Evolution of menopause

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Menopause is the permanent cessation of menstruation due to the loss of ovarian follicular activity.[1] Although the proximal causes of menopause are well understood the evolutionary causes remain unclear. When considered in the mammalian trajectory, menopause is an unusual life history trait. Although there has been some suggestive evidence reported in a few nonhuman primate species (see section 3), only toothed whales and human females are reported as having a true post reproductive life span. The cessation of reproduction seems counter intuitive to natural selection. According to natural selection, animals are expected to maximize their reproductive capabilities. In most instances this means reproducing until time of death. With menopause, human females can live up to fifty years beyond natural reproduction.


Determining the key variables resulting in the evolution of menopause has been challenging for scientists. A main constraint is the lack of fossilization in soft tissues such as reproductive organs. Indirect measures such as hormonal and bone density changes through osteoporosis, require a number of specimens that are not yet available. Most research into the evolution of menopause focuses on the trade offs between continuing reproduction late into life and ceasing reproduction prior to death.

The Evolution of a post-reproductive life span

Genetic factors of aging have been proposed and provide some insight into the aging process. In one experiment, laboratory animals from the same species but with different genomes were exposed to similar environmental pressures and had pronounced differences in their natural lifespans[2]. Natural experiments with human twins support these findings. Monozygotic twins lifespans were found to be statistically closer to one another’s than those of dizygotic twins, suggesting that over 25% of lifespan determination is genetic. The remaining 75% of variation not directly impacted by genetic factors is accounted for by behavioral and environmental differences[3].

All species of mammals have a geriatric stage of life. This stage is rarely achieved by non-captive individuals. Frail individuals exposed to environmental pressures are more likely to die of extrinsic causes than intrinsic ones. Extrinsic pressures that affect mortality include nutrition, disease, climate and environment. Humans have been able to offset the cost of extrinsic pressures for themselves through culturally acquired knowledge [2]. By controlling these factors human populations across the world have extended their lifespans.

Controlling extrinsic variables of survival, humans have been able to uncover mechanisms for somatic maintenance and repair that help secure the longevity of an individual [2]. If the majority of animals are likely to die before middle age it is unlikely that natural selection will affect later stages of life. According to the disposable soma theory, animals with high extrinsic mortality and short survival periods typically focus their resources in reproduction instead of maintenance. Conversely, animals living in conditions where the level of extrinsic mortality is low are likely to direct more resources into their somatic maintenance and construction over reproduction.

Mechanisms for somatic maintenance and repair that enable longevity in the individual have been bolstered by humanities ability to control extrinsic variables [2]. According to the disposable soma hypothesis, the ability to control these variables may have helped direct more resources into the body’s somatic maintenance and less into reproduction. Paired with our ability to mollify the immediate costs of reproduction and growth, the disposable soma hypothesis may help explain our species longevityCite error: Closing </ref> missing for <ref> tag. Never the less, women with the least amount of children were found to live the longest, suggesting a trade off between longevity and the ability to fix general physiological wear and tear as it occurs[3].

Post reproductive lifespan in nonhuman primates

Due to their physical, cognitive and genetic similarities to ''Homo sapiens'', nonhuman primates provide an important comparative model in the study of human evolution. As our closest living relatives, the great apes are particularly important for the study of menopause. Their behaviors may shadow early forms of social development and organization in the ancestry of Homo sapiens.

Human life history traits differ significantly from other primates. This difference is particularly obvious when considering the ubiquitous nature of reproductive termination in humans and its virtual non-existence in nonhuman primates. In comparison with the other great apes, reproductive termination is not early. Instead it is our extended post reproductive lifespan that is dramatically different.

Non-human primates can provide a biological and behavioral comparison for human life history traits such as menopause. Although informative, primate studies into post reproductive senescence face two key problems. First, primate studies frequently have small sample size. Second, it is difficult to accurately determine when old females have fully terminated reproduction as opposed to experiencing an extended interbirth interval.

