Is There Adaptive Value to Reproductive Termination in Japanese Macaques? A Test of Maternal Investment Hypotheses

Evolutionary biologists often argue that menopause evolved in the human female as the result of selection for a postreproductive phase of life, during which increased maternal investment in existing progeny could lead to enhanced survivorship of descendents. Adaptive theories relating menopause to enhanced maternal investment are known as the mother (first-generation) and grandmother (second-generation-offspring) hypotheses. Although menopause—universal midlife termination of reproduction—has not been documented in primates other than humans, some researchers have argued that postreproductive alloprimates also have a positive impact on the survivorship of first and second generation progeny. We tested the maternal investment hypotheses in Japanese macaques by comparing the survivorship of offspring, final infants, and great-offspring of females that terminated reproduction before death with females that continued to reproduce until death. SURVIVAL analyses revealed no significant difference in the survivorship of descendents of postreproductive and reproductive females, though final infants of postreproductive females were 13% more likely to survive than final infants of females that reproduced until death were. We also explored possible differences between these two groups of females, other than survivorship of progeny. We found no difference in dominance rank, matrilineal affiliation, body weight, infant sex ratio, age at first birth, fecundity rate or lifetime reproductive success. However, postreproductive females are significantly longer-lived than reproductive females and as a result experienced more years of reproduction and produced more infants in total. Apart from final infants, offspring survival is marginally lower in postreproductive females. Since offspring survival is not significantly enhanced in postreproductive females, the greater number of infants produced did not translate into greater lifetime reproductive success. Our findings fail to support the maternal investment hypotheses and instead suggest that reproductive termination in this population of Japanese macaques is most closely associated with enhanced longevity and its repercussions.     

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.     

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.     

SELECTION ON MENOPAUSE IN TWO PREMODERN HUMAN POPULATIONS: NO EVIDENCE FOR THE MOTHER HYPOTHESIS

Evolutionary theory suggests that natural selection should synchronize senescence of reproductive and somatic systems. In some species, females show dramatic discordance in senescence rates in these systems, leading to a clear menopause coupled with prolonged postreproductive life span. The Mother Hypothesis proposes that menopause evolved to avoid higher reproductive‐mediated mortality risk in late‐life and ensure the survival of existing offspring. Despite substantial theoretical interest, the critical predictions of this hypothesis have never been fully tested in populations with natural fertility and mortality. Here, we provide an extensive test, investigating both short‐ and long‐term consequences of mother loss for offspring, using multigenerational demographic datasets of premodern Finns and Canadians. We found no support for the Mother Hypothesis. First, although the risk of maternal death from childbirth increased from middle age, the risk only reached 1–2% at age 50 and was predicted to range between 2% and 8% by 70. Second, offspring were adversely affected by maternal loss only in their first two years (i.e., preweaning), having reduced survival probability in early childhood as well as ultimate life span and fitness. Dependent offspring were not affected by maternal death following weaning, either in the short‐ or long‐term. We suggest that although mothers are required to ensure offspring survival preweaning in humans, maternal loss thereafter can be compensated by other family members. Our results indicate that maternal effects on dependent offspring are unlikely to explain the maintenance of menopause or prolonged postreproductive life span in women.     

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.     

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.     

Are all grandmothers equal? A review and a preliminary test of the “grandmother hypothesis” in Tokugawa Japan

An unresolved question arising from human evolutionary research relates to the function of the postreproductive period in human females. If menopause is not merely an artifact resulting from the benefits of civilization, there must be an adaptive mechanism favoring the offspring of women who continue to thrive well past the time of their last ovulation. The "grandmother hypothesis" was developed on the basis of the original suggestion by Williams (1957 Evolution 11:32-39) that "stopping early" would benefit already-born children. This idea, combined with the concepts of kin selection (Hamilton 1964 J Theor Biol 7:1-52) and parental investment (Trivers 1972 Sexual Selection and the Descent of Man, Chicago: Aldine, p. 136-179), was expanded to suggest that postreproductive women (in contrast to males) contribute to their inclusive fitness by extending support to their grandchildren. We used discrete time event history analysis (Allison [1984] Event History Analysis, Newbury Park: Sage; Allison [1995] Survival Analysis, Cary, NC: SAS Institute) and logistic regression on data provided in population registers (Shūmon Aratame Chō, or SAC) from a village in central Japan, covering the period from 1671-1871, in a preliminary investigation of the effects of household grandparental presence on the probability of a child's death. We found that after accounting for the presence of other household members, the only grandparent whose presence exerted a consistent negative effect on the likelihood of a child's death was the mother's mother. Due to the small sample size of households that contained maternal grandmothers, these results failed to achieve statistical significance. Their importance, however, is in what they suggest about future research, i.e., census data from preindustrial societies can provide a basis for testing evolutionary proposals, including the "grandmother hypothesis."     

