Sex-related differences in aging rate are associated with sex chromosome system in amphibians

Hugo Cayuela; Jean François Lemaître; Jean Paul Léna; Victor Ronget; Iñigo Martínez-Solano; Erin Muths; David S. Pilliod; Benedikt R. Schmidt; Gregorio Sánchez-Montes; Jorge Gutiérrez-Rodríguez; Graham Pyke; Kurt Grossenbacher; Omar Lenzi; Jaime Bosch; Karen H. Beard; Lawrence L. Woolbright; Brad A. Lambert; David M. Green; Nathalie Jreidini; Justin M. Garwood; Robert N. Fisher; Kathleen Matthews; David Dudgeon; Anthony Lau; Jeroen Speybroeck; Rebecca Homan; Robert Jehle; Eyup Başkale; Emiliano Mori; Jan W. Arntzen; Pierre Joly; Rochelle M. Stiles; Michael J. Lannoo; John C. Maerz; Winsor H. Lowe; Andrés Valenzuela-Sánchez; Ditte G. Christiansen; Claudio Angelini; Jean Marc Thirion; Juha Merilä; Guarino R. Colli; Mariana M. Vasconcellos; Taissa C.V. Boas; Ísis da C. Arantes; Pauline Levionnois; Beth A. Reinke; Cristina Vieira; Gabriel A.B. Marais; Jean Michel Gaillard; David A.W. Miller

doi:10.1111/evo.14410

Sex-related differences in aging rate are associated with sex chromosome system in amphibians

Hugo Cayuela
, Jean François Lemaître
, Jean Paul Léna
, Victor Ronget
, Iñigo Martínez-Solano
, Erin Muths
, David S. Pilliod
, Benedikt R. Schmidt
, Gregorio Sánchez-Montes
, Jorge Gutiérrez-Rodríguez
, Graham Pyke
, Kurt Grossenbacher
, Omar Lenzi
, Jaime Bosch
, Karen H. Beard
, Lawrence L. Woolbright
, Brad A. Lambert
, David M. Green
, Nathalie Jreidini
, Justin M. Garwood

Robert N. Fisher, Kathleen Matthews, David Dudgeon, Anthony Lau, Jeroen Speybroeck, Rebecca Homan, Robert Jehle, Eyup Başkale, Emiliano Mori, Jan W. Arntzen, Pierre Joly, Rochelle M. Stiles, Michael J. Lannoo, John C. Maerz, Winsor H. Lowe, Andrés Valenzuela-Sánchez, Ditte G. Christiansen, Claudio Angelini, Jean Marc Thirion, Juha Merilä, Guarino R. Colli, Mariana M. Vasconcellos, Taissa C.V. Boas, Ísis da C. Arantes, Pauline Levionnois, Beth A. Reinke, Cristina Vieira, Gabriel A.B. Marais, Jean Michel Gaillard, David A.W. Miller

Division of Biological and Biomedical Sciences

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

14 Scopus citations

Abstract

Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture–recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the “unguarded X/Z effect”) or repeat-rich Y/W chromosome (the “toxic Y/W effect”) could accelerate aging in the heterogametic sex in some vertebrate clades.

Original language	English
Pages (from-to)	346-356
Number of pages	11
Journal	Evolution
Volume	76
Issue number	2
DOIs	https://doi.org/10.1111/evo.14410
State	Published - Feb 2022

Funding

We thank researchers, technicians, and students as all everyone who contributed to collect the capture–recapture data used our study. We also thank Thomas Flatt (Associate Editor) and the three anonymous reviewers for their useful and constructive comments. HC was supported as a postdoctoral researcher by the Vanier-Banting postdoctoral fellowship program and the Swiss National Science Foundation (SNF grant number 31003A_182265). Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This manuscript is contribution #782 of the USGS Amphibian Research and Monitoring Initiative. We thank researchers, technicians, and students as all everyone who contributed to collect the capture–recapture data used our study. We also thank Thomas Flatt (Associate Editor) and the three anonymous reviewers for their useful and constructive comments. HC was supported as a postdoctoral researcher by the Vanier‐Banting postdoctoral fellowship program and the Swiss National Science Foundation (SNF grant number 31003A_182265). Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This manuscript is contribution #782 of the USGS Amphibian Research and Monitoring Initiative.

