Menopause, the permanent cessation of ovulation, occurs in humans well before the end of the expected lifespan, leading to an extensive post-reproductive period which remains a puzzle for evolutionary biologists. All human populations display this particularity; thus, it is difficult to empirically evaluate the conditions for its emergence. In this study, we used artificial neural networks to model the emergence and evolution of allocation decisions related to reproduction in simulated populations. When allocation decisions were allowed to freely evolve, both menopause and extensive post-reproductive life-span emerged under some ecological conditions. This result allowed us to test various hypotheses about the required conditions for the emergence of menopause and extensive post-reproductive life-span. Our findings did not support the Maternal Hypothesis (menopause has evolved to avoid the risk of dying in childbirth, which is higher in older women). In contrast, results supported a shared prediction from the Grandmother Hypothesis and the Embodied Capital Model. Indeed, we found that extensive post-reproductive lifespan allows resource reallocation to increase fertility of the children and survival of the grandchildren. Furthermore, neural capital development and the skill intensiveness of the foraging niche, rather than strength, played a major role in shaping the age profile of somatic and cognitive senescence in our simulated populations. This result supports the Embodied Capital Model rather than the Grand-Mother Hypothesis. Finally, in simulated populations where menopause had already evolved, we found that reduced post-reproductive lifespan lead to reduced children’s fertility and grandchildren’s survival. The results are discussed in the context of the evolutionary emergence of menopause and extensive post-reproductive life-span.

In all human populations, regardless of environmental and socioeconomic conditions, menopause occurs in women well before the end of their expected lifespan. Conversely, extensive post-reproductive life-span is rare in other species; except in some cetaceans. Evolutionary theory predicts that menopause and extensive post-reproductive lifespan should emerge and persist in populations only if it is advantageous for gene transmission. Identifying this advantage is a long-standing issue. We provide a better understanding by demonstrating that humans’ cognitive abilities, in association with grand-mothering, are required for the emergence of this pattern. Indeed, cognitive abilities allow accumulation of skills and experience over the lifespan, thus providing an advantage for resource acquisition. These surplus resources can then be used to increase the number of offspring or be transmitted to existing offspring and grandoffspring. Stopping reproduction during aging allows allocating more resources to assist offspring and grandoffspring, thus increasing children’s fertility and grandchildren’s survival.

Introduction

Menopause, the permanent cessation of ovulation, occurs in women well before the end of their expected lifespan; reproductive senescence occurs substantially earlier than somatic senescence, leading to a particularly long post-reproductive life [1]. This is a rather uniform pattern across traditional and modern human societies. For example, if a man or a woman reaches age 45, he or she can expect to live at least an additional two decades [2–5]. However, and remarkably consistently across populations, reproductive senescence in women is largely completed by age 45 [6]. Extensive post-reproductive life-span (PRLS) in humans is thus not a consequence of modern improvements to nutrition, hygiene or medicine. Rather, reproductive cessation occurring approximately twenty years before the end of the expected lifespan appears as a constant feature of human biology [5, 7]. Among other species, only pilot and killer whales also exhibit extensive female PRLS. For instance, female killer whales can live into the 90s although they usually stop reproducing around age 40 [8–10]. However, patterns of reproductive and somatic senescence in killer whales differ from those of humans in some other ways, especially for males. Indeed, males rarely live beyond 50 years. Moreover, they do not undergo reproductive cessation [11]. In contrast, observations in traditional human populations have suggested that men may often undergo reproductive cessation once their wives reach menopause [12].

Understanding the conditions involved in the evolution of menopause and extensive PRLS is a long-standing challenge for biologists. First, an early end to reproduction seems contrary to maximizing Darwinian fitness. Second, the selective advantage associated with long life after the end of reproduction is not trivial. Various hypotheses have been proposed (for a review see [13]), including the Maternal hypothesis (MH), the Grand-mother Hypothesis (GMH), and the Embodied capital model (ECM). The MH is the idea that menopause has evolved in humans to avoid the risk of dying at childbirth, which is higher in older women, and to ensure the survival of the last offspring [14,15]. This hypothesis might thus explain why ageing women stop reproduction. However, as it relies on costs but not on benefits, the MH seems unlikely to explain alone the particularly long duration of PRLS observed in women. Indeed, whereas age-related costs of reproduction may explain early end of reproduction, it cannot explain why additional life after reproduction may be advantageous. Furthermore, death in childbirth may not be common enough to constitute a sufficient cost [16]. According to GMH [7] and ECM [12], both menopause and long life after reproduction may have evolved as two parts of the same allocation strategy consisting of ceasing to allocate resources to direct reproduction (i.e. producing new children) to favor indirect reproduction (i.e parental or grandparental care). Indeed, menopause and extensive PRLS may allow additional resource allocation to grandoffspring care and, therefore, increased fertility of the children and survival of the grandchildren. There are two main differences between the GMH and the ECM. The first resides in the specific causal hypotheses involved [17]. Indeed, according to the GMH, strength (e.g. proxied by body size) is the primary determinant of resource production [18–21]. Children productivity is low because foraging requires strength. As human growth is particularly slow, benefit of grand-mothering for grand-children survival and fertility is high, generating selection for older women to increase longevity [21]. According to the ECM, neural capital development and the skill intensiveness of the human foraging niche play the major role in shaping the age profile of resource production and transfers. In traditional societies, a peak of resource production is reached approximately twenty years after the peak of strength (mid-twenties) [12]. This is because earlier-life investments in neural capital lead to later-life energetic returns from such investments, with the consequences that individuals still acquire more resources than they need for survival until age 70 [12]. These extra resources could be used either for direct reproduction or for indirect reproduction. However, if the cost of reproduction increases with age (for instance, due to physiological constraints), it may be more advantageous to use these resources for increasing condition and fertility of the children and grandchildren, rather than increasing the number of children. The second difference between GMH and ECM resides in the fact the ECM is a two-sex model, whereas males may not be considered in the GMH. Indeed, as the traditional hunter-gatherer pattern of production, reproduction, and parental investment depends fundamentally on a cooperative division of labor between men and women, the ECM predicts that both aging women and men may stop producing new children to allocate resources to existing children and grand-children.

