Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women

Evolutionary theory of senescence emphasizes the importance of intense selection on early reproduction owing to the declining force of natural selection with age that constrains lifespan. In humans, recent studies have, however, suggested that late-life mortality might be more closely related to late rather than early reproduction, although the role of late reproduction on fitness remains unclear. We examined the association between early and late reproduction with longevity in historical post-reproductive Sami women. We also estimated the strength of natural selection on early and late reproduction using path analysis, and the effect of reproductive timing on offspring survival to adulthood and maternal risk of dying at childbirth. We found that natural selection favoured both earlier start and later cessation of reproduction, and higher total fecundity. Maternal age at childbirth was not related to offspring or maternal survival. Interestingly, females who produced their last offspring at advanced age also lived longest, while age at first reproduction and total fecundity were unrelated to female longevity. Our results thus suggest that reproductive and somatic senescence may have been coupled in these human populations, and that selection could have favoured late reproduction. We discuss alternative hypotheses for the mechanisms which might have promoted the association between late reproduction and longevity.     

Fertility History,Children’s Gender,and Post-Reproductive Survival in a Longevous Population

The question of whether mothers’ fertility history influences their post-reproductive survival has been addressed frequently in the scientific literature. Using data from Villagrande Strisaili, Sardinia, where longevity is higher than anywhere else in Europe, we analyzed the relationship between the fertility pattern of mothers who survived past age 50 (n = 539) and their post-reproductive lifespan. We find that, after adjustment for potential confounders (mothers’ birth cohort, survival of spouse), the mothers who on average delivered their children later displayed a reduced mortality risk (?2.9 percent for each additional year), supporting previously reported findings. We also find that a male-skewed offspring ratio was associated with decreased mortality risk of mothers, with longer survival of mothers who delivered their sons above age 35 (p = 0.005), a result not found for daughters. So far, no biological explanation has been suggested for the positive effect of delivering sons later in life. We conjecture that in our dataset stronger nonbiological factors such as gender-specific sociocultural and economic factors may have masked the negative effect reported in other populations, for which a biological explanation was proposed.     

The role of survival for the evolution of female philopatry in a solitary forager, the grey mouse lemur (Microcebus murinus)

It is widely accepted that natal philopatry is a prerequisite for the evolution of sociality. The life-history hypothesis maintains that longevity of adults results in extended territory tenure and thus limits breeding vacancies for offspring, which makes natal philopatry more likely. Here, we tested the importance of longevity for natal philopatry in females of a basal primate, the grey mouse lemur (Microcebus murinus). This species is regarded as being solitary due to its foraging habits but while males disperse, female offspring in this species forgo dispersal and form long-term sleeping groups with their mothers. We tested whether high adult survival could be a cause for natal philopatry of female offspring. In addition, we assessed costs and benefits associated with space sharing between mothers and daughters and whether mothers actively increase survival of daughters by beqeauthal of territories, information transfer about resources or thermoregulation. Contrary to our predictions, adult females had low-survival rates. Space sharing appeared to improve survival of both, mothers and daughters. This could be a result of information transfer about sleeping sites and thermoregulatory benefits. Our results cast doubt on the idea that longevity predisposes species for social traits and provide support for benefits of philopatry.     

If you would live long, choose your parents well

Human longevity appears to have a modest but significant heritable component. A recent study in Iceland has added to this evidence by making a unique assessment based on records for an entire population. Although the evidence for inheritance of human lifespans appears robust, there remains considerable uncertainty about the extent of the genetic versus the nongenetic contribution and about the importance of gene-environment interactions. Sex-specific patterns of transmission of lifespan between parents and offspring might provide clues to the basis of lifespan heritability, but the reported patterns are neither conclusive nor consistent.     

Biogeographical and evolutionary importance of the European high mountain systems

Background

Menopause is a seemingly maladaptive life-history trait that is found in many long-lived mammals. There are two competing evolutionary hypotheses for this phenomenon; in the adaptive view of menopause, the cessation of reproduction may increase the fitness of older females; in the non-adaptive view, menopause may be explained by physiological deterioration with age. The decline and eventual cessation of reproduction has been documented in a number of mammalian species, however the evolutionary cause of this trait is unknown.

