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

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 cla...

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Autores principales: Cayuela, Hugo, Lemaître, Jean‐François, Léna, Jean‐Paul, Ronget, Victor, Martínez‐Solano, Iñigo, Muths, Erin, Pilliod, David S., Schmidt, Benedikt R., Sánchez‐Montes, Gregorio, Gutiérrez‐Rodríguez, Jorge, Pyke, Graham, Grossenbacher, Kurt, Lenzi, Omar, Bosch, Jaime, Beard, Karen H., Woolbright, Lawrence L., Lambert, Brad A., Green, David M., Jreidini, Nathalie, Garwood, Justin M., Fisher, Robert N., Matthews, Kathleen, Dudgeon, David, Lau, Anthony, Speybroeck, Jeroen, Homan, Rebecca, Jehle, Robert, Başkale, Eyup, Mori, Emiliano, Arntzen, Jan W., Joly, Pierre, Stiles, Rochelle M., Lannoo, Michael J., Maerz, John C., Lowe, Winsor H., Valenzuela‐Sánchez, Andrés, Christiansen, Ditte G., Angelini, Claudio, Thirion, Jean‐Marc, Merilä, Juha, Colli, Guarino R., Vasconcellos, Mariana M., Boas, Taissa C. V., Arantes, Ísis da C., Levionnois, Pauline, Reinke, Beth A., Vieira, Cristina, Marais, Gabriel A. B., Gaillard, Jean‐Michel, Miller, David A. W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9304222/
https://www.ncbi.nlm.nih.gov/pubmed/34878663
http://dx.doi.org/10.1111/evo.14410
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author Cayuela, Hugo
Lemaître, Jean‐François
Léna, Jean‐Paul
Ronget, Victor
Martínez‐Solano, Iñigo
Muths, Erin
Pilliod, David S.
Schmidt, Benedikt R.
Sánchez‐Montes, Gregorio
Gutiérrez‐Rodríguez, Jorge
Pyke, Graham
Grossenbacher, Kurt
Lenzi, Omar
Bosch, Jaime
Beard, Karen H.
Woolbright, Lawrence L.
Lambert, Brad A.
Green, David M.
Jreidini, Nathalie
Garwood, Justin M.
Fisher, Robert N.
Matthews, Kathleen
Dudgeon, David
Lau, Anthony
Speybroeck, Jeroen
Homan, Rebecca
Jehle, Robert
Başkale, Eyup
Mori, Emiliano
Arntzen, Jan W.
Joly, Pierre
Stiles, Rochelle M.
Lannoo, Michael J.
Maerz, John C.
Lowe, Winsor H.
Valenzuela‐Sánchez, Andrés
Christiansen, Ditte G.
Angelini, Claudio
Thirion, Jean‐Marc
Merilä, Juha
Colli, Guarino R.
Vasconcellos, Mariana M.
Boas, Taissa C. V.
Arantes, Ísis da C.
Levionnois, Pauline
Reinke, Beth A.
Vieira, Cristina
Marais, Gabriel A. B.
Gaillard, Jean‐Michel
Miller, David A. W.
author_facet Cayuela, Hugo
Lemaître, Jean‐François
Léna, Jean‐Paul
Ronget, Victor
Martínez‐Solano, Iñigo
Muths, Erin
Pilliod, David S.
Schmidt, Benedikt R.
Sánchez‐Montes, Gregorio
Gutiérrez‐Rodríguez, Jorge
Pyke, Graham
Grossenbacher, Kurt
Lenzi, Omar
Bosch, Jaime
Beard, Karen H.
Woolbright, Lawrence L.
Lambert, Brad A.
Green, David M.
Jreidini, Nathalie
Garwood, Justin M.
Fisher, Robert N.
Matthews, Kathleen
Dudgeon, David
Lau, Anthony
Speybroeck, Jeroen
Homan, Rebecca
Jehle, Robert
Başkale, Eyup
Mori, Emiliano
Arntzen, Jan W.
Joly, Pierre
Stiles, Rochelle M.
Lannoo, Michael J.
Maerz, John C.
Lowe, Winsor H.
Valenzuela‐Sánchez, Andrés
Christiansen, Ditte G.
Angelini, Claudio
Thirion, Jean‐Marc
Merilä, Juha
Colli, Guarino R.
Vasconcellos, Mariana M.
