Post-reproductive Lifespan Research Articles

Diagnosis of Menopause in a Captive Sumatran Orangutan (Pongo abelii).

Humans were long thought to be the only mammal to experience menopause, the permanent cessation of reproduction followed by a long post-reproductive lifespan. More recently, evidence has been found for the existence of menopause in other long-lived mammals, including chimpanzees and gorillas. However, orangutans, which have the longest interbirth interval of any primate, have rarely been studied in this period of their lives. In this paper, we describe clinical, ultrasound, endocrine, and histological evidence consistent with a natural menopause in a captive, previously fertile, Sumatran orangutan (Pongo abelii), aged approximately 50. Consecutive serum samples showed low levels of estradiol and high levels of follicle-stimulating hormone. Transvaginal ultrasound revealed an atrophic uterus with an antero-posterior diameter of 2.36 cm, an endometrial thickness of 2 mm, and inactive ovaries. Following this female's death from a subdural hematoma, histological examination of the ovaries showed a dense stroma with corpora albicantia, in comparison to the numerous primordial follicles seen in the ovaries of a stillborn infant female orangutan. These multiple lines of evidence suggest that Sumatran orangutans can now be added to the list of mammals which undergo a true menopause, which may ensure that females' final offspring can be reared to independence.

Reproductive Cessation and Post-Reproductive Lifespan in Honeybee Workers.

The post-reproductive lifespan is an evolutionary enigma because the cessation of reproduction in animals seems contrary to the maximization of Darwinian fitness. Several theories aim to explain the evolution of menopause, one of which suggests that females of a certain age receive more fitness benefits via indirect selection (kin selection) than they would directly from continuing reproduction. Post-reproductive lifespans are not very common in nature but have been described in humans, nonhuman primates, a few species of toothed whales, guppies, and in some insect societies consisting of clonal colony members, such as aphid and ant societies. Here, we provide evidence that menopause also exists in honeybee societies. Our study shows that workers with a short life expectancy (older and/or injured workers) invest fewer resources and less time in their own reproduction than workers with a long life expectancy (younger and/or uninjured workers), even if their colony is hopelessly queenless. These results are consistent with the kin selection explanation for the evolution of menopause and help us understand the net effects of relatedness and social cooperation in animals.

No sign of reproductive cessation in the old workers of a queenless ponerine ant

In many social hymenopterans, workers of different ages engage in different tasks; younger workers remain inside the nest as intranidal workers, while older workers go outside the nest as extranidal workers (i.e., age polyethism). Previous studies have shown that ovarian activity is diminished in old, extranidal workers, but it remains unclear whether workers’ reproductive ability persists for life or whether they exhibit post-reproductive lifespans. In this study, we investigated the age-dependence of worker reproductive ability in a monomorphic ponerine ant Diacamma cf. indicum. In Diacamma ants, all females in a colony have reproductive ability, but effective reproduction is limited to one or a few dominant females, and the remaining females act as sterile helpers. Using long-term laboratory rearing, we investigated whether worker reproductive ability lasts throughout a worker’s lifetime. The ages of workers were accurately tracked, and the reproductive ability of young and old workers was examined by creating several gamergate-less sub-colonies. Results showed that at least one individual in each sub-colony developed ovaries, even in the sub-colonies that solely consisted of very old workers (> 252 days old). Interestingly, in the presence of younger workers, old workers rarely showed ovarian development. Besides age, we found a positive correlation between the amount of fat (i.e., nutritional condition) and ovarian development in old workers. Our data suggest that reproductive activity of old workers is low but maintained throughout their life in Diacamma.Significance statementFemales of social animals, such as cetaceans, are known to stop reproducing before the end of their lifespan. It is suggested that the reproductive ability of ant queens does not decline and is maintained throughout their lives; however, it is unclear whether this is also true in ant workers. We maintained ant colonies for more than 500 days and then tested whether the reproductive ability of ant workers is maintained throughout their lifespan. Even in small groups composed of only very old workers (> 252 days old), at least one individual in each group always reproduced actively. Interestingly, the presence of young workers seemed to suppress the reproduction of old workers. In addition, fat content was positively associated with the individual’s reproductive potential.

