Grandmothering and natural selection

Humans are unique among primates in that women regularly outlive their reproductive period by decades. The grandmother hypothesis proposes that natural selection increased the length of the human post-menopausal period—and, thus, extended longevity—as a result of the inclusive fitness benefits of grandmothering. However, it has yet to be demonstrated that the inclusive fitness benefits associated with grandmothering are large enough to warrant this explanation. Here, we show that the inclusive fitness benefits are too small to affect the evolution of longevity under a wide range of conditions in simulated populations. This is due in large part to the relatively weak selection that applies to women near or beyond the end of their reproductive period. However, we find that grandmothers can facilitate the evolution of a shorter reproductive period when their help decreases the weaning age of their matrilineal grandchildren. Because selection favours a shorter reproductive period in the presence of shorter interbirth intervals, this finding holds true for any form of allocare that helps mothers resume cycling more quickly. We conclude that while grandmothering is unlikely to explain human-like longevity, allocare could have played an important role in shaping other unique aspects of human life history, such as a later age at first birth and a shorter female reproductive period.     

Increased longevity evolves from grandmothering

Postmenopausal longevity may have evolved in our lineage when ancestral grandmothers subsidized their daughters'' fertility by provisioning grandchildren, but the verbal hypothesis has lacked mathematical support until now. Here, we present a formal simulation in which life spans similar to those of modern chimpanzees lengthen into the modern human range as a consequence of grandmother effects. Greater longevity raises the chance of living through the fertile years but is opposed by costs that differ for the sexes. Our grandmother assumptions are restrictive. Only females who are no longer fertile themselves are eligible, and female fertility extends to age 45 years. Initially, there are very few eligible grandmothers and effects are small. Grandmothers can support only one dependent at a time and do not care selectively for their daughters'' offspring. They must take the oldest juveniles still relying on mothers; and infants under the age of 2 years are never eligible for subsidy. Our model includes no assumptions about brains, learning or pair bonds. Grandmother effects alone are sufficient to propel the doubling of life spans in less than sixty thousand years.     

Grandmothers' longevity negatively affects daughters' fertility

The evolution of postmenopausal longevity in human females has been the subject of debate. Specifically, there is disagreement about whether the evolution of the trait should be understood as an adaptive or a neutral process, and if the former, what the selective mechanism is. There are two main adaptive proposals to explain the evolution of postreproductive longevity: the grandmother and the mother hypotheses. The grandmother hypothesis proposes that postreproductive longevity evolved because it is selectively advantageous for females to stop reproducing and to help raise their grandchildren. The mother hypothesis states that postmenopausal longevity evolved because it is advantageous for women to cease reproduction and concentrate their resources and energy in raising the children already produced. In this article, we test the mother and the grandmother hypotheses with a historical data set from which we bootstrapped random samples of women from different families who lived from the 1500s to the 1900s in the central valley of Costa Rica. We also compute the heritability of longevity, which allows us to determine if genes involved in longevity are nearly fixed in this population. Here we show that although longevity positively affects a woman's fertility, it negatively affects her daughter's fertility; for this reason, the heritability of longevity is unexpectedly high. Our data provide strong grounds for questioning the universality of the grandmother hypothesis and for supporting the mother hypothesis as a likely explanation for the evolution of human postreproductive longevity.     

Brief communication: Evaluating grandmother effects

Women who have outlived child‐bearing have long been described as postreproductive. But contributions they make to the survival or fertility of their descendants enhance the reproduction of their genes. Consequently, natural selection affects this characteristic stage of human life history. Grandmother effects can be measured in data sets that include births and deaths over several generations, but unmeasured covariates complicate the task. Here we focus on two complications: cohort shifts in mortality and fertility, and maternal age at death. We use the Utah Population Database to show that longevity of grandmothers may be associated with fewer grandchildren, as reported by Madrigal and Melendez‐Obando (Am J Phys Anthropol 136 (2008) 223–229) for a Costa Rican sample, even when grandmother effects are actually positive. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

