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 MURTHS, 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

Research output: Journal PublicationsJournal Article (refereed)peer-review

1 Citation (Scopus)

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.
Original languageEnglish
Pages (from-to)346-356
Number of pages11
JournalEvolution; international journal of organic evolution
Volume76
Issue number2
Early online date8 Dec 2021
DOIs
Publication statusPublished - Feb 2022

Bibliographical note

Funding Information:
We thank researchers, technicians, and students as all everyone who contributed to collect the capture?recapture data used our study. We also thank Thomas Flatt (Associate Editor) and the three anonymous reviewers for their useful and constructive comments. HC was supported as a postdoctoral researcher by the Vanier-Banting postdoctoral fellowship program and the Swiss National Science Foundation (SNF grant number 31003A_182265). Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This manuscript is contribution #782 of the USGS Amphibian Research and Monitoring Initiative.

Funding Information:
We thank researchers, technicians, and students as all everyone who contributed to collect the capture–recapture data used our study. We also thank Thomas Flatt (Associate Editor) and the three anonymous reviewers for their useful and constructive comments. HC was supported as a postdoctoral researcher by the Vanier‐Banting postdoctoral fellowship program and the Swiss National Science Foundation (SNF grant number 31003A_182265). Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This manuscript is contribution #782 of the USGS Amphibian Research and Monitoring Initiative.

Publisher Copyright:
© 2021 The Authors. Evolution © 2021 The Society for the Study of Evolution.

Keywords

  • Aging
  • amphibians
  • senescence
  • sex chromosome

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