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Grandmothering and cognitive resources are required for the emergence of menopause and extensive post-reproductive lifespan.

ABSTRACT: 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.

SUBMITTER: Aime C

PROVIDER: S-EPMC5519007 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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Grandmothering and cognitive resources are required for the emergence of menopause and extensive post-reproductive lifespan.

Aimé Carla C André Jean-Baptiste JB Raymond Michel M

PLoS computational biology 20170720 7

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 populatio ...[more]

PMID: 28727724

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Project description:IntroductionShort post-reproductive lifespan is widespread across species, but prolonged post-reproductive life-stages of potential adaptive significance have been reported only in few mammals with extreme longevity. Long post-reproductive lifespan contradicts classical evolutionary predictions of simultaneous senescence in survival and reproduction, and raises the question of whether extreme longevity in mammals promotes such a life-history. Among terrestrial mammals, elephants share the features with great apes and humans, of having long lifespan and offspring with long dependency. However, little data exists on the frequency of post-reproductive lifespan in elephants. Here we use extensive demographic records on semi-captive Asian elephants (n = 1040) and genealogical data on pre-industrial women (n = 5336) to provide the first comparisons of age-specific reproduction, survival and post-reproductive lifespan in both of these long-lived species.ResultsWe found that fertility decreased after age 50 in elephants, but the pattern differed from a total loss of fertility in menopausal women with many elephants continuing to reproduce at least until the age of 65 years. The probability of entering a non-reproductive state increased steadily in elephants from the earliest age of reproduction until age 65, with the longer living elephants continuing to reproduce until older ages, in contrast to humans whose termination probability increased rapidly after age 35 and reached 1 at 56 years, but did not depend on longevity. Post-reproductive lifespan reached 11-17 years in elephants and 26-27 years in humans living until old age (depending on method), but whereas half of human adult lifespan (of those reproductive females surviving to the age of 5% fecundity) was spent as post-reproductive, only one eighth was in elephants. Consequently, although some elephants have long post-reproductive lifespans, relatively few individuals reach such a phase and the decline in fertility generally parallels declines in survivorship in contrast to humans with a decoupling of senescence in somatic and reproductive functions.ConclusionsOur results show that the reproductive and survival patterns of Asian elephants differ from other long-lived animals exhibiting menopause, such as humans, and extreme longevity alone does not promote the evolution of menopause or post-reproductive lifespan, adding weight to the unusual kin-selected benefits suggested to favour such traits in humans and killer whales.

Project description:1. While-classical life-history theory does not predict post-reproductive lifespan (PRLS), it has been detected in a great number of taxa, leading to the view that it is a broadly conserved trait, and attempts to reconcile theory with these observations. We suggest an alternative: the apparently wide distribution of significant PRLS is an artifact of insufficient methods.2. PRLS is traditionally measured in units of time between each individual's last parturition and death, after excluding those individuals for whom this interval is short. A mean of this measure is then calculated as a population value. We show this traditional population measure (which we denote PrT) to be inconsistently calculated, inherently biased, strongly correlated with overall longevity, uninformative on the importance of PRLS in a population's life-history, unable to use the most-commonly available form of relevant data and without a realistic null hypothesis. Using data altered to ensure that the null hypothesis is true, we find a false positive rate of 0.47 for PrT.3. We propose an alternative population measure, using life-table methods. Post-reproductive Representation (PrR) is the proportion of adult years lived which are post-reproductive. We briefly derive PrR and discuss its properties. We employ a demographic simulation, based on the null hypothesis of simultaneous and proportional decline in survivorship and fecundity, to produce a null distribution for PrR based on the age-specific rates of a population.4. In an example analysis, using data on 84 populations of human and non-human primates, we demonstrate the ability of PrR to represent the effects of artificial protection from mortality and of humanness on PRLS. PrR is found to be higher for all human populations under a wide range of conditions than for any non-human primate in our sample. A strong effect of artificial protection is found, but humans under the most-adverse conditions still achieve PrR of >0.3.5. PrT should not be used as a population measure, and should be used as an individual measure only with great caution. The use of PrR as an intuitive, statistically valid and intercomparable population life-history measure is encouraged.

