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

Hugo Cayuela·Jean-François Lemaître·Jean-Paul Léna·Victor Ronget·Inigo Martinez-Solano·Erin L. Muths·David S. Pilliod·Benedikt Schmidt·Gregorio Sanchez-Montes·Jorge Gutierrez-Rodriguez·Graham Pyke·Kurt Grossenbacher·Omar Lenzi·Jaime Bosch·Karen H. Beard·Lawrence L. Woolbright·Brad A. Lambert·David M. Green·Justin M Garwood·Robert N. Fisher·Kathleen Matthews·David Dudgeon·Anthony Lau·Jeroen Speybroeck·Rebecca Homan·Robert Jehle·Eyup Baskale·Emiliano Mori·Jan W. Arntzen·Pierre Joly·Rochelle Stiles·Michael J Lannoo·John C. Maerz·Winsor H. Lowe·Andres Valenzuela-Sanchez·Ditte Christianson·Claudio Angelini·Jean-Marc Thirion·Juha Merila·Guarino R. Colli·Mariana M. Vasconcellos·Taissa C. Boas·Isis da C. Arantes·Pauline Levionnois·Beth A. Reinke·Cristina Vieira·Gabriel A. B. Marais·Jean-Michael Gaillard·David A.W. Miller
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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.

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Hugo Cayuela, Jean-François Lemaître, Jean-Paul Léna, Victor Ronget, Inigo Martinez-Solano, Erin L. Muths, David S. Pilliod, Benedikt Schmidt, Gregorio Sanchez-Montes, Jorge Gutierrez-Rodriguez, Graham Pyke, Kurt Grossenbacher, Omar Lenzi, Jaime Bosch, Karen H. Beard, Lawrence L. Woolbright, Brad A. Lambert, David M. Green, Justin M Garwood, Robert N. Fisher, Kathleen Matthews, David Dudgeon, Anthony Lau, Jeroen Speybroeck, Rebecca Homan, Robert Jehle, Eyup Baskale, Emiliano Mori, Jan W. Arntzen, Pierre Joly, Rochelle Stiles, Michael J Lannoo, John C. Maerz, Winsor H. Lowe, Andres Valenzuela-Sanchez, Ditte Christianson, Claudio Angelini, Jean-Marc Thirion, Juha Merila, Guarino R. Colli, Mariana M. Vasconcellos, Taissa C. Boas, Isis da C. Arantes, Pauline Levionnois, Beth A. Reinke, Cristina Vieira, Gabriel A. B. Marais, Jean-Michael Gaillard, David A.W. Miller. 2022-01-07. Sex‐related differences in aging rate are associated with sex chromosome system in amphibians. https://doi.org/10.1111/evo.14410

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