Cayuela H et al. (2022), Sex-related differences in aging rate are assoc...

XB-ART-60826

Evolution 2022 Feb 01;762:346-356. doi: 10.1111/evo.14410.

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

Cayuela H , Lemaître JF , Léna JP , Ronget V , Martínez-Solano I , Muths E , Pilliod DS , Schmidt BR , Sánchez-Montes 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 , Dudgeon D , Lau A , Speybroeck J , Homan R , Jehle R , Başkale E , Mori E , Arntzen JW , Joly P , Stiles RM , Lannoo MJ , Maerz JC , Lowe WH , Valenzuela-Sánchez A , Christiansen DG , Angelini C , Thirion JM , Merilä J , Colli GR , Vasconcellos MM , Boas TCV , Arantes ÍDC , Levionnois P , Reinke BA , Vieira C , Marais GAB , Gaillard JM , Miller DAW .

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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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Figure 1Sex-specific variation in aging patterns and rates in 12 randomly selected species of amphibians with XY (panels A–F) and ZW (panels G–L) sex chromosome systems. Mortality curves of males and females are shown in blue and red, respectively. Aging patterns of the other species are presented in Supporting Information Figs. S4–S11.

Figure 2Sex chromosome system and sex-specific aging rate in 36 amphibian species. (A) Sex differences in aging rate across amphibians: for a given species, the sex difference was measured as the ratio [(male aging rate)/(female aging rate)]. (B) Bayesian stochastic mapping implemented in the R package phytools used to infer the sex chromosome system in species for which genetic sex-determination system was not documented (26 of 36 species)—Bayesian posterior probabilities for tips are provided in Supporting Information Table S2. We considered 111 amphibian species for which sex chromosome system documented in online databases (Tree of Sex Consortium 2014; Perkins et al. 2019) and recently published papers (Jeffries et al. 2018; Dufresnes et al. 2020). The 36 species considered in our study are mapped along the tree. 1: Bombina pachypus, 2: Bombina variegata, 3: Pelobates cultripes, 4: Pelobates fuscus, 5: Rana temporaria, 6: Rana luteiventris, 7: Rana cascadae, 8: Rana muscosa, 9: Rana sierrae, 10: Rana areolata, 11: Pelophylax esculentus, 12: Pelophylax caralitanus, 13: Pelophylax perezi, 14: Eleutherodactylus coqui, 15: Rhinoderma darwinii, 16: Litoria aurea, 17: Pseudacris maculata, 18: Hyla molleri, 19: Epidalea calamita, 20: Bufo spinosus, 21: Bufo bufo, 22: Rhinella schneideri, 23: Rhinella rubescens, 24: Anaxyrus fowleri, 25: Anaxyrus boreas, 26: Ambystoma maculatum, 27: Salamandra salamandra, 28: Pleurodeles waltl, 29: Paramesotriton hongkongensis, 30: Triturus marmoratus, 31: Triturus carnifex, 32: Triturus cristatus, 33: Notophthalmus viridescens, 34: Gyrinophilus porphyriticus, 35: Plethodon jordani, 36: Plethodon cinereus. (C) Variation of ratio [(male aging rate)/(female aging rate)] in XY and ZW systems. We also provide the posterior probability distribution (curve filled in gray) of the effect size for the sex chromosome system on the ratio [(male aging rate)/(female aging rate)] obtained from Bayesian univariate mixed models (mean estimates and 95% CI are shown in full and dashed lines, respectively). (D) Posterior probability distribution of aging rate in heterogametic (XY) and homogametic (ZZ) males from the bivariate mixed model; the posterior distribution probability on the left shows the effect size for sex chromosome system across males. (E) Posterior probability distribution of aging rate in heterogametic (ZW) and homogametic (XX) females from the bivariate mixed model; the posterior distribution probability on the left shows the effect size for sex chromosome system across females.