Funder number
31003A_182265

Keywords

Aging
amphibians
senescence
sex chromosome

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10.1111/evo.14410

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Cayuela, H., Lemaître, J. F., Léna, J. P., Ronget, V., Martínez-Solano, I., Muths, E., Pilliod, D. S., Schmidt, B. R., Sánchez-Montes, G., Gutiérrez-Rodríguez, J., Pyke, G., Grossenbacher, K., Lenzi, O., Bosch, J., Beard, K. H., Woolbright, L. L., Lambert, B. A., Green, D. M., Jreidini, N., ... Miller, D. A. W. (2022). Sex-related differences in aging rate are associated with sex chromosome system in amphibians. Evolution, 76(2), 346-356. https://doi.org/10.1111/evo.14410

@article{233cb669fbe8478e9d4990b9f66a6a28,

title = "Sex-related differences in aging rate are associated with sex chromosome system in amphibians",

abstract = "Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture–recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the “unguarded X/Z effect”) or repeat-rich Y/W chromosome (the “toxic Y/W effect”) could accelerate aging in the heterogametic sex in some vertebrate clades.",

keywords = "Aging, amphibians, senescence, sex chromosome",

author = "Hugo Cayuela and Lema{\^i}tre, \{Jean Fran{\c c}ois\} and L{\'e}na, \{Jean Paul\} and Victor Ronget and I{\~n}igo Mart{\'i}nez-Solano and Erin Muths and Pilliod, \{David S.\} and Schmidt, \{Benedikt R.\} and Gregorio S{\'a}nchez-Montes and Jorge Guti{\'e}rrez-Rodr{\'i}guez and Graham Pyke and Kurt Grossenbacher and Omar Lenzi and Jaime Bosch and Beard, \{Karen H.\} and Woolbright, \{Lawrence L.\} and Lambert, \{Brad A.\} and Green, \{David M.\} and Nathalie Jreidini and Garwood, \{Justin M.\} and Fisher, \{Robert N.\} and Kathleen Matthews and David Dudgeon and Anthony Lau and Jeroen Speybroeck and Rebecca Homan and Robert Jehle and Eyup Ba{\c s}kale and Emiliano Mori and Arntzen, \{Jan W.\} and Pierre Joly and Stiles, \{Rochelle M.\} and Lannoo, \{Michael J.\} and Maerz, \{John C.\} and Lowe, \{Winsor H.\} and Andr{\'e}s Valenzuela-S{\'a}nchez and Christiansen, \{Ditte G.\} and Claudio Angelini and Thirion, \{Jean Marc\} and Juha Meril{\"a} and Colli, \{Guarino R.\} and Vasconcellos, \{Mariana M.\} and Boas, \{Taissa C.V.\} and Arantes, \{{\'I}sis da C.\} and Pauline Levionnois and Reinke, \{Beth A.\} and Cristina Vieira and Marais, \{Gabriel A.B.\} and Gaillard, \{Jean Michel\} and Miller, \{David A.W.\}",

note = "Publisher Copyright: {\textcopyright} 2021 The Authors. Evolution {\textcopyright} 2021 The Society for the Study of Evolution.",