Results

We examined a unique 30-year time series of killer whales, tracking the reproductive performance of individuals through time. Killer whales are extremely long-lived, and may have the longest documented post-reproductive lifespan of any mammal, including humans. We found no strong support for either of the adaptive hypotheses of menopause; there was little support for the presence of post-reproductive females benefitting their daughter's reproductive performance (interbirth interval and reproductive lifespan of daughters), or the number of mature recruits to the population. Oldest mothers (> 35) did appear to have a small positive impact on calf survival, suggesting that females may gain experience with age. There was mixed support for the grandmother hypothesis – grandoffspring survival probabilities were not influenced by living grandmothers, but grandmothers may positively influence survival of juveniles at a critical life stage.

Conclusion

Although existing data do not allow us to examine evolutionary tradeoffs between survival and reproduction for this species, we were able to examine the effect of maternal age on offspring survival. Our results are consistent with similar studies of other mammals – oldest mothers appear to be better mothers, producing calves with higher survival rates. Studies of juvenile survival in humans have reported positive benefits of grandmothers on newly weaned infants; our results indicate that 3-year old killer whales may experience a positive benefit from helpful grandmothers. While our research provides little support for menopause evolving to provide fitness benefits to mothers or grandmothers, our work supports previous research showing that menopause and long post-reproductive lifespans are not a human phenomenon.     

An Old Mom Keeps You Young: Mother’s Age at Last Birth and Offspring Longevity in Nineteenth-Century Utah

This study analyzes the intergenerational effects of late childbearing on offspring’s adult longevity in a population in Utah (United States) that does not display evidence of parity-specific birth control—a so-called natural fertility population. Studies have found that for women who experience late menopause and prolonged reproduction, aging is postponed and longevity is increased. This is believed to indicate female “robustness” and the impact of biological or genetic factors. If indeed there is a genetic component involved, one would expect to also find evidence for the intergenerational transmission of longevity benefits. Our study investigates the relationship between prolonged natural fertility of mothers and their offspring’s survival rates in adulthood. Gompertz regression models (N = 7,716) revealed that the offspring of mothers who were naturally fertile until a relatively advanced age lived significantly longer. This observed positive effect of late reproduction was not independent of but conditional upon survival of the mother to the end of her fecundity (defined as age 50). Offspring’s relative risks at death beyond age 50 were 6–12 percent lower than those of their counterparts born to mothers who had an average age at last birth. Our results, which account for various early, adult, and later-life conditions, as well as shared frailty, suggest that there is a positive relationship between mother’s age at last birth and offspring longevity, and strengthen the notion that age at menopause is a good predictor of this relationship.     

Sex‐specific deposition and survival effects of maternal antibodies: a case study with the gull‐billed tern Gelochelidon nilotica

There is a growing body of evidence that maternal antibodies transferred to offspring have potential implications in the evolutionary ecology of birds. This transfer of maternal antibodies is a potentially flexible mechanism of non‐genetic inheritance by which mothers could favour some offspring over others and/or increase offspring survival, but this is a phenomenon that remains poorly understood. We examined sex‐specific deposition of maternal antibodies and its effects on early (5 d) and fledging (17 d) survival in semiprecocial chicks of the gull‐billed tern Gelochelidon nilotica, a long‐distance migratory bird. Mothers transferred a significantly greater amount of maternal antibodies to sons than to daughters. We found evidence for positive associations between maternal antibody levels at hatching and early offspring survival. This association might be sex‐specific, which can be understood as a mechanism of parental favouritism for the most sensitive sex.     

The Trade-Off between Female Fertility and Longevity during the Epidemiological Transition in the Netherlands

Several hypotheses have been put forward to explain the relationship between women’s fertility and their post-reproductive longevity. In this study, we focus on the disposable soma theory, which posits that a negative relationship between women’s fertility and longevity can be understood as an evolutionary trade-off between reproduction and survival. We examine the relationship between fertility and longevity during the epidemiological transition in the Netherlands. This period of rapid decline in mortality from infectious diseases offers a good opportunity to study the relationship between fertility and longevity, using registry data from 6,359 women born in The Netherlands between 1850 and 1910. We hypothesize that an initially negative relationship between women’s fertility and their longevity gradually turns less negative during the epidemiological transition, because of decreasing costs of higher parities. An initially inversed U-shaped association between fertility and longevity changes to zero during the epidemiological transition. This does suggest a diminishing environmental pressure on fertility. However, we find no evidence of an initial linear trade-off between fertility and post-reproductive survival.     

