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

doi:10.1111/evo.14410

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

Authors

H Cayuela

J-F Lemaitre

J-P Lena

V Ronget

I Martinez-Solano

E Muths

DS Piliod

BR Schmidt

G Sanchez-Montez

J Gutiérrez-Rodríguez

G Pyke

K Grossenbacher

O Lenzi

J Bosch

KH Beard

LL Woolbright

BA Lambert

DM Green

N Jreidini

JM Garwood

RN Fisher

K Matthews

D Dugeon

A Lau

J Speybroeck

R Homan

Dr Robert Jehle R.Jehle@salford.ac.uk
Associate Professor/Reader

E Başkale

E Mori

JW Arntzen

P Joly

RM Stiles

MJ Lanoo

JC Maerz

WH Lowe

A Valenzuela-Sánchez

DG Christiansen

C Angelini

JM Thirion

J Merilä

GR Colli

MM Vasconcellos

TCV Boas

IC Arantes

P Levionnois

BA Reinke

C Vieira

GAB Marais

JM Gaillard

DAW Miller

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.

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/