Do grandparents favor granddaughters? Biased grandparental investment in UK

Differential grandparental investment in grandchildren is often explained with paternity uncertainty. The asymmetric inheritance of the sex chromosomes, especially of the X chromosomes, may also bias grandparental investment. Recent studies show that ignoring the sex of the grandchild can mask important differences in the investment patterns of the same grandparent category, but this has not been tested in contemporary societies with nationally representative data. With 17 variables from the Involved Grandparenting and Child Well-Being 2007 survey, we tested differential grandparental investment as reported by British and Welsh adolescents and compared predictions based on X-chromosomal relatedness with predictions based on paternity uncertainty. The theories are expected to differ with regard to grandmaternal investment in grandsons and granddaughters. We test whether paternal grandmothers invest (H1) more in granddaughters than in grandsons, (H2) more in granddaughters than maternal grandmothers do and (H3) less in grandsons than maternal grandmothers do. In addition, following the suggestion that paternal grandmothers may reduce sibling competition between girls and boys by harming grandsons, we study whether (H4) paternal grandmothers channel more noninvestment into grandsons than into granddaughters. The results show no convincing support for the type of sex discrimination of grandchildren that is predicted by X-chromosomal relatedness theories, but do provide support for the paternity uncertainty theory. X-chromosomal relatedness does not appear to shape grandparental behavior in developed societies.     

Availability and adaptive value of reproductive and postreproductive Japanese macaque mothers and grandmothers

Prior tests of the grandmother hypothesis have suggested that postreproductive female Japanese macaques,Macaca fuscata , do not significantly improve the survivorship of their descendents. However, not all postreproductive females are grandmothers, and not all grandmothers are postreproductive. In this study we looked at the daughters and grandchildren of 70 female Japanese macaques to assess the availability and adaptive value of reproductive and postreproductive mothers and grandmothers. We found that postreproductive Japanese macaque grandmothers are very rare. Only 2.8% of the sample of daughters had a postreproductive grandmother available when they began to reproduce, and only 4.2% of the reproductive life span of the daughter (less than 6 months for the average female) was spent with a postreproductive grandmother available to help the daughter. Grandchildren who survived to age 5 had a postreproductive grandmother available to them for only 4% of the first 5 years of life (i.e. a couple of months on average). The presence of a living mother, irrespective of her reproductive status, was associated with improved reproduction in her adult daughters, and the presence of a postreproductive grandmother was associated with significantly improved survivorship of grandchildren to age 1. While improved maternal investment does not appear to be the primary explanation for reproductive termination in Japanese monkeys, the few postreproductive females that have unweaned grandchildren available appear to have a positive influence on their survival. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Transgenerational health effects of in utero exposure to economic hardship: Evidence from preindustrial Southern Norway

We studied whether in utero exposure to economic hardship during a grandmother’s pregnancy has a transgenerational effect on her grandchildren's health condition. We used an individual-level three-generation data set covering people born between 1734 and 1840 in the municipality of Rendalen in Norway. We found a culling effect in which grandchildren whose grandmothers gave birth in years of economic hardship lived approximately ten years longer than grandchildren whose mothers were born in years of economic well-being. This impact was only observed among the grandmothers who belong to the lowest social classes. Our results also showed that in higher social classes, economic hardship during a grandmother’s pregnancy deteriorated her grandchildren’s health by “scarring” the mother’s health.     

Will granny save me? Birth status,survival, and the role of grandmothers in historical Finland