Average Proportion of Postreproductive Female Lifespan Across Primate Species[4] [5]

Species Percentage of Female Lifespan that is Postreproductive
Mountain Gorillas 1-3%
Japanese Macaques 9%
Humans 20-40%

Japanese macaques

Japanese Macaque Mom and Infant.jpg

The post reproductive patterns of Japanese macaques (Macaca fuscata) have been evaluated with the survivorship of their offspring, final infants and their great-offspring. Few female Japanese macaques reach reproductive termination. Those females who terminated reproduction before death have been shown to have similar offspring survivorship as those females who reproduced until death. However, final infants of females who reproduced until death were 13% less likely to survive then the final infants of females with a post reproductive lifespan. Females with a post reproductive lifespan are significantly longer lived and have a greater fecundity then those females that reproduced until death [4]. The rarity of female Japanese macaques experiencing reproductive termination suggests that this life history trait is likely an epiphenomenon for longevity.

Comparative Life History Traits of Great Apes[6]

Species Average Adult Lifespan Age at Maturity Age at Weaning Period of Independent Growth Ratio of Weaning Weight to Adult Weight Daughters per Year
Orangutans 17.9 14.3 6 8.3 .28 .063
Gorilla 13.9 9.3 2 6.3 .21 .126
Chimpanzees 17.9 13 4.8 8.2 .27 .087
Humans 32.9 17.3 2.8 14.5 .21 .142

Great apes

Neither gorillas (Gorilla gorilla) or chimpanzees (Pan troglodytes) regularly experience a post reproductive period of life. Although the birthrates of African Apes decrease with age, the survivorship of their offspring improves with maternal experience. In gorillas, miscarriage rates are significantly higher for older females then younger females [5]. This is similar to pattern of miscarriage in both hanuman langurs and humans females [7]. In gorillas, there is not a significant difference between the mortality of infants whose mother died of natural causes and those who continued reproducing. In one population, no mother died of natural causes while she had offspring below weaning age [5]. The lack of fitness benefits from continued parturition in old age may indicate that reproductive cessation in humans evolved through antagonistic pleiotrophy [8].

Gorilla Baby.jpg

Menopause: epiphenomenon or adaptation?

There are two overarching theories regarding the emergence of a postreproductive life span. These include menopause either as an epiphenomenon or as an adaptation.

Menopause as an epiphenomenon

An epiphenomenon is a secondary phenomenon that accompanies a physical phenomenon but has no causal influence in itself. Under this model, menopause is an epiphenomenon of a long life span and a reduction in oocyte viability instead of being directly adaptive in it’s own right [4].

Menopause as an adaptation

Adaptive theories contend that human females were able to gain direct or indirect benefits from having a post reproductive lifespan. There are three main adaptive hypothesis regarding the evolution of menopause. These include the maternal investment model, the mother hypothesis, and both forms of the grandmother hypothesis. At the core of each hypothesis is the idea that by maximizing maternal investment, human mothers can gain increased reproductive success post reproductively.

Maternal investment model

The maternal investment model holds that mothers can gain more from investing in their current offspring and their great offspring then by continuing to invest in new offspring. This is a combination of the mother and grandmother and mother hypothesis models.

Mother hypothesis

The mother model contends that older females were able to gain an advantage by curtailing the length of their reproductive lives and investing that energy into their current offspring. In the absence of the mother or alloparent a young child’s chance of survival is very low. Thus, if a female can curtail her reproductive output at the end of life and invest heavily in her surviving offspring her reproductive gain would be significantly higher.

The original grandmother hypothesis

The grandmother hypothesis has been proposed as a potential evolutionary reason for menopause. This hypothesis suggests that a post-reproductive life span was selected for in humans as a way of reducing the costs of reproducing late in life while simultaneously improving their daughter’s reproductive fitness. Proponents of the grandmother hypothesis suggest that the emergence of communal breeding enabled middle aged women to gain inclusive fitness benefits and mitigate their own reproductive costs while improving their daughter’s reproductive success. As a result, the individual reproductive success of females begins to wane at the approximate time that their own offspring could be expected to give birth. By relieving their daughter’s energetic burden in child care, maternal grandmothers enable their offspring to produce more children and improve the survivorship of those they already have [9] [10] [11] [12]