Grandmother effects over the Finnish demographic transition.

Demographic transitions are defining events for human societies, marking shifts from natural mortality and fertility rates to the low rates seen in industrialised populations. These transitions can affect trait evolution through altering the direction and strength of selection when variance in fertility and mortality decline. One key feature of human evolution is the evolution of extended post-reproductive life through indirect fitness benefits from grandmothering. Although studies in pre- and post-transition societies have documented beneficial grandmother presence, it remains unknown whether these associations changed before, during, or after the transition. Here, we use genealogical data from eighteenth- to twientieth-century Finland to show grandmother-associated changes of two measures of evolutionary fitness (grandchild survival and birth rate) over the transition. We find that grandmothers had greater opportunity to help as the transition progressed, but their effect on grandchild survival declined alongside general mortality rates, implying that selection on lifespan from grandmothering declined too. Whilst grandmother presence was still associated with reduced birth intervals and hence more grandchildren born post-transition, the nature of this relationship changed greatly. This suggests that although potential for intergenerational interactions increased over the demographic transition, the (hypothesised) evolutionary importance of these interactions declined, which reduced selection for extended post-reproductive lifespan.

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.

Lack of intergenerational reproductive conflict, rather than lack of inclusive fitness benefits, explains absence of post-reproductive lifespan in long-finned pilot whales.

Life-history theory suggests that individuals should reproduce until death, yet females of a small number of mammals live for a significant period after ceasing reproduction, a phenomenon known as post-reproductive lifespan. It is thought that the evolution of this trait is facilitated by increasing local relatedness throughout a female's lifetime. This allows older females to gain inclusive fitness through helping their offspring (known as a mother effect) and/or grandoffspring (known as a grandmother effect), rather than gaining direct fitness through reproducing. However, older females may only benefit from stopping reproducing when their direct offspring compete with those of their daughters. Here, we investigate whether a lack of post-reproductive lifespan in long-finned pilot whales (Globicephala melas) results from minimal benefits incurred from the presence of older females, or from a lack of costs resulting from mother-daughter co-reproduction. Using microsatellite data, we conducted parentage analysis on individuals from 25 pods and find that younger females were more likely to have offspring if their mother was present in their pod, indicating that mothers may assist inexperienced daughters to reproduce. However, we found no evidence of reproductive conflict between co-reproducing mothers and daughters, indicating that females may be able to reproduce into old age while simultaneously aiding their daughters in reproduction. This highlights the importance of reproductive conflict in the evolution of a post-reproductive lifespan and demonstrates that mother and grandmother effects alone do not result in the evolution of a post-reproductive lifespan.

Temporal dynamics of mother-offspring relationships in Bigg's killer whales: opportunities for kin-directed help by post-reproductive females.

Age-related changes in the patterns of local relatedness (kinship dynamics) can be a significant selective force shaping the evolution of life history and social behaviour. In humans and some species of toothed whales, average female relatedness increases with age, which can select for a prolonged post-reproductive lifespan in older females due to both costs of reproductive conflict and benefits of late-life helping of kin. Killer whales (Orcinus orca) provide a valuable system for exploring social dynamics related to such costs and benefits in a mammal with an extended post-reproductive female lifespan. We use more than 40 years of demographic and association data on the mammal-eating Bigg's killer whale to quantify how mother-offspring social relationships change with offspring age and identify opportunities for late-life helping and the potential for an intergenerational reproductive conflict. Our results suggest a high degree of male philopatry and female-biased budding dispersal in Bigg's killer whales, with some variability in the dispersal rate for both sexes. These patterns of dispersal provide opportunities for late-life helping particularly between mothers and their adult sons, while partly mitigating the costs of mother-daughter reproductive conflict. Our results provide an important step towards understanding why and how menopause has evolved in Bigg's killer whales.