Grandma plays favourites: X-chromosome relatedness and sex-specific childhood mortality

Biologists use genetic relatedness between family members to explain the evolution of many behavioural and developmental traits in humans, including altruism, kin investment and longevity. Women''s post-menopausal longevity in particular is linked to genetic relatedness between family members. According to the ‘grandmother hypothesis’, post-menopausal women can increase their genetic contribution to future generations by increasing the survivorship of their grandchildren. While some demographic studies have found evidence for this, others have found little support for it. Here, we re-model the predictions of the grandmother hypothesis by examining the genetic relatedness between grandmothers and grandchildren. We use this new model to re-evaluate the grandmother effect in seven previously studied human populations. Boys and girls differ in the per cent of genes they share with maternal versus paternal grandmothers because of differences in X-chromosome inheritance. Here, we demonstrate a relationship between X-chromosome inheritance and grandchild mortality in the presence of a grandmother. With this sex-specific and X-chromosome approach to interpreting mortality rates, we provide a new perspective on the prevailing theory for the evolution of human female longevity. This approach yields more consistent support for the grandmother hypothesis, and has implications for the study of human evolution.     

Adaptive co‐evolution of mitochondria and the Y‐chromosome: A resolution to conflict between evolutionary opponents

In most species with motile sperm, male fertility depends upon genes located on the Y‐chromosome and in the mitochondrial genome. Coordinated adaptive evolution for the function of male fertility between genes on the Y and the mitochondrion is hampered by their uniparental inheritance in opposing sexes: The Y‐chromosome is inherited uniparentally, father to son, and the mitochondrion is inherited maternally, mother to offspring. Preserving male fertility is problematic, because maternal inheritance permits mitochondrial mutations advantageous to females, but deleterious to male fertility, to accumulate in a population. Although uniparental inheritance with sex‐restricted adaptation also affects genes on the Y‐chromosome, females lack a Y‐chromosome and escape the potential maladaptive consequences of male‐limited selection. Evolutionary models have shown that mitochondrial mutations deleterious to male fertility can be countered by compensatory evolution of Y‐linked mutations that restore it. However, direct adaptive coevolution of Y‐ and mitochondrial gene combinations has not yet been mathematically characterized. We use population genetic models to show that adaptive coevolution of Y and mitochondrial genes are possible when Y‐mt gene combinations have positive effects on male fertility and populations are inbred.     

Evolution and ageing

Did senescence evolve as a direct result of natural selection in order to limit the life-span or did increases in longevity evolve in the face of random events that ordinarily limit the life-span? The adaptive hypothesis is that senescence is a programmed process which appeared in evolution because a limited life-span has selective advantages for certain species. Non-adaptive theorists hold that evolution has acted to lengthen the life-span and maximize reproduction and that senescence is only an evolutionary by-product since natural selection does not act directly on postreproductive events. The assumptions and arguments underlying these hypotheses are examined critically in the light of experimental evidence. While theoretical study of the evolution of ageing may advance our understanding of the nature of ageing itself, it is likely that further clarification of the relationship between evolution and ageing will depend on experimental approaches that are now becoming possible.     

