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. GarwoodRobert 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

^*Corresponding author for this work

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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
Publication status	Published - Feb 2022

Bibliographical note

Copyright the Author(s) 2021. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

Keywords

Aging
senescence
sex chromosome
amphibians

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10.1111/evo.14410

Publisher version (open access)Final published version, 1.46 MBLicence: CC BY-NC

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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

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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, senescence, sex chromosome, amphibians",

author = "Hugo Cayuela and Jean-Fran{\c c}ois Lema{\^i}tre and Jean-Paul L{\'e}na 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 Jean-Michel Gaillard and Miller, {David A. W.}",

note = "Copyright the Author(s) 2021. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher. ",

year = "2022",

month = feb,

doi = "10.1111/evo.14410",

language = "English",

volume = "76",

pages = "346--356",

journal = "Evolution",

issn = "0014-3820",

publisher = "Wiley-Blackwell, Wiley",

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Cayuela, H, Lemaître, J-F, Léna, J-P, 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, J-M & 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.

N1 - Copyright the Author(s) 2021. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

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 - senescence

KW - sex chromosome

KW - amphibians

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U2 - 10.1111/evo.14410

DO - 10.1111/evo.14410

M3 - Article

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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

Abstract

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Keywords

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