Grandmothers play a crucial role in families enhancing grandchild wellbeing and survival but their effects can be context-dependent, and the children born in poor conditions are most likely to benefit from the investments made by helping grandmothers. In this study, we examined, for the first time, whether grandmothers' presence modified associations between adverse birth status and survival up to 5 years of age. In detail, we verified, whether (i) firstborns, (ii) twins, (iii) children born within 24 months after their sibling, and (iv) children followed by short interval (i.e. their younger sibling was born within 24 months) survived better when either their maternal, paternal, or both grandmothers were present. Moreover, we evaluated whether illegitimate children survived better when the maternal grandmother was present. We used an extensive and largely pre-industrial demographic dataset collected from parish population registers kept by the Lutheran Church of Finland from years 1730–1895. We show that although grandmother presence cannot mitigate adverse effects of many poorer birth conditions, grandchildren whose next sibling was born after a short interval survived better when the maternal grandmother was present. Taken together, these findings highlight an important role of grandmothers in compensating the mother's investment in the new baby, thus enabling overall faster successful reproductive rate of mothers. Whilst the opportunity for grandmothers to mitigate the risks of adverse birth statuses is limited, this study does show - through the beneficial effect on survival for those with a short subsequent birth interval - that grandmothers can increase their daughters' and their own reproductive success.     

Of love and fur: grandmothers,class, and pre‐mortem inheritance in a southern Polish city

This article analyses the pre‐mortem alternate‐generation inheritance of fur clothing in Kraków: a practice that speaks to the conventions of grandmother‐granddaughter relationships and also to the connection between inheritance and social class. The perception of fur as a symbolically loaded material enhances its suitability for being ‘kept in the family’. Clothing inheritance fosters bourgeois belonging over multiple generations, encouraging the patronage of selected spaces and services (including furriers). In the shorter term, however, generational differences within amicable grandmother‐granddaughter pairs are amplified in part through the way pre‐mortem inheritance practices highlight granddaughters' non‐reciprocable debt to their grandmothers. A focus on fur as a particular kind of object highlights the significance of certain inheritance practices and their links to the affective ties in the reproduction of class in Poland. The article also contributes to a broader understanding of the reproduction of class by analysing the interconnections between taste, the body, and memory.     

Maternal grandmothers improve nutritional status and survival of children in rural Gambia

Hypotheses for the evolution of human female life-history characteristics have often focused on the social nature of human societies, which allows women to share the burden of childcare and provisioning amongst other members of their kin group. We test the hypothesis that child health and survival probabilities will be improved by the presence of kin using a longitudinal database from rural Gambia. We find that the only kin to improve the nutritional status of children significantly (apart from mothers) are maternal grandmothers, and that this is reflected in higher survival probabilities for children with living maternal grandmothers. There is also evidence that the reproductive status of the maternal grandmother influences child nutrition, with young children being taller in the presence of non-reproductive grandmothers than grandmothers who are still reproductively active. Paternal grandmothers and male kin, including fathers, have negligible impacts on the nutritional status and survival of children.     

Old grandmothers provide essential care to their young granddaughters in a free-ranging group of Japanese monkeys (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

This study reports 2 cases in which old grandmothers without dependent offspring provided essential care to their young granddaughters in a free-ranging group of Japanese monkeys (Macaca fuscata). In the first case, a 24-year-old grandmother provided essential care for the survival of her 2-month-old granddaughter for at least 6 days during which the mother had temporarily disappeared from the group for reasons unknown. In the second case, a 14-month-old granddaughter began sucking from her 23-year-old grandmother within 6 weeks after her mother gave birth to a younger sibling. For at least 6 months, the grandmother exhibited various patterns of maternal behavior toward her granddaughter. The behavioral data obtained in this study indicated that old yet healthy females without dependent offspring could contribute to the survival of their young grandchildren.     

Patterns of grandmaternal behaviour in free-ranging Hanuman langurs (Presbytis entellus)

The behaviour of two Hanuman langur grandmothers towards their grandchildren is examined with emphasis on the spatial relationship, the contact behaviour, and vigilance. Interaction patterns with infants and juveniles are analysed separately to disclose the influence of a social partner's reproductive value and the variance of this value on grandmaternal behaviour. The shape of grandmaternal behaviour seems to differ for male and female grandchildren, and it seems to depend on the reproductive value of both, the grandmother and the grandchild. These results are in accordance with sociobiological hypotheses. Evaluation of costs and benefits suggests that grandmaternal behaviour in langurs can be called investment.     