An unusual incident of adoption in a wild chimpanzee (Pan troglodytes) population at Gombe National Park

Allomothering and adoption are well documented across primate species. Multiple hypotheses have been proposed to explain the evolution of such behavior according to the costs and benefits to the caregiver, mother, and infant. Permanent adoptions and allomothering have been observed in chimpanzees, but they typically involve the infants' siblings or nulliparous females. Here, I report a unique incident of adoption where an infant was adopted by its grandmother without the death of its mother. I conclude by considering how the adoption may have benefited the grandmother, mother, and infant.     

The Evolution of Reversed Sexual Size Dimorphism in Hawks,Falcons and Owls: A Comparative Study

Many hypotheses have been proposed to account for the origin and maintenance of reversed size dimorphism (RSD, females being larger than males) in hawks, falcons and owls, but no consensus has been reached. I performed comparative analyses, using both cross-taxa data and phylogenetically independent contrasts, to investigate potential correlates of reversed size dimorphism. Using a similar set of explanatory variables, covering morphology, life history and ecology, I tested whether any trait coevolved with size dimorphism in all three groups and hence provided a general explanation for the evolution of RSD. For hawks, strong correlates were found in the foraging-variable complex, so RSD might have evolved in species hunting large and agile prey. This is consistent with the intersexual-competition hypothesis (sexes have evolved different sizes to lessen intersexual competition for food), but especially the small-male hypothesis (males have evolved to be smaller to be more efficient foragers). Evolutionary pathway analyses suggest that RSD evolved most likely as a precursor of changes in hunting strategy but as a consequence of high reproduction. The falcons showed a similar pattern: species with strong RSD hunted larger and more agile prey. The evolutionary pathway analysis supported the idea that RSD evolved before the specialisation on more agile and/or larger prey. Finally for owls, the results showed clear parallels. RSD increased with prey size, consistent with the small-male hypothesis. Evolutionary pathway analysis suggests that RSD in owls has most likely evolved before specialisation on large prey, so a small and more agile male might be advantageous even when hunting small prey. These results suggest that RSD in hawks, falcons and owls evolved due to natural-selection pressures rather than sexual-selection pressures. Co-ordinating editor: J. Tuomi     

Heritability of fertility in human populations and the structure of Crow's index

Heritability of fertility was determined in populations with natural character of reproduction (Middle Asia Republics) and in populations with family planning (Middle Russia). The material was collected by interviewing the married women of postreproductive age. The heritability of fertility was estimated as a doubled coefficient of correlations between sisters for effective fertility. In populations with natural character of reproduction the heritability was about 50% and it did not differ from O in the populations with family planning. The values of heritability were used in the components of the Crow index analysis. The main contribution into broad-sense heritability of fertility comes from additive component, as shown in an Asia population (Turkmen). The values of heritability of fecundability (86%) and of postpartum sterility (66%) have been calculated for the same population.     

Can fertility signals lead to quality signals? Insights from the evolution of primate sexual swellings

The sexual swellings of female primates have generated a great deal of interest in evolutionary biology. Two hypotheses recently proposed to elucidate their functional significance argue that maximal swelling size advertises either female fertility within a cycle or female quality across cycles. Published evidence favours the first hypothesis, and further indicates that larger swellings advertise higher fertility between cycles. If so, a male preference for large swellings might evolve, driving females to use swellings as quality indicators, as proposed by the second hypothesis. In this paper, we explore this possibility using a combination of empirical field data and mathematical modelling. We first test and find support for three key predictions of the female-quality hypothesis in wild chacma baboons (Papio ursinus): (i) inter-individual differences in swelling size are maintained across consecutive cycles, (ii) females in better condition have larger swellings and higher reproductive success, and (iii) males preferentially choose females with large swellings. We then develop an individual-based simulation model that indicates that females producing larger swellings can achieve higher mating success even when female–female competition is low and within-female variance in the trait is high. Taken together, our findings show that once sexual swellings have evolved as fertility signals, they might, in certain socio-sexual systems, be further selected to act as quality signals. These results, by reconciling two hypotheses, help to clarify the processes underlying sexual swelling evolution. More generally, our findings suggest that mate choice for direct benefits (fertility) can lead to indirect benefits (good genes).     