Boas, Taissa C. V.
Arantes, Ísis da C.
Levionnois, Pauline
Reinke, Beth A.
Vieira, Cristina
Marais, Gabriel A. B.
Gaillard, Jean‐Michel
Miller, David A. W.
author_sort Cayuela, Hugo
collection PubMed
description 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.
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spelling pubmed-93042222022-07-28 Sex‐related differences in aging rate are associated with sex chromosome system in amphibians Cayuela, Hugo Lemaître, Jean‐François Léna, Jean‐Paul Ronget, Victor Martínez‐Solano, Iñigo Muths, Erin Pilliod, David S. Schmidt, Benedikt R. Sánchez‐Montes, Gregorio Gutiérrez‐Rodríguez, Jorge Pyke, Graham Grossenbacher, Kurt Lenzi, Omar Bosch, Jaime Beard, Karen H. Woolbright, Lawrence L. Lambert, Brad A. Green, David M. Jreidini, Nathalie Garwood, Justin M. Fisher, Robert N. Matthews, Kathleen Dudgeon, David Lau, Anthony Speybroeck, Jeroen Homan, Rebecca Jehle, Robert Başkale, Eyup Mori, Emiliano Arntzen, Jan W. Joly, Pierre Stiles, Rochelle M. Lannoo, Michael J. Maerz, John C. Lowe, Winsor H. Valenzuela‐Sánchez, Andrés Christiansen, Ditte G. Angelini, Claudio Thirion, Jean‐Marc Merilä, Juha Colli, Guarino R. Vasconcellos, Mariana M. Boas, Taissa C. V. Arantes, Ísis da C. Levionnois, Pauline Reinke, Beth A. Vieira, Cristina Marais, Gabriel A. B. Gaillard, Jean‐Michel Miller, David A. W. Evolution Original Articles 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. John Wiley and Sons Inc. 2022-01-07 2022-02 /pmc/articles/PMC9304222/ /pubmed/34878663 http://dx.doi.org/10.1111/evo.14410 Text en © 2021 The Authors. Evolution © 2021 The Society for the Study of Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Original Articles
Cayuela, Hugo
Lemaître, Jean‐François
Léna, Jean‐Paul
Ronget, Victor
Martínez‐Solano, Iñigo
Muths, Erin
Pilliod, David S.
Schmidt, Benedikt R.
Sánchez‐Montes, Gregorio
Gutiérrez‐Rodríguez, Jorge
Pyke, Graham
Grossenbacher, Kurt
Lenzi, Omar
Bosch, Jaime
Beard, Karen H.
Woolbright, Lawrence L.
Lambert, Brad A.
Green, David M.
Jreidini, Nathalie
Garwood, Justin M.
Fisher, Robert N.
Matthews, Kathleen
Dudgeon, David
Lau, Anthony
Speybroeck, Jeroen
Homan, Rebecca
Jehle, Robert
Başkale, Eyup
Mori, Emiliano
Arntzen, Jan W.
Joly, Pierre
Stiles, Rochelle M.
Lannoo, Michael J.
Maerz, John C.
Lowe, Winsor H.
Valenzuela‐Sánchez, Andrés
Christiansen, Ditte G.
Angelini, Claudio
Thirion, Jean‐Marc
Merilä, Juha
Colli, Guarino R.
Vasconcellos, Mariana M.
Boas, Taissa C. V.
Arantes, Ísis da C.
Levionnois, Pauline
Reinke, Beth A.
Vieira, Cristina
Marais, Gabriel A. B.
Gaillard, Jean‐Michel
Miller, David A. W.
Sex‐related differences in aging rate are associated with sex chromosome system in amphibians
title Sex‐related differences in aging rate are associated with sex chromosome system in amphibians
title_full Sex‐related differences in aging rate are associated with sex chromosome system in amphibians
title_fullStr Sex‐related differences in aging rate are associated with sex chromosome system in amphibians
title_full_unstemmed Sex‐related differences in aging rate are associated with sex chromosome system in amphibians
title_short Sex‐related differences in aging rate are associated with sex chromosome system in amphibians
title_sort sex‐related differences in aging rate are associated with sex chromosome system in amphibians
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9304222/
https://www.ncbi.nlm.nih.gov/pubmed/34878663
http://dx.doi.org/10.1111/evo.14410
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