X*Y females exhibit steeper reproductive senescence in the African pygmy mouse

Abstract

A wave of studies has recently emphasized the influence of sex chromosomes on both lifespan and actuarial senescence patterns across vertebrates and invertebrates. Basically, the heterogametic sex (XY males in XX/XY systems or ZW females in ZW/ZZ systems) typically displays a lower lifespan and a steeper rate of actuarial senescence than the homogametic sex. However, whether these effects extend to the senescence patterns of other phenotypic traits or physiological functions is yet to be determined. Here, we investigated whether sex chromosomes modulate reproductive senescence using females from the African pygmy mouse (Mus minutoides). This biological model exhibits an odd sex determining system with a third, feminizing sex chromosome, X*, resulting in three distinct female genotypes (XX, X*X, or X*Y) that coexist in natural populations. We found that the rate of senescence in litter size at birth is much more pronounced in heterogametic X*Y females than in homogametic XX or X*X females that may support the unguarded X or toxic Y hypotheses and can be directly linked to the complex and unique X*Y phenotype. A decrease in neonatal survival with mother's age has also been found, but this decline is not different between the three female genotypes.

Keywords: Mus minutoides; litter size; neonatal survival; reproductive ageing.

Fig. 1.

Mean difference in litter size at birth (A), litter size at weaning (B), and neonatal survival (C) between females from the three genotypes.

Fig. 2.

Relationship between litter size at birth and maternal age for XX (A), X*X (B), and X*Y (C) females. The threshold value for X*Y females is 311 d and the threshold value for X*X females is 338 d. The figure (D) represents the differences in the rate of senescence in litter size at birth between the three female genotypes over the whole maternal lifespan (with the same color code as in A, B, and C).

Fig. 3.

Relationship between litter size at weaning and maternal age for XX (A), X*X (B), and X*Y (C) females. The threshold value for X*Y females is 251 d. The figure (D) represents the differences in the rate of senescence in litter size at weaning between the three female genotypes when maternal age varies between 42 and 251 d of age (with the same color code as in A, B, and C).

Fig. 4.

Relationship between neonatal survival and maternal age for each genotype. X*Y females are in blue, XX females are in green, and X*X females are in orange.