Grandmother and Infant.jpg

Support of the grandmother hypothesis: role of maternal grandmothers in modern and pre-modern societies

The importance of maternal grandmothers to their daughter’s fertility and offspring survival has been documented cross culturally. Pre-modern populations of Finnish and Canadian women with extended post-reproductive lifespans had more grandchildren then those who had shorter post-reproductive lifespans [13]. In Tokugaw, Japan the maternal grandmother was the only grandparent whose presence reduced the instances of child mortality [14]. Infants with surviving maternal grandmothers in early populations in Krummhörn, Germany were 1.8 times less likely to succumb to infant mortality between the 6th and 12th months of age. Comparatively, living paternal grandparents within the same population nearly doubled the relative risk of infant mortality within the first month of life [15]

In Gambia, the presence of maternal kin has been shown to improve child survivorships but not the fertility of females. Alternatively, patrilineal grandparents increased the mother’s birth rate but often had negative effects on fertility [16]. Maternal grandmothers were the only kin besides mothers who significantly improved the nutritional status of children. Children raised in the presence of a post-reproductive maternal grandmother were taller than those whose grandmothers were still reproductively active. Comparatively, paternal kin had negligible effects on the nutritional status of children in this population [17]. In this same patrilineal society, children who lived with their maternal grandmothers had a higher survival rate then those living with paternal relatives [9].

The relative fitness benefits of care from maternal kin can be more significant than maternal care itself at the population level. The first two years of life are a tremendously dangerous for children [18]. Maternal grandmothers are able to provide a competitive edge to their grandchildren, especially after the age of two [16] [17]. A child weaned at this age faces few health repercussions but helps reduce the energetic costs to the mother by enabling her to delegate childcare responsibilities to other adults. The importance of additional care givers is exemplified in Gambia where the survivorship of children over the age of two was not significantly affected by their mother’s mortality [16]. Taken together, these results indicate that maternal grandmothers are able to improve the reproductive success of their daughters and the survivorship of their grandchildren.

Responses to the grandmother hypothesis

These four challenges to the grandmother hypothesis were originally articulated by Pecci (2001) [19]

1.) Cross-population qualitative and quantitative evidence for helpful grandmothers is not compelling.


Much of the evidence citing the impact of maternal grandmothers on the well being of their grandchildren is focused upon nutritional support and services. However, marked nutritional support seems to be rare. Instead grandmothers more frequently support their grandchildren in nondepreciable care. This includes assisting in food preparation, and filling administrative needs surrounding sustenance. Although these behaviors could have fitness-enhancing qualities for grandmothers and daughters, these benefits are applied simultaneously to all grandchildren with little individual cost per child [19].


2.) Mathematical models do not support the fitness advantage of reproductive cessation in favor of increased investment in adult daughters and granddaughters.


The grandmother hypothesis suggests that the inclusive fitness benefits gained by supporting your female offspring outweigh the benefits of continuing reproduction late into life. Costs to late life reproduction in human females includes an escalated risk of miscarriage, premature birth, birth defects, still births, and death [20] [21] [22]. Although the costs associated with late reproduction seem daunting, they alone are unable to eliminate the fitness benefits of reproducing late [23].


Demographic models were constructed to determine the impact grandmothers on the fertility of their daughters and the survivorship of their grandchildren. These models utilized modern Ache demographic data and determined the point at which women could maximize fitness by diverting energy away from personal reproduction and towards investment in kin. Results of this study were unable to support the grandmother hypothesis [24]


3.) The grandmother hypothesis requires female philopatry, which does not appear likely in the hominine line.


According to the grandmother hypothesis, active participation of maternal grandmothers in their grandchildren’s lives has been an adaptive force behind the evolution of a postreproductive lifespan and menopause. However, this would suggest that human females must maintain lifelong contact with their mothers for a considerable portion of human evolution. From this it could be postulated that human ancestors commonly utilized a form of female philopatry in which female’s maintained contact with their natal group while the males dispersed. However, this evolutionary scenario is unlikely considering the evidence supporting male philopatry and female dispersal as the dominant organizational pattern present throughout evolution.


