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

Research output: Contribution to journalArticlepeer-review

7 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 languageEnglish (US)
Pages (from-to)346-356
Number of pages11
JournalEvolution
Volume76
Issue number2
DOIs
StatePublished - Feb 2022

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • General Agricultural and Biological Sciences

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