Of dolphins, humans, other long-lived animals and Alzheimer's disease (Commentary on Vacher et al.).

Of dolphins, humans, other long-lived animals and Alzheimer's disease (Commentary on Vacher et al.).

Theoretical perspectives on reproductive aging

Age patterns of female reproduction vary widely among iteroparous animal species with determinate growth. Often fertility declines with age, but in other cases, it may be flat or rise across age. Sometimes fertility ceases altogether, leaving a substantial post-reproductive life span. In this article, we discuss theories that may provide some insights into how these diverse patterns might evolve. We present a simple optimal life history model and consider circumstances in which fertility might rise or fall with age. In our model, without assuming that costs per birth rise with age, that foraging efficiency declines, or that net intergenerational transfers increase, we find that optimal fertility would tend to rise rather than decline. This happens because less energy would be allocated to survival at older ages, leaving more to allocate to fertility. In our analysis, optimal fertility could decline at older ages when an older female makes heavy net intergenerational transfers to multiple offspring or grandoffspring, reducing resources for her own reproduction. This pattern is more likely to evolve when costs of fertility at older ages are higher, when costs of reducing juvenile mortality are low, and when the level of juvenile mortality is high. We also derive conditions for the evolution of menopause, for determinate growth, and for juvenile mortality that declines with age. The optimal life history can exhibit a variety of age patterns of fertility, rising, flat, or falling, depending on the constraints and opportunities faced.

Natural Selection, Technological Progress, and the Origin of Human Longevity

AbstractThis paper suggests that feedback effects between technological progress and human longevity lie at the heart of their common emergence in human history. It connects two major research questions. First, the long life span after menopause is a unique but puzzling feature of humans among primates. Second, the shift in human behavior at least 50,000 years ago, which led to an unprecedented pace of technological progress, is still not well understood. The paper develops an evolutionary growth theory that builds on the trade–off between the quantity and the quality of offspring. It suggests that early technological advances gradually increased the importance of intergenerational transfers of knowledge. Eventually, the fertility advantage shifted towards individuals that were characterized by higher parental investment in offspring and a significant post–reproductive life span. Subsequently, the rise in human longevity reinforced the process of development and laid the foundations for sustained technological progress. As a key feature, the theory resolves the debate about a “revolution” in human behavior in an entirely new way. It shows that a gradual emergence of modern behavior is sufficient to trigger a demographic shift that appears as a “behavioral revolution” in the archeological record.

Is autologous platelet activation the key step in ovarian therapy for fertility recovery and menopause reversal?

Platelets are a uniquely mammalian physiologic feature. As the only non-marine vertebrates to experience menopause, humans have a substantial post-reproductive lifespan and are believed to have a limited, non-renewable oocyte supply. Ovarian reserve typically declines after about age 35yrs, marking losses which cannot be recovered by available fertility medications. When in vitro fertilization fails due to low or absent ovarian response, gonadotropin adjustments are often ineffectual and if additional oocytes are occasionally harvested, egg quality is usually poor. This problem was confronted by Greek researchers who developed a new surgical method to insert autologous platelet-rich plasma (PRP) into ovaries; the first ovarian PRP success to improve reproductive outcomes was published from Athens in 2016. This innovation influenced later research with condensed platelet-derived growth factors, leading to correction of oocyte ploidy error, normal blastocyst development, and additional term livebirths. Yet women's health was among the last clinical domains to explore PRP, and its role in 'ovarian rejuvenation' remains unsettled. One critical aspect in this procedure is platelet activation, a commonly overlooked step in the cytokine release cascade considered essential for successful transition of undifferentiated ovarian stem cells to an oocyte lineage. Poor activation of platelets thus becomes an unforced error, potentially diminishing or even negating post-treatment ovarian follicular response. To answer this query, relevant theory, current disagreements, and new data on platelet activation are presented, along with clinical challenges for regenerative fertility practice.

