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

Cayuela, H; Lemaitre, J-F; Lena, J-P; Ronget, V; Martinez-Solano, I; Muths, E; Piliod, DS; Schmidt, BR; Sanchez-Montez, 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; Dugeon, D; Lau, A; Speybroeck, J; Homan, R; Jehle, R; Başkale, E; Mori, E; Arntzen, JW; Joly, P; Stiles, RM; Lanoo, MJ; Maerz, JC; Lowe, WH; Valenzuela-Sánchez, A; Christiansen, DG; Angelini, C; Thirion, JM; Merilä, J; Colli, GR; Vasconcellos, MM; Boas, TCV; Arantes, IC; Levionnois, P; Reinke, BA; Vieira, C; Marais, GAB; Gaillard, JM; Miller, DAW

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 influences 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 were 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.

Citation

Cayuela, H., Lemaitre, J., Lena, J., Ronget, V., Martinez-Solano, I., Muths, E., …Miller, D. (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

• Journal Article Type: Article
• Acceptance Date: Nov 16, 2021
• Online Publication Date: Dec 8, 2021
• Publication Date: Feb 15, 2022
• Deposit Date: Dec 9, 2021
• Publicly Available Date: Jan 8, 2022
• Journal: Evolution
• Print ISSN: 0014-3820
• Electronic ISSN: 1558-5646
• Publisher: Wiley
• Volume: 76
• Issue: 2
• Pages: 346-356
• DOI: https://doi.org/10.1111/evo.14410
• Publisher URL: https://doi.org/10.1111/evo.14410
• Related Public URLs: http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1558-5646/