Senescence of reproduction may explain adaptive menopause in humans: a test of the "mother" hypothesis

The "mother" hypothesis is one of the main adaptive explanations of human menopause. It postulates that reproductive cessation constitutes a strategy that has been selected for during human evolution because mothers at older ages might maximize their fitness by investing resources in the survival and reproduction of their living children rather than by continuing to reproduce. This study provides a test of this hypothesis. Fertility functions that maximize fitness are built into a model incorporating the fact that the survival of females during the rearing period is a major determinant of their children's survival. Results are given according to different scenarios of increase with mothers' age of maternal mortality risk and risk of stillbirth and birth defects (on the assumption that these females do not experience menopause). Different estimates of the effect of a mother's death on her child's survival were also incorporated. Finally, a population genetics framework allows us to estimate selection on these optimal fertility functions. To determine whether or not these fertility functions show a menopause, three criteria are discussed: the rapidity of fertility decline, if any; the magnitude of selection on menopause compared with a nonmenopausal strategy; and the selection on survival during post-reproductive life. Our results show that menopause and subsequent post-reproductive life are significantly advantageous when two conditions are satisfied: a marked increase in stillbirth and risk of birth defects as well as in maternal mortality with mother's age.     

A life history perspective on skin cancer and the evolution of skin pigmentation

The ancestral state of human skin pigmentation evolved in response to high ultraviolet radiation (UVR) stress. Some argue that pigmentation evolved to limit folate photolysis, therein limiting neural tube defects. Pigmentation also protects against sunburn which decreases the efficiency of sweating and potentiates skin infection. Pigmentation increases the efficacy of skin as a barrier to infection. Skin cancer has been rejected or minimized as a selective pressure because it is believed to have little or no effect on mortality during reproductive years. This argument ignores evidence of human longevity as a derived life history trait and the adaptive value of investment in offspring and kin, particularly during the post‐reproductive lifespan. Opponents argue that lifespan in prehistoric hunter‐gatherers was too short to be relevant to the evolution of skin pigmentation. This argument is flawed in that it relies on estimates of longevity at birth rather than adolescence. When appropriate estimates are used, it is clear that human longevity has a deep evolutionary history. We use a life history perspective to demonstrate the value of skin pigmentation as an adaptation to skin cancer with the following points: UVR exposure increases dysregulation of gene expression in skin cells leading to immortal cell lines; cutaneous malignant melanoma (CMM) affects individuals throughout reproductive years; and lifespan was longer than has previously been acknowledged, providing the opportunity for kin selection. This hypothesis is not at odds with the folate or barrier hypotheses. We stress that the evolution of skin pigmentation is complex and is an ongoing process. Am J Phys Anthropol 153:1–8, 2014. © 2013 Wiley Periodicals, Inc.     

Women’s work,child care,and helpers-at-the-nest in a hunter-gatherer society

Considerable research on helpers-at-the-nest demonstrates the positive effects of firstborn daughters on a mother’s reproductive success and the survival of her children compared with women who have firstborn sons. This research is largely restricted to agricultural settings. In the present study we ask: “Does ‘daughter first’ improve mothers’ reproductive success in a hunting and gathering context?” Through an analysis of 84 postreproductive women in this population we find that the sex of the first- or second-born child has no effect on a mother’s fertility or the survival of her offspring. We conclude that specific environmental and economic factors underlay the helpers-at-the-nest phenomenon.     

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.     

Human breasts: Unsupported hypotheses reviewed

Unlike other apes, human females’ breasts develop before first pregnancy and are permanently enlarged. Evidence suggests breasts act as signals to males but the critical data required to confirm this are lacking. These facts have led to a number of hypotheses about the evolutionary and adaptive significance of the human breast which fall into two groups. Those that address the presence of breasts in humans are (a) that they act as releasers of male sexual behaviour, (b) that they enable females to hide their reproductive condition, and (c) that they allow infants to nurse from their mother’s hip. Those that address variability in breast size are (d) that large breasts indicate lactational potential, (e) ability of mothers to invest prenatally in offspring, (f) mother’s fecundity, and (g) her longevity. Each hypothesis is reviewed and evaluated using logical or empirical arguments. Possible ways in which the adaptive significance of human breasts can be determined in contemporary populations are outlined.     

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.