year = "2022",

month = feb,

doi = "10.1111/evo.14410",

language = "English",

volume = "76",

pages = "346--356",

journal = "Evolution",

issn = "0014-3820",

publisher = "Oxford University Press",

number = "2",

}

Cayuela, H, Lemaître, JF, Léna, JP, Ronget, V, Martínez-Solano, I, Muths, E, Pilliod, DS, Schmidt, BR, Sánchez-Montes, G, Gutiérrez-Rodríguez, J, Pyke, G, Grossenbacher, K, Lenzi, O, Bosch, J, Beard, KH, Woolbright, LL, Lambert, BA, Green, DM, Jreidini, N, Garwood, JM, Fisher, RN, Matthews, K, Dudgeon, D, Lau, A, Speybroeck, J, Homan, R, Jehle, R, Başkale, E, Mori, E, Arntzen, JW, Joly, P, Stiles, RM, Lannoo, MJ, Maerz, JC, Lowe, WH, Valenzuela-Sánchez, A, Christiansen, DG, Angelini, C, Thirion, JM, Merilä, J, Colli, GR, Vasconcellos, MM, Boas, TCV, Arantes, ÍDC, Levionnois, P, Reinke, BA, Vieira, C, Marais, GAB, Gaillard, JM & Miller, DAW 2022, 'Sex-related differences in aging rate are associated with sex chromosome system in amphibians', Evolution, vol. 76, no. 2, pp. 346-356. https://doi.org/10.1111/evo.14410

TY - JOUR

T1 - Sex-related differences in aging rate are associated with sex chromosome system in amphibians

AU - Cayuela, Hugo

AU - Lemaître, Jean François

AU - Léna, Jean Paul

AU - Ronget, Victor

AU - Martínez-Solano, Iñigo

AU - Muths, Erin

AU - Pilliod, David S.

AU - Schmidt, Benedikt R.

AU - Sánchez-Montes, Gregorio

AU - Gutiérrez-Rodríguez, Jorge

AU - Pyke, Graham

AU - Grossenbacher, Kurt

AU - Lenzi, Omar

AU - Bosch, Jaime

AU - Beard, Karen H.

AU - Woolbright, Lawrence L.

AU - Lambert, Brad A.

AU - Green, David M.

AU - Jreidini, Nathalie

AU - Garwood, Justin M.

AU - Fisher, Robert N.

AU - Matthews, Kathleen

AU - Dudgeon, David

AU - Lau, Anthony

AU - Speybroeck, Jeroen

AU - Homan, Rebecca

AU - Jehle, Robert

AU - Başkale, Eyup

AU - Mori, Emiliano

AU - Arntzen, Jan W.

AU - Joly, Pierre

AU - Stiles, Rochelle M.

AU - Lannoo, Michael J.

AU - Maerz, John C.

AU - Lowe, Winsor H.

AU - Valenzuela-Sánchez, Andrés

AU - Christiansen, Ditte G.

AU - Angelini, Claudio

AU - Thirion, Jean Marc

AU - Merilä, Juha

AU - Colli, Guarino R.

AU - Vasconcellos, Mariana M.

AU - Boas, Taissa C.V.

AU - Arantes, Ísis da C.

AU - Levionnois, Pauline

AU - Reinke, Beth A.

AU - Vieira, Cristina

AU - Marais, Gabriel A.B.

AU - Gaillard, Jean Michel

AU - Miller, David A.W.

PY - 2022/2

Y1 - 2022/2

N2 - Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture–recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the “unguarded X/Z effect”) or repeat-rich Y/W chromosome (the “toxic Y/W effect”) could accelerate aging in the heterogametic sex in some vertebrate clades.

AB - Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture–recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the “unguarded X/Z effect”) or repeat-rich Y/W chromosome (the “toxic Y/W effect”) could accelerate aging in the heterogametic sex in some vertebrate clades.

KW - Aging

KW - amphibians

KW - senescence

KW - sex chromosome

UR - https://www.scopus.com/pages/publications/85122512421

U2 - 10.1111/evo.14410

DO - 10.1111/evo.14410

M3 - Article

C2 - 34878663

AN - SCOPUS:85122512421

SN - 0014-3820

VL - 76

SP - 346

EP - 356

JO - Evolution

JF - Evolution

IS - 2

ER -

Sex-related differences in aging rate are associated with sex chromosome system in amphibians

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