APOE ɛ4 allele and TOMM40-APOC1 variants jointly contribute to survival to older ages.

Age-related diseases characteristic of post-reproductive life, aging, and life span are the examples of polygenic non-Mendelian traits with intricate genetic architectures. Polygenicity of these traits implies that multiple variants can impact their risks independently or jointly as combinations of specific variants. Here, we examined chances to live to older ages, 85 years and older, for carriers of compound genotypes comprised of combinations of genotypes of rs429358 (APOE ɛ4 encoding polymorphism), rs2075650 (TOMM40), and rs12721046 (APOC1) polymorphisms using data from four human studies. The choice of these polymorphisms was motivated by our prior results showing that the ɛ4 carriers having minor alleles of the other two polymorphisms were at exceptionally high risk of Alzheimer's disease (AD), compared with non-carriers of the minor alleles. Consistent with our prior findings for AD, we show here that the adverse effect of the ɛ4 allele on survival to older ages is significantly higher in carriers of minor alleles of rs2075650 and/or rs12721046 polymorphisms compared with their non-carriers. The exclusion of AD cases made this effect stronger. Our results provide compelling evidence that AD does not mediate the associations of the same compound genotypes with chances to survive until older ages, indicating the existence of genetically heterogeneous mechanisms. The survival chances can be mainly associated with lipid- and immunity-related mechanisms, whereas the AD risk, can be driven by the AD-biomarker-related mechanism, among others. Targeting heterogeneous polygenic profiles of individuals at high risks of complex traits is promising for the translation of genetic discoveries to health care.

Age- and sex-specific survivorship of the Southern Hemisphere long-finned pilot whale (Globicephala melas edwardii).

Biodiversity loss is a major global challenge of the 21st century. Ultimately, extinctions of species are determined by birth and death rates; thus, conservation management of at-risk species is dependent on robust demographic data. In this study, data gathered from 381 (227 females, 154 males) long-finned pilot whales (Globicephala melas edwardii) that died in 14 stranding events on the New Zealand coast between 2006 and 2017 were used to construct the first age- and sex-specific life tables for the subspecies. Survivorship curves were fitted to these data using (1) a traditional maximum likelihood approach, and (2) Siler's competing-risk model. Life table construction and subsequent survival curves revealed distinct differences in the age- and sex-specific survival rates, with females outliving males. Both sexes revealed slightly elevated rates of mortality among the youngest age-classes (<2 years) with postweaning mortality rates decreasing and remaining relatively low until the average life expectancy is reached; 11.3 years for males and 14.7 years for females. Overall (total) mortality is estimated to be 8.8% and 6.8% per annum for males and females, respectively. The mortality curve resembles that of other large mammals, with high calf mortality, lower postweaning mortality, and an exponentially increasing risk of senescent mortality. An accelerated mortality rate was observed in mature females, in contrast to the closely related short-finned pilot whale (G. macrorhynchus), which selects for an extension to the postreproductive life span. The reason for the observed differences in the mortality rate acceleration and postreproductive life span between the two pilot whale species have not been established and warrant further investigation. Obtaining robust information on the life history of long-lived species is challenging, but essential to improve our understanding of population dynamics and help predict how future pressures may impact populations. This study illustrates how demographic data from cetacean stranding events can improve knowledge of species survival rates, thus providing essential information for conservation management.

