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Evolutionary theory suggests that natural selection should synchronize senescence of reproductive and somatic systems. In some species, females show dramatic discordance in senescence rates in these systems, leading to a clear menopause coupled with prolonged postreproductive life span. The Mother Hypothesis proposes that menopause evolved to avoid higher reproductive-mediated mortality risk in late-life and ensure the survival of existing offspring. Despite substantial theoretical interest, the critical predictions of this hypothesis have never been fully tested in populations with natural fertility and mortality. Here, we provide an extensive test, investigating both short- and long-term consequences of mother loss for offspring, using multigenerational demographic datasets of premodern Finns and Canadians. We found no support for the Mother Hypothesis. First, although the risk of maternal death from childbirth increased from middle age, the risk only reached 1-2% at age 50 and was predicted to range between 2% and 8% by 70. Second, offspring were adversely affected by maternal loss only in their first two years (i.e., preweaning), having reduced survival probability in early childhood as well as ultimate life span and fitness. Dependent offspring were not affected by maternal death following weaning, either in the short- or long-term. We suggest that although mothers are required to ensure offspring survival preweaning in humans, maternal loss thereafter can be compensated by other family members. Our results indicate that maternal effects on dependent offspring are unlikely to explain the maintenance of menopause or prolonged postreproductive life span in women., (© 2010 The Author(s). Evolution© 2010 The Society for the Study of Evolution.)

Most animals reproduce until they die, but in humans, females can survive long after ceasing reproduction. In theory, a prolonged post-reproductive lifespan will evolve when females can gain greater fitness by increasing the success of their offspring than by continuing to breed themselves. Although reproductive success is known to decline in old age, it is unknown whether women gain fitness by prolonging lifespan post-reproduction. Using complete multi-generational demographic records, we show that women with a prolonged post-reproductive lifespan have more grandchildren, and hence greater fitness, in pre-modern populations of both Finns and Canadians. This fitness benefit arises because post-reproductive mothers enhance the lifetime reproductive success of their offspring by allowing them to breed earlier, more frequently and more successfully. Finally, the fitness benefits of prolonged lifespan diminish as the reproductive output of offspring declines. This suggests that in female humans, selection for deferred ageing should wane when one's own offspring become post-reproductive and, correspondingly, we show that rates of female mortality accelerate as their offspring terminate reproduction.