Early weaning in bighorn sheep, Ovis canadensis affects growth of males but not of females

Theories of parental investment and parent-offspring conflictassume that investment involves a cost to the parent and a benefitto the offspring, but for herbivorous mammals, behavioral andnutritional weaning are gradual processes that are difficultto define, and little is known about the consequences of individualvariation during weaning. To study the effects of late maternalcare on offspring fitness, we removed female bighorn sheep (Oviscanadensis) from a marked population in Alberta, Canada, andmonitored the survival, growth, and reproductive success oforphan and nonorphan lambs. Mothers were removed when lambswere 3.5–4.0 months, about 2–4 weeks before thesuspected time of nutritional weaning. Femaleorphans and nonorphanshad the same weight as yearlings, the same probability of producingtheir first lamb at 2 years of age, the same lifetime reproductivesuccess (lambs produced or lambs that survived to early autumn),and the same longevity. Male orphans from most cohorts weresmaller as yearlings compared to nonorphans from the same cohort.They were unable to compensate for this early weight differencein later life: at 4 years, orphan males had smaller horns andwere lighter than nonorphans. Small horn and body size likelylowered the reproductive success of orphaned males comparedto nonorphans from the same cohort. We suggest that in thissexually dimorphic species late maternal care is more importantfor males than for females. Because late maternal care had nomeasurable benefit for daughters, we suggest that parent-offspringconflict over the duration of maternal care may not exist formother-daughter pairs. or mother-son pairs it remains to beshown whether late maternal care involves a cost to the mother,but the assumption of a benefit to the son was met.     

Beautiful parents have more daughters: a further implication of the generalized Trivers-Willard hypothesis (gTWH)

The generalized Trivers-Willard hypothesis (gTWH) [Kanazawa, S., 2005. Big and tall parents have more sons: further generalizations of the Trivers-Willard hypothesis. J. Theor. Biol. 235, 583-590) proposes that parents who possess any heritable trait which increases the male reproductive success at a greater rate than female reproductive success in a given environment will have a higher-than-expected offspring sex ratio, and parents who possess any heritable trait which increases the female reproductive success at a greater rate than male reproductive success in a given environment will have a lower-than-expected offspring sex ratio. One heritable trait which increases the reproductive success of daughters much more than that of sons is physical attractiveness. I therefore predict that physically attractive parents have a lower-than-expected offspring sex ratio (more daughters). Further, if beautiful parents have more daughters and physical attractiveness is heritable, then, over evolutionary history, women should gradually become more attractive than men. The analysis of the National Longitudinal Study of Adolescent Health (Add Health) confirm both of these hypotheses. Very attractive individuals are 26% less likely to have a son, and women are significantly more physically attractive than men in the representative American sample.     

Evolution of the human menopause

Menopause is an evolutionary puzzle since an early end to reproduction seems contrary to maximising Darwinian fitness. Several theories have been proposed to explain why menopause might have evolved, all based on unusual aspects of the human life history. One theory is that menopause follows from the extreme altriciality of human babies, coupled with the difficulty in giving birth due to the large neonatal brain size and the growing risk of child-bearing at older ages. There may be little advantage for an older mother in running the increased risk of a further pregnancy when existing offspring depend critically on her survival. An alternative theory is that within kin groups menopause enhances fitness by producing post-reproductive grandmothers who can assist their adult daughters. Such theories need careful quantitative assessment to see whether the fitness benefits are sufficient to outweigh the costs, particularly in circumstances of relatively high background mortality typical of ancestral environments. We show that individual theories fail this test, but that a combined model incorporating both hypotheses can explain why menopause may have evolved.     

Expression and modulation of embryonic male-killing in Drosophila innubila: opportunities for multilevel selection

Organisms and the symbionts they harbor may experience opposing forces of selection. In particular, the contrasting inheritance patterns of maternally transmitted symbionts and their host's nuclear genes can engender conflict among organizational levels over the optimal host offspring sex ratio. This study uses a male-killing Wolbachia endosymbiont and its host Drosophila innubila to experimentally address the potential for multilevel selection in a host-symbiont system. We show that bacterial density can vary among infected females, and that females with a higher density have a more female-biased offspring sex ratio. Furthermore, bacterial density is an epigenetic and heritable trait: females with a low bacterial load have daughters with a lower-than-average bacterial density, whose offspring then experience less severe male-killing. For infected sons, the probability of embryonic mortality increases with the bacterial density in their mothers. The frequency distribution of Wolbachia density among individual D. innubila females, and therefore the dynamics of infection within populations of these flies, results both from processes affecting the growth and regulation of bacterial populations within cytoplasmic lineages and from selection among cytoplasmic lineages that vary in bacterial density. Estimates of effective population size of Wolbachia within cytoplasmic lineages and of D. innubila at the host population level suggest that selection among cytoplasmic lineages is likely to overwhelm the results of selection within lineages.     