Reproductive Aging in Caenorhabditis elegans: From Molecules to Ecology

Aging animals display a broad range of progressive degenerative changes, and one of the most fascinating is the decline of female reproductive function. In the model organism Caenorhabditis elegans, hermaphrodites reach a peak of progeny production on day 2 of adulthood and then display a rapid decline; progeny production typically ends by day 8 of adulthood. Since animals typically survive until day 15 of adulthood, there is a substantial post reproductive lifespan. Here we review the molecular and cellular changes that occur during reproductive aging, including reductions in stem cell number and activity, slowing meiotic progression, diminished Notch signaling, and deterioration of germ line and oocyte morphology. Several interventions have been identified that delay reproductive aging, including mutations, drugs and environmental factors such as temperature. The detailed description of reproductive aging coupled with interventions that delay this process have made C. elegans a leading model system to understand the mechanisms that drive reproductive aging. While reproductive aging has dramatic consequences for individual fertility, it also has consequences for the ecology of the population. Population dynamics are driven by birth and death, and reproductive aging is one important factor that influences birth rate. A variety of theories have been advanced to explain why reproductive aging occurs and how it has been sculpted during evolution. Here we summarize these theories and discuss the utility of C. elegans for testing mechanistic and evolutionary models of reproductive aging.

Reevaluating the grandmother hypothesis.

Menopause is an evolutionary mystery: how could living longer with no capacity to reproduce possibly be advantageous? Several explanations have been offered for why female humans, unlike our closest primate relatives, have such an extensive post-reproductive lifespan. Proponents of the so-called "grandmother hypothesis" suggest that older women are able to increase their fitness by helping to care for their grandchildren as allomothers. This paper first distinguishes the grandmother hypothesis from several other hypotheses that attempt to explain menopause, and then develops a formal model by which these hypotheses can be compared and tested by empirical researchers. The model is then modified and used to respond to a common objection to the grandmother hypothesis: that human fathers, rather than grandmothers, are better suited to be allomothers due to their physical strength and a high incentive to invest in their own children. However, fathers-unlike maternal grandmothers-can never be sure that the children they are caring for are their own. Incorporating paternity uncertainty into the model demonstrates the conditions under which the grandmother hypothesis is more plausible than a hypothesis that focuses on the contributions of men.

A long postreproductive life span is a shared trait among genetically distinct killer whale populations.

The extended female postreproductive life span found in humans and some toothed whales remains an evolutionary puzzle. Theory predicts demographic patterns resulting in increased female relatedness with age (kinship dynamics) can select for a prolonged postreproductive life span due to the combined costs of intergenerational reproductive conflict and benefits of late‐life helping. Here, we test this prediction using >40 years of longitudinal demographic data from the sympatric yet genetically distinct killer whale ecotypes: resident and Bigg's killer whales. The female relatedness with age is predicted to increase in both ecotypes, but with a less steep increase in Bigg's due to their different social structure. Here, we show that there is a significant postreproductive life span in both ecotypes with >30% of adult female years being lived as postreproductive, supporting the general prediction that an increase in local relatedness with age predisposes the evolution of a postreproductive life span. Differences in the magnitude of kinship dynamics however did not influence the timing or duration of the postreproductive life span with females in both ecotypes terminating reproduction before their mid‐40s followed by an expected postreproductive period of about 20 years. Our results highlight the important role of kinship dynamics in the evolution of a long postreproductive life span in long‐lived mammals, while further implying that the timing of menopause may be a robust trait that is persistent despite substantial variation in demographic patterns among populations.

Ongoing selection for a uniquely human null allele of SIGLEC12 in world-wide populations may protect against the risk of advanced carcinomas.

