 Millsaps College
85 EA - Éco-Anthropologie
2 Penn State - Pennsylvania State University
3 DEE - Department of Ecology and Evolution [UNIL, Lausanne] = Département d'écologie et évolution
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 IEU - 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 Denison University
19 US Geological Survey Lincoln]
20 University of Montana
21 CEBC - Centre d'Études Biologiques de Chizé - UMR 7372
22 FRESC - Forest and Rangeland Ecosystem Science Center
23 Flinders University [Adelaide, Australia]
24 SAM - South Australian Museum
25 CEFE - Centre d’Ecologie Fonctionnelle et Evolutive
26 University of Belgrade [Belgrade]
27 Macedonian Ecological Society
28 University of Kent [Canterbury]
29 Naturalis Biodiversity Center [Leiden]
30 CEREEP-Ecotron Ile de France (UMS 3194)
31 iEES Paris - Institut d'écologie et des sciences de l'environnement de Paris
32 Institute for Development, Ecology, Conservation and Cooperation [Rome, Italy]
33 Rivers State University of Science and Technology
34 Université de Lomé [Togo]
35 Museo Civico di Zoologia
36 U.S. Geological Survey
37 Wildlife Biology Program
38 UF - University of Florida [Gainesville]
39 Department of Wildlife Ecology and Conservation, University of Florida
40 Department of Biodiversity, Conservation and Attractions [Australia]
41 CSU - Colorado State University [Fort Collins]
42 Redpath Museum
43 KIB - Kunming Institute of Botany [CAS]
44 Macquarie University
45 OBIOS - Association Objectifs Biodiversités
46 E2C - Équipe 4 - Écophysiologie, Comportement, Conservation
47 CSIRO, EcoSciences Precinct
48 StatiPOP, scientific consulting
49 Conservatoire d'Espaces Naturels de Nouvelle-Aquitaine
50 OSU - Ohio State University [Columbus]
51 Northern Illinois University
52 California Department of Fish and Wildlife
53 Universidad de Oviedo = University of Oviedo
54 Department of Biology [Mato Grosso]
55 ESALQ - Escola Superior de Agricultura "Luiz de Queiroz"
56 RMIT University - Royal Melbourne Institute of Technology University
57 UHI - University of the Highlands and Islands
58 Naturhistorisches Museum [Bern]
59 USDA Forest Service Rocky Mountain Forest and Range Experiment Station
60 LEHNA - Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés
61 Deakin University [Waurn Ponds]
62 Palmerston North Research Centre
63 SETE - Station d'écologie théorique et expérimentale
64 Universidad Austral de Chile
65 ONG Ranita de Darwin
66 U.S Geological Survey
67 U.S. Geological Survey
68 School of Earth and Environmental Sciences [Wollongong]
69 UR - Université de Rennes
70 ONF - Office national des forêts
71 University of Georgia [USA]
72 2C2A-CERFE - Centre de Recherche et de Formation en Eco-éthologie
73 Adnan Menderes Üniversitesi
74 University College of Kristianstad
75 Watershed Protection Department
76 Cornell Laboratory of Ornithology
77 Indiana University School of Medicine
78 University of Virginia
79 AU - Auburn University
80 University of Richmond
81 CITMA - Ministerio de Ciencia, Tecnología y Medio Ambiente
82 Pamukkale University
83 Stellenbosch University
84 Millsaps College
85 EA - Éco-Anthropologie
Beth Reinke
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Hugo Cayuela
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Jean-François Lemaître
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Jean-Michel Gaillard
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Ditte Marie Christiansen
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Iñigo Martínez-Solano
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Alain J. Crivelli
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Annegret Grimm-Seyfarth
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Emiliano Mori
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Gaëtan Guiller
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Erin Muths
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Xavier Bonnet
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David Pilliod
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Marc Cheylan
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Jean-François Le Galliard
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Frank Mazzotti
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David Pearson
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Pierre Joly
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Aurelien Besnard
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Kurt Grossenbacher
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Jean Clobert
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Murielle Richard
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Andrés Valenzuela-Sánchez
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Résumé
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.
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