Project description:Study questionAre there genetic variants that interact with smoking to reduce reproductive lifespan in East-Asian women?Summary answerOur study corroborates several recently identified genetic loci associated with reproductive lifespan and highlights specific genetic predispositions that may interact with smoking status to adversely affect reproductive lifespan in East-Asian women.What is known alreadyEpidemiological data as well as evaluations on genetic predisposition to smoke indicate on the importance of smoking in adverse effects on reproductive lifespan in women. However, there are no previous smoking and gene interaction studies for reproductive traits in East-Asian women.Study design, size, durationThis population-based prospective cohort study comprised 11 643 East-Asian Chinese women with overlapping genome-wide genotyping and reproductive data.Participants/materials, setting, methodsWe performed a genome-wide association study for reproductive lifespan in women (n = 11 643) from the Singapore Chinese Health Study (SCHS) and carried out a genome-wide interaction study to identify loci that interacted with smoking status to affect age of natural menopause and reproductive-time.Main results and the role of chanceTwo known loci associated with menopause, rs113430717 (near HMCES, chromosome 3, Pmeta = 5.72 × 10-15) and rs3020136 (near RAD21, chromosome 8, Pmeta = 1.38 × 10-8) were observed beyond genome-wide levels of association with age at menopause in this study. For reproductive lifespan, the genome-wide association observed at rs79784106 (chromosome 3, Pmeta = 5.05 × 10-12) was in linkage disequilibrium with the menopause lead single-nucleotide polymorphism (SNP) (rs113430717). Four additional loci, first reported to be associated with menopause, were also associated with reproductive lifespan in our study (PAdj between 7.42 × 10-5 to 4.51 × 10-3). A significant interaction was observed between smoking and an East-Asian specific SNP, rs140146885, for reduced reproductive lifespan, per copy of the minor C allele (beta = -1.417 years, Pinteraction = 2.31 × 10-10). This interaction was successfully replicated in additional independent samples (beta = -1.389 years, Pinteraction = 6.78 × 10-3). Another known variant associated with menopause, rs11031006 (near FSHB), was also observed to interact with smoking status to reduce age at menopause in our dataset (beta = -0.450 years, Padj = 0.042).Limitations, reasons for cautionThe modest sample size of the replication datasets used likely affected the statistical power to firmly replicate all identified novel loci observed in our smoking interaction analyses.Wider implications of the findingsAge of natural menopause and reproductive lifespan have clear genetic predispositions with distinct ethnic differences, and they may be adversely truncated by lifestyle factors such as smoking, which can pose a significant impact on the reproductive lifespan and future health outcomes in women.Study funding/competing interest(s)The Singapore Chinese Health Study is funded by the National Medical Research Council, Singapore (NMRC/CIRG/1456/2016), National Institutes of Health (R01 CA144034 and UM1 CA182876) and National Research Foundation, Singapore (Project Number 370062002). W.-P.K. is supported by the National Medical Research Council, Singapore (MOH-CSASI19nov-0001). The corresponding author had full access to all the data in the study and had final responsibility for the decision to submit for publication. The authors do not report conflicts of interest.Trial registration numberN/A.

Project description:ObjectivesThe parent-child relationship is critical for human development, yet little is known about its association with offsprings' reproductive health outside the context of abuse and neglect. We investigated whether childhood experiences of poor-quality parenting (characterized as decreased parental care and increased parental overprotection) are associated with women's reproductive timing and lifespan.Study designObservational study of 2383 women aged 55-89 years in 2007 from the English Longitudinal Study of Ageing (ELSA). Multinomial logistic regression models were estimated.Main outcome measuresSelf-reported ages at menarche and menopause and duration of reproductive lifespan.ResultsIncreasing maternal and paternal overprotection were associated with later menarche (≥16 years) after adjustment for age and childhood socioeconomic position (relative risk ratio (RRR) 1.11, 95% CI 1.02-1.21 and 1.11, 95% CI 1.01-1.21, respectively, per unit increase in the predictor). Increasing parental overprotection and decreasing paternal care were associated with earlier menarche (≤10 years). However, these associations were marginally non-significant. Maternal and paternal overprotection were also inversely associated with age at natural menopause after adjustment for age, childhood socioeconomic position and age at menarche (p value for linear trend = 0.041 and 0.004, respectively). Further, increasing paternal overprotection was associated with a shorter reproductive lifespan (≤33 years) (RRR 1.09 (1.01-1.18), per unit increase in the predictor) after adjustment for age and childhood socioeconomic position. Adjustment for additional childhood and adult factors did not explain these associations.ConclusionsWomen who experienced poor-quality parenting in childhood, especially increased levels of parental overprotection, might be at increased risk of an unfavourable reproductive health profile that is characterized by late or early menarche, premature menopause and a shorter reproductive lifespan.

Dataset Information

Grandmothering and cognitive resources are required for the emergence of menopause and extensive post-reproductive lifespan.

Publications

Grandmothering and cognitive resources are required for the emergence of menopause and extensive post-reproductive lifespan.

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