The evolution of menopause in cetaceans and humans: the role of demography

Abstract

Human females stop reproducing long before they die. Among other mammals, only pilot and killer whales exhibit a comparable period of post-reproductive life. The grandmother hypothesis suggests that kin selection can favour post-reproductive survival when older females help their relatives to reproduce. But although there is an evidence that grandmothers can provide such assistance, it is puzzling why menopause should have evolved only among the great apes and toothed whales. We have previously suggested (Cant & Johnstone 2008 Proc. Natl Acad. Sci. USA 105, 5332–5336 (doi:10.1073/pnas.071191110510.1073/pnas.0711911105)) that relatedness asymmetries owing to female-biased dispersal in ancestral humans would have favoured younger females in reproductive competition with older females, predisposing our species to the evolution of menopause. But this argument appears inapplicable to menopausal cetaceans, which exhibit philopatry of both sexes combined with extra-group mating. Here, we derive general formulae for ‘kinship dynamics’, the age-related changes in local relatedness that occur in long-lived social organisms as a consequence of dispersal and mortality. We show that the very different social structures of great apes and menopausal whales both give rise to an increase in local relatedness with female age, favouring late-life helping. Our analysis can therefore help to explain why, of all long-lived, social mammals, it is specifically among the great apes and toothed whales that menopause and post-reproductive helping have evolved.

Menopause Female Reproductive Senescence from the Viewpoint of Evolutionary Anthropology

“…Some signs of reproductive ageing are found among invertebrates in particular tephritid fruit lies [17] and the nematode Caenorhabditis elegans [18]. A kind of reproductive ageing characterized by a decline of sex steroid levels and a reduced probability of successful reproduction is found among several free living social mammals such as toothed whales, elephants, lions, or irst of all primates [19][20][21][22][23][24][25]. An obligatory postreproductive life stage of 30 years and more, however, is exclusively found among human females [23].…”

“…Long postreproductive periods are uncommon among animals, even among large social mammals such as nonhuman primates and elephants. Only two Cetacean species such as short-inned pilot whales (Globicephala macrorhynchus) and killer whales (Orcinus orca) exhibit postreproductive life spans comparable to those of female Homo sapiens [22,26]. Female short inned pilot whales stop to reproduce by about 36 years of age but they can live up to 65 years [22].…”

When not to have another baby: An evolutionary approach to low fertility

“…However, while reproductive conflict predicts that reproductive generations should reduce overlap, it not does address the question of why the older woman rather than the younger woman foregoes reproduction, as is generally the case in most co-operatively breeding birds or mammals (Clutton-Brock et al 2010;Hatchwell and Komdeur 2000). Johnstone and Cant argued that this competition is particularly intense for older females in species in which females disperse, as this means that the older females will not be closely related to the younger breeding females entering their group (Cant and Johnstone 2008;Johnstone and Cant 2010). Female dispersal is unusual among mammals, but is thought to be the most common arrangement among chimpanzees (Pan troglodytes) and possibly among ancestral humans, although there is variation in the residence patterns of contemporary hunter-gatherers (Hill et al 2011).…”

“…The ESS models show that the younger woman is more likely to win the competition, and the older woman is destined to become the sterile helper. Johnstone and Cant (2010) argued that this helps explain late-life low fertility in whale and primate groups in which females either disperse or mate outside the group, and that humans generally fall into the former category. This raises the possibility that part-and perhaps the greater part of a grandmother's contribution is her failure to compete, and that this is linked to sex-biased dispersal patterns.…”

Evolution of Helping and Harming in Viscous Populations When Group Size Varies

“…This striking result has stimulated the development of a large body of theoretical-and, to a lesser extent, empirical-research examining what additional factors may decouple the relatedness and competition ef-fects of limited dispersal, so that indiscriminate helping may be favored in viscous populations. Some of these factors include population elasticity (Taylor 1992b), overlapping generations (Taylor and Irwin 2000;Irwin and Taylor 2001), budding dispersal (Gardner and West 2006;Lehmann et al 2006b;Kümmerli et al 2009), an organism's life cycle and timing of social behavior (Taylor 1992a;Lehmann and Rousset 2010), behaviors mediating patchextinction probabilities (Lehmann et al 2006b), transgenerational altruism (Lehmann 2007(Lehmann , 2010, dispersaldependent social behavior (El Mouden and Gardner 2008), empty sites (Alizon and Taylor 2008), sex-biased dispersal (Johnstone and Cant 2008;Gardner 2010), reproductive skew (Johnstone 2008), age structure (Johnstone and Cant 2010), and heterogeneity in resource availability (Rodrigues and Gardner 2012).…”