Female reproductive competition within families in rural Gambia

Many studies show that the extended human family can be helpful in raising offspring, with maternal grandmothers, in particular, improving offspring survival. However, less attention has been given to competition between female kin and co-residents. It has been argued that reproductive conflict between generations explains the evolution of menopause in cooperatively breeding species where females disperse, and that older females are related to the offspring of younger females through their sons, whereas younger, incoming females are unrelated to older females. This means the pattern of help will be asymmetric, so older females lose in reproductive conflict and become 'sterile helpers'. Here, we seek evidence for female reproductive competition using longitudinal demographic data from a rural Gambian population, and examine when women are helping or harming each other's reproductive success. We find that older women benefit and younger women suffer costs of reproductive competition with women in their compound. But the opposite is found for mothers and daughters; if mother and daughter's reproductive spans overlap, the older woman reduces her reproduction if the younger woman (daughter) reproduces, whereas daughters' fertility is unaffected by their mothers' reproduction. Married daughters are not generally co-resident with their mothers, so we find not only competition effects with co-resident females, but also with daughters who have dispersed. Dispersal varies across human societies, but our results suggest reproductive conflict could be influencing reproductive scheduling whatever the dispersal pattern. A cultural norm of late male marriage reduces paternal grandmother/daughter-in-law reproductive overlap almost to zero in this population. We argue that cultural norms surrounding residence and marriage are themselves cultural adaptations to reduce reproductive conflict between generations in human families.     

Different optimal offspring sizes for sons versus daughters may favor the evolution of temperature-dependent sex determination in viviparous lizards

Temperature-dependent sex determination (TSD) has evolved independently in at least two lineages of viviparous Australian scincid lizards, but its adaptive significance remains unclear. We studied a montane lizard species (Eulamprus heatwolei) with TSD. Our data suggest that mothers can modify the body sizes of their offspring by selecting specific thermal regimes during pregnancy (mothers with higher and more stable temperatures produced smaller offspring), but cannot influence sons versus daughters differentially in this way. A field mark-recapture study shows that optimal offspring size differs between the sexes: larger body size at birth enhanced the survival of sons but reduced the survival of daughters. Thus, a pregnant female can optimize the fitness of either her sons or her daughters (via yolk allocation and thermoregulation), but cannot simultaneously optimize both. One evolutionary solution to reduce this fitness cost is to modify the sex-determining mechanism so that a single litter consists entirely of either sons or daughters; TSD provides such a mechanism. Previous work has implicated a sex difference in optimal offspring size as a selective force for TSD in turtles. Hence, opposing fitness determinants of sons and daughters may have favored evolutionary transitions from genetic sex determination to TSD in both oviparous turtles and viviparous lizards.     

Violent men have more sons: further evidence for the generalized Trivers-Willard hypothesis (gTWH)

The generalized Trivers-Willard hypothesis (gTWH) [Kanazawa, S., 2005a. Big and tall parents have more sons; further generalizations of the Trivers-Willard hypothesis. J. Theor. Biol. 235, 583-590] proposes that parents who possess any heritable trait which increases the male reproductive success at a greater rate than female reproductive success in a given environment have a higher-than-expected offspring sex ratio, and parents who possess any heritable trait which increases the female reproductive success at a greater rate than male reproductive success in a given environment have a lower-than-expected offspring sex ratio. One heritable trait which increases the reproductive success of sons significantly more than that of daughters in the ancestral environment is the tendency toward violence and aggression. I therefore predict that violent parents have a higher-than-expected offspring sex ratio (more sons). The analysis of both American samples and a British sample demonstrates that battered women, who are mated to violent men, have significantly more sons than daughters.     

Variation in Male Reproductive Longevity across Traditional Societies

Most accounts of human life history propose that women have short reproductive spans relative to their adult lifespans, while men not only remain fertile but carry on reproducing until late life. Here we argue that studies have overlooked evidence for variation in male reproductive ageing across human populations. We apply a Bayesian approach to census data from Agta hunter-gatherers and Gambian farmers to show that long post-reproductive lifespans characterise not only women but also males in some traditional human populations. We calculate three indices of reproductive ageing in men (oldest age at reproduction, male late-life reproduction, and post-reproductive representation) and identify a continuum of male reproductive longevity across eight traditional societies ranging from !Kung, Hadza and Agta hunter-gatherers exhibiting low levels of polygyny, early age at last reproduction and long post-reproductive lifespans, to male Gambian agriculturalists and Turkana pastoralists showing higher levels of polygyny, late-life reproduction and shorter post-reproductive lifespans. We conclude that the uniquely human detachment between rates of somatic senescence and reproductive decline, and the existence of post-reproductive lifespans, are features of both male and female life histories, and therefore not exclusive consequences of menopause.     