The effects of kin propinquity on infant mortality

This study tests the grandmother hypothesis and analyzes the effect of kin propinquity on infant mortality in a 19th century American frontier communal, polygynous population. The study shows that the presence of maternal grandmothers, aunts, uncles, and paternal aunts were significantly associated with increased infant survivorship while grandfathers, paternal grandmothers, and paternal uncles showed little effect. This study has implications for understanding the evolution of a long postreproductive life span, postmarital residential strategies, and behavioral strategies that enhance inclusive fitness.     

Caregiving within and beyond the family is associated with lower mortality for the caregiver: A prospective study

Grandparenting has been proposed as an ultimate evolutionary mechanism that has contributed to the increase in human life expectancy (see the grandmother hypothesis). The neural and hormonal system – originally rooted in parenting and thus grandparenting – that is activated in the process of caregiving has been suggested as a potential proximate mechanism that promotes engagement in prosocial behavior towards kin and non-kin alike. Evidence and theory suggest that activating this caregiving system positively impacts health and may reduce the mortality of the helper. Although some studies have found grandparental care to have beneficial effects on grandparents' health outcomes, most studies have focused on the detrimental health consequences of providing custodial care for grandchildren. Little is known about how non-custodial grandparental and other forms of caregiving relate to mortality hazards for the care provider. Using an evolutionary framework, we examined whether caregiving within and beyond the family is related to mortality in older adults. Survival analyses based on data from the Berlin Aging Study revealed that mortality hazards for grandparents who provided non-custodial childcare were 37% lower than for grandparents who did not provide childcare and for non-grandparents. These associations held after controlling for physical health, age, socioeconomic status and various characteristics of the children and grandchildren. Furthermore, the effect of caregiving extended to non-grandparents and to childless older adults who helped beyond their families. Potential ultimate and proximate mechanisms underlying these effects are discussed.     

Lineage, Sex, and Wealth as Moderators of Kin Investment

Supporting Hamilton’s inclusive fitness theory, archival analyses of inheritance patterns in wills have revealed that people invest more of their estates in kin of closer genetic relatedness. Recent classroom experiments have shown that this genetic relatedness effect is stronger for relatives of direct lineage (children, grandchildren) than for relatives of collateral lineage (siblings, nieces, nephews). In the present research, multilevel modeling of more than 1,000 British Columbian wills revealed a positive effect of genetic relatedness on proportions of estates allocated to relatives. This effect was qualified by an interaction with lineage, such that it was stronger for direct than for collateral relatives. Exploratory analyses of the moderating role of benefactors’ sex and estate values showed the genetic relatedness effect was stronger among female and wealthier benefactors. The importance of these moderators to understanding kin investment in modern humans is discussed.     

An evolutionary perspective on the association between grandmother-mother relationships and maternal mental health among a cohort of pregnant Latina women

Grandmothers are often critical helpers during a mother's reproductive career. Studies on the developmental origins of health and disease demonstrate how maternal psychological distress can negatively influence fetal development and birth outcomes, highlighting an area in which soon-to-be grandmothers (henceforth “grandmothers”) can invest to improve both mother and offspring well-being. Here, we examine if and how a pregnant woman's mental health– specifically, depression, state-anxiety, and pregnancy-related anxiety– is influenced by her relationship with her fetus' maternal and paternal grandmother, controlling for relationship characteristics with her fetus' father. In a cohort of pregnant Latina women in Southern California (N = 216), we assessed social support, geographic proximity, and communication between the fetus' grandmothers and pregnant mother. We assessed maternal mental health with validated questionnaire-based instruments. We find that both social support from and communication with the maternal grandmother were statistically associated with less depression, while no paternal grandmother relationship characteristics were statistically significant in association with any mental health variable. These results align with the idea that maternal grandmothers are more adaptively incentivized to invest in their daughters' well-being during pregnancy than paternal grandmothers are for their daughters-in-law. Results suggest that the positive association of maternal grandmothers with mothers' mental health may not hinge on geographic proximity, but rather, potentially function through emotional support. This work represents a novel perspective describing a psychological and prenatal grandmaternal effect.     