The CD33-related subset of Siglecs (Sialic Acid binding Immunoglobulin superfamily Lectins) are well-known signaling receptors on immune cells, but Siglec-XII is also expressed on epithelial cell surfaces.1, 2 A point mutation eliminating the canonical sialic acid-binding function of Siglec-XII is unique to humans2, 3 and fixed in all populations worldwide. We and others reported a further polymorphic frameshift mutation in the human SIGLEC12 gene that appears to be undergoing selection favoring a null and/or truncated allele in all human populations.1, 4, 5 Individuals who have an ancestral SIGLEC12 allele with an intact open reading frame appear more prone to develop advanced carcinomas.6 The likely mechanism involves aberrant signaling via recruitment of the SHP2 phosphatase to the cytosolic tail of the dysfunctional Siglec-XII. We appreciate the strongly supportive and positive comments by Voskarides7 about our article published in this journal,6 which suggested that human-specific polymorphic pseudogenization of SIGLEC12 protects against advanced cancer progression. Voskarides appropriately emphasizes the relevance of George Williams' classic theory of “antagonistic pleiotropy”,8 in which selection for an allele's beneficial effects in early life can have deleterious consequences in late life.9 A 2018 meta-analysis of 247 Genome-Wide Association Studies (GWAS) identified an association between 1377 cancer-associated genes in populations living in extremely cold environments and very high altitudes.10-12 It is suggested that genetic variants that contributed to the survival of early humans living in these extreme environments are now associated with cancer incidence in contemporary populations, that is, the accumulation of deleterious mutations in tumor-suppressor, apoptosis, and cell cycle regulation genes.7 In response to the interesting commentary which compares our discovery with previous examples of antagonistic pleiotropy, we should emphasize that our findings on Siglec-XII are somewhat different from these instances. First, we report selection for the null alleles of SIGLEC12 in all human populations. Second, SIGLEC12 expression is not associated with the incidence or risk for carcinomas. Rather, the null state is associated with a decrease in advanced carcinomas commonly found in humans.1, 6, 13 Third, unlike the genes discussed by Voskarides, many of which are extensively studied and fundamental to cancer biology, Siglec-XII has received very little attention to date. Moreover, our studies represent the first implications of SIGLEC12 in human cancer, with currently unknown potential impact on cancer biology, prevention, and therapy. Despite the above differences between our findings6 and those of Voskarides, we believe his perspective gives some useful additional clues. First, the deleterious SIGLEC12 mutation is not fully studied and understood under stressful conditions. It might be that the status of SIGLEC12 in populations living in extreme vs non-extreme conditions is different, following the trend shown for tumor-suppressor and DNA repair genes. Our data also shows that unlike the other examples, Siglec-XII seems to be a suitable prognostic marker. In a large cohort study of late-stage colon cancer patients, we found that Siglec-XII non-expressors had a two fold higher survival than expressors.6 Siglec-XII also has the potential to be a therapeutic target, as we previously also showed that it undergoes rapid endocytosis upon binding a Siglec-XII antibody, allowing selective delivery of a conjugated toxin.1 In keeping with the conventional theory, Voskarides also emphasizes that it is very hard for natural selection to eliminate mutations that cause cancer after the end of reproductive age. With SIGLEC12, ongoing selection for the null state might be an example of a “less-is-more” evolutionary scenario, where losing expression of the full-length protein is beneficial under current selective pressures.6, 14, 15 It is also potentially an example of selection for prolonged post-reproductive life span, a trait that is unique to humans among all land mammals. Indeed, it is consistent with the grandmother hypothesis, which posits that post-reproductive individuals (predominantly grandmothers) can improve the survival of helpless younger kin.16-18 In this regard, we have reported one example of a uniquely human allele of CD33 that protects against cognitive decline during the post-reproductive lifespan of humans.19, 20 Overall, we believe that the scenario with Siglec-XII is different from other cancer genes undergoing positive selection, but further studies are needed.

Multi-system physiological dysregulation and ageing in a subsistence population.