The evolution of polyandry: patterns of genotypic variation in female mating frequency, male fertilization success and a test of the sexy-sperm hypothesis

The sexy-sperm hypothesis predicts that females obtain indirect benefits for their offspring via polyandy, in the form of increased fertilization success for their sons. I use a quantitative genetic approach to test the sexy-sperm hypothesis using the field cricket Teleogryllus oceanicus. Previous studies of this species have shown considerable phenotypic variation in fertilization success when two or more males compete. There were high broad-sense heritabilities for both paternity and polyandry. Patterns of genotypic variance were consistent with X-linked inheritance and/or maternal effects on these traits. The genetic architecture therefore precludes the evolution of polyandry via a sexy-sperm process. Thus the positive genetic correlation between paternity in sons and polyandry in daughters predicted by the sexy-sperm hypothesis was absent. There was significant heritable variation in the investment by females in ovaries and by males in the accessory gland. Surprisingly there was a very strong genetic correlation between these two traits. The significance of this genetic correlation for the coevolution of male seminal products and polyandry is discussed.     

Probing the evolution of senescence inDrosophila melanogaster withP-element tagging

Natural populations host a wealth of genetic variation in longevity and age-specific schedules of reproduction. This variation provides critical information for inferring the evolutionary origin of senescence. Patterns of mutational effects on age-specific fecundity and survival provide additional insight to distinguish alternative models of senescence. In this study,P-elements bearing thewhite minigene were inserted at random into a common genetic background, generating lines ofD. melanogaster with single, stable transposon inserts. A series of 48 single-P-element lines revealed statistically significant heterogeneity in both longevity and fecundity. Longevity and early fecundity were only weakly positively correlated (r=0.286,P=0.0398). Both the pooled sample and 30 of the individual lines exhibited a leveling of age-specific mortality at advanced ages, in opposition to the classical demographic models. To the extent that these mutational effects are representative of naturally-occurring mutations in heterogeneous populations, this result presents a problem for the evolutionary theory of senescence. Natural selection is inefficient at removing deleterious mutations that are expressed only at late ages, and selection may not differentiate between mutations whose effects on longevity are post-reproductive. A leveling of the mortality rate would also be seen if mutations whose expression is delayed until very late simply do not occur. A simulation of mutation-selection balance among the 48P-element tagged lines shows that the mean longevity declines monotonically with increasing mutation rate, consistent with the mutation-accumulation model.     

Spatial analysis of the aptitude to late maternity on the island of Sardinia

This study examines local heterogeneity in the aptitude of Sardinian mothers towards late reproduction, and explores its temporal persistence and association with both post-reproductive longevity and propensity to consanguineous marriage. Data on women's fertility from 1961 and birth records for 1980-1996 from Vital Statistics were analysed by means of the following indicators: the incidence of old mothers at last childbirth, female mortality (1980-2001) at 80 years of age and over and the proportion of consanguineous marriages (1930-1969). A variable kernel-smoothing method was used to create interpretable representations of the true spatial structure of the indicators, and to highlight areas of higher than expected intensity. In particular, an area of reproductive and post-reproductive longevity was identified where the traits combine with a higher tendency to relatedness. Intriguingly, this area corresponds approximately to the geographically and historically well defined central-eastern zone, which was the refuge of Sardinians during past invasions, and overlaps the Ogliastra region, which has been widely studied for its genetic homogeneity.     

Female reproductive success in captive Ammotragus lervia (Bovidae, Artiodactyla). Study of its components and effects of hierarchy and inbreeding

Four components of female reproductive success in captive Saharan arrui (Barbary sheep), Ammotragus lervia sahariensis (Rothschild, 1913), have been analysed: longevity, fecundity, offspring one-month survival rate and the age at first birth. Longevity accounts for 69.9% of the variance of reproductive success, fecundity for 54.2%, offspring one-month survival rate for 29.8%, and the age at first birth for 10.4%. A detailed study of these components leads to the following conclusions: (a) longevity is higher in those individuals in better physical condition; (b) fecundity is related to age and social rank; (c) heavier offspring at birth have a higher probability of surviving during their first month of life; and (d) the age at first birth is delayed by high levels of population density, inbreeding coefficients, and birth weights. On the other hand, highranking females are characterized by shorter inter-birth intervals and give birth to a higher proportion of twins.