Human aging and somatic point mutations in mtDNA: A comparative study of generational differences (grandparents and grandchildren)

The accumulation of somatic mutations in mtDNA is correlated with aging. In this work, we sought to identify somatic mutations in the HVS-1 region (D-loop) of mtDNA that might be associated with aging. For this, we compared 31 grandmothers (mean age: 63 ± 2.3 years) and their 62 grandchildren (mean age: 15 ± 4.1 years), the offspring of their daughters. Direct DNA sequencing showed that mutations absent in the grandchildren were detected in a presumably homoplasmic state in three grandmothers and in a heteroplasmic state in an additional 13 grandmothers; no mutations were detected in the remaining 15 grandmothers. However, cloning followed by DNA sequencing in 12 grandmothers confirmed homoplasia in only one of the three mutations previously considered to be homoplasmic and did not confirm heteroplasmy in three out of nine grandmothers found to be heteroplasmic by direct sequencing. Thus, of 12 grandmothers in whom mtDNA was analyzed by cloning, eight were heteroplasmic for mutations not detected in their grandchildren. In this study, the use of genetically related subjects allowed us to demonstrate the occurrence of age-related (> 60 years old) mutations (homoplasia and heteroplasmy). It is possible that both of these situations (homoplasia and heteroplasmy) were a long-term consequence of mitochondrial oxidative phosphorylation that can lead to the accumulation of mtDNA mutations throughout life.     

Age-specific changes in epistatic effects on mortality rate in Drosophila melanogaster

Models for the evolution of senescence assume that genes with age-specific effects act independently of one another. Although recent empirical data show that longevity is influenced in part by interactions between genes, there are currently few data on whether epistasis influences age-specific components of mortality. To gauge if and how interactions affect age-specific traits, we incorporated the Drosophila visible marker mutations ebony, forked, and purple into seven wild-caught strains of D. melanogaster to examine gene x genetic background interactions. We found significant natural genetic variation for longevity and baseline mortality rates. Gene x genetic background interactions were prevalent not only for longevity but also for baseline mortality rates and age-specific mortality rates. We conclude that gene x genetic background epistasis is prevalent for aging-related traits and could play a significant role in the evolution of aging. These results suggest that future genetic models for the evolution of aging should incorporate the effects of epistasis.     

Dynamics of the caring family

When several individuals simultaneously provide for offspring, as in families, the effort of any one individual will depend on the efforts of the other family members. This conflict of interest among family members is made more complicated by their relatedness because relatives share genetic interest to some degree. The conflict resolution will also be influenced by the differences in reproductive value between breeders and helpers. Here, we calculate evolutionarily stable provisioning efforts in families with up to two helpers. We explicitly consider that the behavioral choices are made in a life-history context, and we also consider how group sizes change dynamically; this affects, for example, average relatedness among group members. We assume two different scenarios: intact families in which the breeder is 100% monogamous and stepfamilies in which the breeder shifts mate between breeding events. The average relatedness among family members is allowed to evolve in concert with changes in provisioning effort. Our model shows that an individual's provisioning effort is not easy to predict from either its relatedness to the offspring or its reproductive value. Instead, it is necessary to consider the inclusive fitness effect of provisioning, which is determined by a combination of relatedness, reproductive value, and the reproductive value of the offspring.     

Grandmothers and the evolution of human longevity: A review of findings and future directions

Women and female great apes both continue giving birth into their forties, but not beyond. However humans live much longer than other apes do. 1 Even in hunting and gathering societies, where the mortality rate is high, adult life spans average twice those of chimpanzees, which become decrepit during their fertile years and rarely survive them. 2 , 3 Since women usually remain healthy through and beyond childbearing age, human communities include substantial proportions of economically productive postmenopausal women. 4 - 7 A grandmother hypothesis^8–12 may explain why greater longevity evolved in our lineage while female fertility still ends at ancestral ages. This hypothesis has implications for the evolution of a wide array of human features. Here we review some history of the hypothesis, recent findings, and questions for ongoing research.