Humans have the longest post-reproductive lifespans and lowest rates of actuarial ageing among primates. Understanding the links between slow actuarial ageing and physiological change is critical for improving the human 'healthspan'. Physiological dysregulation may be a key feature of ageing in industrialized populations with high burdens of chronic 'diseases of civilization', but little is known about age trajectories of physiological condition in subsistence populations with limited access to public health infrastructure. To better characterize human physiological dysregulation, we examined age trajectories of 40 biomarkers spanning the immune (n = 13 biomarkers), cardiometabolic (n = 14), musculoskeletal (n = 6) and other (n = 7) systems among Tsimane forager-horticulturalists of the Bolivian Amazon using mixed cross-sectional and longitudinal data (n = 22 115 observations). We characterized age-related changes using a multi-system statistical index of physiological dysregulation (Mahalanobis distance; Dm) that increases with age in both humans and other primates. Although individual biomarkers showed varied age profiles, we found a robust increase in age-related dysregulation for Tsimane (β = 0.17-0.18) that was marginally faster than that reported for an industrialized Western sample (β = 0.14-0.16), but slower than that of other non-human primates. We found minimal sex differences in the pace or average level of dysregulation for Tsimane. Our findings highlight some conserved patterns of physiological dysregulation in humans, consistent with the notion that somatic ageing exhibits species-typical patterns, despite cross-cultural variation in environmental exposures, lifestyles and mortality. This article is part of the theme issue 'Evolution of the primate ageing process'.

Reproductive and Somatic Senescence in the European Badger (Meles meles): Evidence from Lifetime Sex-Steroid Profiles

Among the Carnivora, there is sparse evidence for any substantive fitness benefits of post reproductive lifespan (PRLS, survival after reproductive cessation, RC). Using the European badger (Meles meles) as a model species, we analyzed sex-specific cross-sectional endocrinological and morphological data to investigate: 1) age-dependent reproductive decline in sex-steroid levels versus prime reproductive age; 2) age-dependent declines in somatic condition and reproductive advertisement (from subcaudal scent gland secretion); 3) changes in reproductive success with age due to somatic and endocrinological decline; 4) occurrence of RC, PRLS, and post reproductive representation (PrR) in the population with reference to pre-pubescent hormone levels and evidenced by fewer cub assignments from pedigree. We provide strong evidence for a gradual, not abrupt, decline in sex-steroid levels with age, with both sexes following a concave (down) quadratic trend. For both sexes, the onset of decline in somatic condition commenced at the age of 3 years. In contrast, decline in reproductive hormones started at age ca. 5.5 years in females and 6 years in males, with similar rates of decline thereafter. Subcaudal gland secretion volume also decreased in both sexes, especially after age 5, suggesting less investment in reproductive advertisement. After age 3, fewer (surviving) females were assigned cubs. This coincided with the onset of somatic decline but came earlier than hormonal decline (5.5 years onwards). The decrease in offspring assignments commenced later in males at age 5-6 years; concomitant with onset of testosterone decline at 6 years. This suggests that, contrary to females, in males declining body condition does not preclude reproductive success (no ‘restraint’) in advance of hormonal senescence (‘constraint’). There was evidence of female PRLS, with very old adults living up to 2.59 ± 1.29 years after RC; although in males this evidence was weaker. We discuss the implications of these findings for RC and PRLS in the context of adaptive and non-adaptive hypotheses. There was evidence of over 2 years of Post Reproductive Life Span in both sexes.

On age-specific selection and extensive lifespan beyond menopause.

Standard evolutionary theory of ageing predicts weaker purifying selection on genes critical to later life stages. Prolonged post-reproductive lifespan (PPRLS), observed only in a few species like humans, is likely a result of disparate relaxation of purifying selection on survival and reproduction in late life stages. While the exact origin of PPRLS is under debate, many researchers agree on hypotheses like mother-care and grandmother-care, which ascribe PPRLS to investment into future generations—provision to one’s descendants to enhance their overall reproductive success. Here, we simulate an agent-based model, which properly accounts for age-specific selection, to examine how different investment strategies affect the strength of purifying selection on survival and reproduction. We observed in the simulations that investment strategies that allow a female individual to remain contributive to its own descendants (infants and adults) at late life stages may lead to differential relaxation of selection on survival and reproduction, and incur the adaptive evolution of PPRLS.