The nature of the fossil record prevents paleoanthropologists from being able to directly infer the behavioral, ecological and adaptive pressures facing our ancestors [25]. Thus an indirect approach is taken to piecing together our history. In addition to the comparative faunal, floral, and archaeological data used to reassemble the paleoenvironments of extinct hominids, the anatomy and behavior of living primates is considered as an analog to hominid adaptation [26].


Unlike many monkey groups, chimpanzees live in male bonded societies [27]. At maturity, females leave their natal groups and disperse into a non-related group, thus permanently separating themselves from their kin. Although there is evidence of slight variation in this pattern of dispersal, male dispersal is uncommon across the species.


Genetic evidence lends support female dispersal as the ancestral condition of modern humans. Using independent noncoding nuclear loci, it is possible to make predictions regarding the dispersal behavior of the ancestral populations that gave rise to extant species of living African apes and modern humans [28]. These results indicate that the last common ancestor of gorillas, chimpanzees and humans were likely to exhibit female philopatric dispersal with female gene flow restricted to short distances. However, the last common ancestor of chimpanzees and humans indicate increased female vagility and movement indicative of female dispersal and male philopatryCite error: Closing </ref> missing for <ref> tag


The importance of men to the nutritional needs of foraging societies may be one of the keys to human organization. This organization may be due to the reliance on unrelated men for acquiring the majority of protein meat in the human diet. Thus it is unlikely that mothers were able to maintain lifelong contact with their daughters or maternal grandchildren.


4.) The role of males and siblings is ignored.


The grandmother hypothesis emphasizes the role of post reproductive females in increasing the fitness of their grandchildren. This does not account for the impact of other individuals on the survivorship of children. The importance of men and children to the care of related offspring must be taken into account. Males play a significant role in the acquisition of protein in foraging societies. Into their sixties, Ache, Hadza, and Hiwi men typically provide a surplus of calories [29]. Older females are less likely to produce a surplus of calories and are therefore nutritionally dependent on their communities.

San Hunters.jpg


Independent foraging on behalf of children could help bolster their fitness and provide critical calories with little input from adult care givers. In addition to freeing human females from lactation, children have been shown to take an active role in addressing their nutritional needs. For instance, research indicates that children of hunter-gathers can play a substantial role in meeting their own nutritional needs and offsetting energetic costs that their families would otherwise be required to meet [30]. In addition, older children may be able to subsidize the nutritional and care giving needs of younger siblings. Older children assist with the allocation and procurement of resources and may provide the opportunity for cooperative breeding in humans [31]. In other words, children’s abilities to partially support themselves nutritionally may have immediate fitness trade-offs while indirectly improving the reproductive output of their mothers.

The new grandmother hypothesis

The new grandmother hypothesis changes the focus away from inclusive fitness and towards their impact on the evolution of hominid traits critical to human reproduction. Human reproductive success has been achieved through a suite of traits critical to the reduction of interbirth intervals. This suite includes reduced cost of lactation, a prolonged childhood and juvenile period, the ability of children to address a portion of their nutritional needs and finally increased communal breeding.

Like other primates, humans have an elongated gestation and an extended period of growth and development prior to maturity. However, significant reduction in interbirth intervals combined with the ability to overlap dependent offspring results in a life history pattern unlike that of any other mammal [32]. Combined, these traits have enabled protracted physical and cognitive growth while simultaneously reducing the energetic costs for both mother and offspring [31]. According to the new grandmother hypothesis, the diversion from a primate life history to a human life history was triggered and maintained by the emergence of grandmothers in the hominid line.

Responses to the new grandmother hypothesis

The new grandmother hypothesis faces the same constraints as the grandmother hypothesis (section 7). In addition, there are four additional constraints facing the new grandmother hypothesis. At the core of these constraints is that fact that life history traits are inextricably impacted by physiological and phylogenetic factors, not just the presence of grandmothers.

1.) Long lifespans, late age at maturity, high fertility and early weaning in humans are not necessarily caused by the emergence of grandmothers.

