Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women

Abstract

Evolutionary theory of senescence emphasizes the importance of intense selection on early reproduction owing to the declining force of natural selection with age that constrains lifespan. In humans, recent studies have, however, suggested that late-life mortality might be more closely related to late rather than early reproduction, although the role of late reproduction on fitness remains unclear. We examined the association between early and late reproduction with longevity in historical post-reproductive Sami women. We also estimated the strength of natural selection on early and late reproduction using path analysis, and the effect of reproductive timing on offspring survival to adulthood and maternal risk of dying at childbirth. We found that natural selection favoured both earlier start and later cessation of reproduction, and higher total fecundity. Maternal age at childbirth was not related to offspring or maternal survival. Interestingly, females who produced their last offspring at advanced age also lived longest, while age at first reproduction and total fecundity were unrelated to female longevity. Our results thus suggest that reproductive and somatic senescence may have been coupled in these human populations, and that selection could have favoured late reproduction. We discuss alternative hypotheses for the mechanisms which might have promoted the association between late reproduction and longevity.

Figure 1

Path model describing linear selection gradients (i.e. standardized partial regression coefficients) on age at last reproduction (ALR), age at first reproduction (AFR), mean inter-birth intervals (IBI), spouse’s age at death (SAAD) and total fecundity (FEC) on lifetime reproductive success (LRS) in historical post-reproductive Sami women. Single-headed arrows represent causal relationships, whereas double-headed arrows represent non-causal correlations between two variables. Positive selection gradients and correlations are shown in solid lines and negative selection gradients in dashed lines, and the thickness of each arrow represents the magnitude of that relationship. Insignificant selection gradients constrained to zero are omitted from the path model shown. R² values for total fecundity and lifetime reproductive success were 0.922 and 0.768, respectively. U denotes the unexplained error variation in dependent variables. (^***p < 0.0001, ^**p < 0.001, ^*p < 0.08). Goodness of fit: CFI = 0.999; NNFI = 0.997; χ² = 6.27; d.f. = 5; p > 0.28.

Figure 2

Estimated survival probability curves for post-reproductive Sami women as a function of age at last reproduction at age 35 (solid line), age 40 (dotted line) and age 45 (dashed line), adjusting for spouse’s age at death.