No time to die: Evolution of a post-reproductive life stage

In some species, permanent curtailment of reproduction part-way through the lifespan of adult females is a feature of their evolved life history. The existence of such a post-reproductive life stage is apparently rare; reasonably robust evidence for this is confined to only six species (humans, Asian elephants and four whales). That it occurs at all appears to contradict our view of natural selection operating to maximize fitness and special circumstances must exist to explain its occurrence. We evaluate the main hypotheses posited to explain the evolution of this life stage, why it occurs in a restricted group of animals, and why only in females. We bring together literature from multiple biological disciplines and levels of enquiry, ranging through evolutionary ecology, developmental biology, physiology, neuroscience, molecular biology, and human medicine. We conclude that while time-limited fertility is not in itself adaptive, the duration of subsequent survival is likely to be linked to inclusive fitness benefits. We present a new hypothesis which posits that the duration of female fertility in certain long-lived, highly encephalised species, with no post-natal oogenesis, is limited by the need for intense screening of oocyte mitochondria. This is required to support endothermy coupled with the very high energy requirement for the development and maintenance of the exceptionally large brain size required for complex social living. This limits the number and shelf-life of oocytes, creating an antagonistically pleotropic effect that is beneficial to the production of high performing offspring but carries the later life cost of time-limited female fertility. But the end of the fertile period is no time to die. Inclusive fitness benefits arising from protracted parental care of offspring, overlapping generations, and kin group structures means that continued survival of post-reproductive females is favoured by selection. We suggest further lines of research to test these ideas.