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      Menopausal chimpanzees deepen the mystery of why women stop reproducing

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          Demographic and hormonal evidence for menopause in wild chimpanzees

          Among mammals, post-reproductive life spans are currently documented only in humans and a few species of toothed whales. Here we show that a post-reproductive life span exists among wild chimpanzees in the Ngogo community of Kibale National Park, Uganda. Post-reproductive representation was 0.195, indicating that a female who reached adulthood could expect to live about one-fifth of her adult life in a post-reproductive state, around half as long as human hunter-gatherers. Post-reproductive females exhibited hormonal signatures of menopause, including sharply increasing gonadotropins after age 50. We discuss whether post-reproductive life spans in wild chimpanzees occur only rarely, as a short-term response to favorable ecological conditions, or instead are an evolved species-typical trait as well as the implications of these alternatives for our understanding of the evolution of post-reproductive life spans. Menopause occurs in all known human societies; however, it is not common to all mammals and has so far only been observed in humans and a few toothed whale species. Wood et al . looked at demographic and endocrine data in a long-studied population of chimpanzees in Uganda and found clear evidence for menopause in females living past the age of 50 (see the Perspective by Cant). Unlike the case for humans and toothed whales, however, postreproductive chimps in this population are not involved in the raising of related offspring, suggesting that a different process is driving its development. —Sacha Vignieri Substantial postfertile survival and menopause occur among wild chimpanzees in the Ngogo community in Kibale National Park, Uganda. It is not obvious why selection should favor menopause or the continued survival of individuals that can no longer reproduce. Among mammals, substantial numbers of post-reproductive females living under natural conditions in the wild have only been observed in humans and a few whale species. The rarity of this trait makes it both interesting and difficult to study. Data from our close primate relatives are especially valuable for the reconstruction and causal modeling of human life history evolution. In this study, we combined demographic and hormonal data to investigate post-reproductive life spans and their underlying physiological mechanisms in chimpanzees ( Pan troglodytes schweinfurthii ), who, along with bonobos, are humans’ closest living relatives. We examined the mortality and fertility rates of 185 female chimpanzees in the Ngogo community of wild chimpanzees in Kibale National Park, Uganda, from 21 years of observation (1995–2016). We calculated the demographic measure PrR (post-reproductive representation), representing the fraction of adult life spent in a post-reproductive state. Human menopause, the nonpathological and permanent cessation of ovarian function resulting from the depletion of ovarian follicles, is reflected in increasing levels of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) and decreasing levels of ovarian steroid hormones (estrogens and progestins). To assess whether Ngogo females undergo humanlike menopause, we analyzed age-associated trends in five hormones measured in 560 urine samples from 66 females of varying reproductive status and age (range: 14 to 67 years). As in other chimpanzee populations and humans, fertility declined after age 30, and no births were observed after age 50. Unlike other chimpanzee populations, but as in humans, it was not unusual for Ngogo females to live past the age of 50 ( N = 16 females). The observed PrR value was 0.195, indicating that a female who reached adulthood (age 14) was post-reproductive for about one-fifth of her adult life, around half as long as human hunter-gatherers. Hormonal measures show that Ngogo females experience a reproductive transition similar to that of humans, characterized by increasing levels of FSH and LH and declining levels of estrogens and progestins as they undergo menopause. Menopause ends reproduction around the age of 50 in both humans and wild chimpanzees. Substantial PrR has not been previously observed in any wild primate population, chimpanzees included. One explanation for this discrepancy is that substantial PrR could be a temporary response to unusually favorable ecological conditions at Ngogo, including low levels of predation, high food availability, and successful between-group competition. A second possibility is that substantial PrR is an evolved, species-typical trait in chimpanzees, which has not been observed elsewhere owing to recent negative human impacts, especially disease epidemics. The grandmother hypothesis suggests that older females could evolve to live past their reproductive years to help increase their daughters’ fertility or their grandoffsprings’ survival. This is unlikely to apply to chimpanzees, whose aged females generally live apart from their daughters, as daughters leave their natal groups at adulthood. In the context of female-biased dispersal, a more relevant theory may be the reproductive conflict hypothesis, which highlights the fact that after migrating into a new group, females become increasingly related to other group members as they age and face competition with younger females for limited breeding opportunities. The oldest females might stop reproducing in order to limit the inclusive fitness costs of that competition. The grandmother and reproductive conflict hypotheses are not mutually exclusive alternatives, and both may be required to explain why all human societies have higher PrR than documented here for chimpanzees.
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            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.
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              Author and article information

              Journal
              Nature
              Nature
              Springer Science and Business Media LLC
              0028-0836
              1476-4687
              October 26 2023
              Article
              10.1038/d41586-023-03308-8
              6be8bed1-4e49-45ee-a465-edc3502696a1
              © 2023

              https://www.springernature.com/gp/researchers/text-and-data-mining

              https://www.springernature.com/gp/researchers/text-and-data-mining

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