Analyses of ovarian activity reveal repeated evolution of post-reproductive lifespans in toothed whales

Abstract

In most species the reproductive system ages at the same rate as somatic tissue and individuals continue reproducing until death. However, females of three species – humans, killer whales and short-finned pilot whales – have been shown to display a markedly increased rate of reproductive senescence relative to somatic ageing. In these species, a significant proportion of females live beyond their reproductive lifespan: they have a post-reproductive lifespan. Research into this puzzling life-history strategy is hindered by the difficulties of quantifying the rate of reproductive senescence in wild populations. Here we present a method for measuring the relative rate of reproductive senescence in toothed whales using published physiological data. Of the sixteen species for which data are available (which does not include killer whales), we find that three have a significant post-reproductive lifespan: short-finned pilot whales, beluga whales and narwhals. Phylogenetic reconstruction suggests that female post-reproductive lifespans have evolved several times independently in toothed whales. Our study is the first evidence of a significant post-reproductive lifespan in beluga whales and narwhals which, when taken together with the evidence for post-reproductive lifespan in killer whales, doubles the number of non-human mammals known to exhibit post-reproductive lifespans in the wild.

Why does women's fertility end in mid-life? Grandmothering and age at last birth

“…As a future continuation of our work, a broad and open question is that if L and M can both freely mutate, why does primate post-fertile longevity only appear in the hominid radiation, rather than also at monkey-like life histories, e.g., why don't at least some of the macaques or baboons that reach menopause at age 25, also have substantial post-fertile life stages? The only other mammalian radiation in which post-fertile life stages evolved, the toothed whales, includes very long-lived taxa (58,59). Perhaps a longevity threshold is a necessary, but (as elephants and some cetaceans show) not sufficient, condition for the evolution of post-fertile longevity.…”

Causes and consequences of female centrality in cetacean societies

“…In this ecotype, there is evidence that offspring of both sexes sometimes disperse either permanently or temporarily [135], which leads to significantly different kinship structure among and within pods compared with the resident type. While it remains unclear if post-reproductive lifespans have evolved among Bigg's killer whales [136], there is a documented case of infanticide among this ecotype [137], where a post-reproductive female and her mature male offspring cooperatively killed the calf of an unrelated female in the same population. This may represent an extreme case of late-life helping, driven by inclusive fitness and likely sexual selection [137], illustrating how highly modular social structure organized around female kinship structure can draw boundaries across which rather direct competition can be selected for.…”

“…An unusual case of this is the evolution of menopause, the typical cessation of reproduction in females long before the end of life. Found only in several species of matrilineal whale and in humans [136], the evolution of menopause is an evolutionary puzzle, but comparisons of female social organization partly stimulated by findings in cetaceans have borne fruit in recent years. Theory [149], as well as some empirical evidence [133], suggests that in species where females are increasingly related to their group mates as they age and have increasing levels of ecological knowledge with experience, the inclusive fitness benefits of assisting and leading group members may outweigh the direct fitness of reproduction.…”

Parturitions, menopause and other physiological stressors are recorded in dental cementum microstructure

“…Indeed, previous research on a variety of mammals shows that events impacting the physiology of an organism, such as a change in diet 64 , exposure to exceptional cold 65 and renal diseases 38 affect the histomorphology of cementum, and likely also its elemental composition. Humans are one of only five mammalian species 66 that experience a PRLS (and the only terrestrial one), hence comparative data from other organisms are unavailable.…”