To test the MH [22, 23] and the GMH [24, 25], empirical studies have compared the fitness of children and grandchildren of women who experienced different durations of post-reproductive life-span. However, it is unclear if these studies help to understand the emergence or maintenance of menopause and extensive PRLS [26]. Indeed, the conditions favoring their maintenance are not the same as the conditions favoring their emergence. This is because female reproductive strategies in a population alter the social environment and determine the benefits of a trait. This change affects competition for reproductive resources and the average relatedness between interacting individuals [26]. Thus, the evolution of menopause and PRLS should not be studied outside of its ecological context or without considering the feedback between the evolution of this trait and the resulting ecology. To empirically study the evolutionary emergence of extensive PRLS, the fitness of rare mutant females who experience menopause should be compared to the fitness of resident females who do not. However, this is a possibility neither in humans, as menopause and extensive PRLS is already present in all populations [26], nor in our closest relative species, as reproductive senescence in midlife seems to be absent in non-human primates [27]. Regarding the ECM, the prediction that both aging women and men may stop producing new children to allocate resources to existing children and grand-children has been already supported by observations in traditional human populations [12]. However, the relation between neural capital development and skill intensiveness of the foraging niche on the one hand, and the duration of PRLS on the other hand, have not been demonstrated yet.

Here, we tested the MH, GMH and ECM for both the emergence and the persistence of menopause and extensive PRLS using a modeling approach based on life-history theory. Life history theory is the idea that living organisms must divide the total energetic potential available to them over their lifetime to perform different tasks, mainly survival, growth, direct reproduction, and parental care [28, 29]. As this energetic potential is limited, trade-offs occur among these tasks, resulting in different life-history strategies. The first trade-off occurs between immediate and future reproduction (via investment in growth and survival). The second trade-off occurs between the quantity and quality of offspring (i.e., having more offspring versus a larger investment in each of them). Modeling the evolution of allocation strategies should allow investigating the conditions for a switch from allocation to direct reproduction to allocation to indirect reproduction, i.e. for the emergence and persistence of both menopause and extensive PRLS. However, it requires a comprehensive model that considers both all of the allocation decisions that an individual has to make during his or her life, and how these decisions are shaped by complex interactions between genes, environment, and the internal state of the individual at the time when he has to make the decision.

We used Artificial Neural Networks (ANNs [30]) to simulate the evolution of resource allocation strategies, including all types of complex, even unforeseen, trade-offs in populations subject to diverse ecological conditions. Allocation decisions were allowed to freely evolve, and menopause and extensive PRLS emerged under some ecological conditions. We then tested for the following predictions: (1) Under the MH, menopause (and thus extensive PRLS) should not be observed without including age-dependent risk of dying at childbirth in the model; (2) Under both the GMH and the ECM, menopause and extensive PRLS should not emerge, whatever the ecological conditions, if resource transfers to grand-offspring are not allowed; (3) Under the ECM only, cognitive resources, because of delayed benefits of investment in neural development, should be a required condition for the emergence of menopause and extensive PRLS. Note that the ECM, as mentioned before, also predicts that both aging women and men may stop producing new children to allocate resources to existing children and grand-children, a prediction which has been supported by observations in traditional human populations [12]. Due to methodological issues (see limitation section), we did not test this prediction here. We rather focused on the relation between cognitive resources and extensive PRLS, which has never been tested before. Finally, we also tested whether MH, GMH and ECM may explain the persistence of extensive PRLS in simulated populations where this trait has already evolved. In these populations, GMH predicts that mother death at the age of menopause or delayed menopause of the mother should lead to decreased fertility of the children and/or decreased grandchildren survival. MH predicts that, under the same conditions, survival of the children should be decreased.