Longevity:

Longevity is likely impacted by multiple variables rather then the presence of a particular family member. Feedback between body size at weaning, annual fertility, paleoecology, human anatomy and physiology and the trade off of extrinsic and intrinsic mortality are all play a role in the shaping the evolution of a species longevity [19]. At one point in human evolution, extrinsic sources of mortality were more common then intrinsic sources. This may not be readily represented in traditional societies who are able to partially mitigate some of the extrinsic sources of mortality with culture. As a result, it is likely that adult mortality rates would be higher then represented by extant human population. In addition, as extrinsic sources of mortality are curtailed, it would be expected that senescent mortality would occur more frequently. Although grandmothers may have helped reduce some extrinsic mortality, it is unlikely that they are the only ones who were capable of making this kind of impact.


Late age at Maturity and Extended Period of Independent Growth:

Humans enjoy an unparalleled extended period of post-natal growth and development which does not depend on continuing maternal nutritional investment. Childhood provides a developmental stage in which offspring can continue to physically and socially grow, while liberating females from the energetic costs of lactation [31]. The new grandmother hypothesis links the extended human lifespan to our increased period of independent growth, however there is no causal evidence of this. It is possible that it occurred in the reverse. There is some evidence that lifespan is the direct consequence of selection for an extended childhood. This extended childhood in turn has been linked to improvements in offspring survival though increased maternal investment [33].


High Fertility


The new grandmother hypothesis links high rates of human fecundity and the late age of maturity to grandmothers. It is assumed that the contribution of grandmothers increases their daughter’s annual fecundity and that birthrates for humans are distinctly different from those of the other great apes.


Great ape grandmothers are unlikely to impact the fitness of their grandchildren. Thus we would expect that life history traits tied to grandmothers would be found only in humans. According to the new grandmother hypothesis, human grandmothers are expected to experience a higher annual fecundity than other hominoid species. It would be expected that there would be distinct differences between the annual birthrate of great apes and humans. Although the annual birthrate of human hunter-gather populations is higher then either orangutans or chimpanzees, it remains similar to the birthrate of gorillas [19]. There is no way of knowing how long chimpanzee and orangutan birthrates have been different from humans and if this life history modification originated in orangutans and chimpanzees instead of humans. Then again, it is unclear if high fertility is an ancestral trait or more modern one based off of changes in nutrition and reduction in extrinsic sources of mortality.


High human annual fecundity may be linked to human life history traits including increased cranial capacity, reduced interbirth intervals, and alloparenting. Humans have significantly bigger brains then other species of primates. In addition they have a greater level of cognition and problem solving skills then do other primates. This enhanced cognition improved foraging skills for all ages and is probably tied to the emergence of important weaning foods. The use of weaning foods as a species would have reduced the energy costs to mothers by enabling her to allocate dependents to other members of her family and community.


A species ability to increase their reproductive output relies on their ability to decrease their interbirth intervals. The reduction of interbirth intervals requires that offspring are no longer dependent on their mother for their primary nutrition and well being (e.g., infants are weaned). In humans, the reduction of interbirth interval has been linked to a mother’s ability to redistribute the cost of non-nutritionally dependent offspring through communal breeding ad allomothering. As discussed in section 7.2, this assistance can come from grandmothers, related females, males and children. Redistribution of the carrying and foraging costs enables females to allocate their energy towards more energetically demanding activities such as lactation and reduces the competing demands of older and younger children by incorporating the help of one into the care of the other.


Early Weaning


Through a mosaic of developmental and social traits, human mothers have been able to mitigate the costs of their reproduction. These traits include the development of a childhood life stage and increased non-maternal care from others in the social group. Of the apes, human’s have the most protracted period of dependency and the shortest period of lactation [34].


Compared to the other great apes, human infants are weaned comparatively early relative to age at maturity [19]. In addition, human infants are more reliant on care givers at weaning then are the other great apes. However, size at weaning relative to their adult size is similar for orangutans, humans, gorillas and chimpanzees. Lactation is the most costly portion of reproduction and requires 26% more energy than non-reproductive states [35]. Whereas ape mothers do not provide nourishment to more than one offspring at a time, humans are able to wean dependent infants earlier while supporting a protracted postnatal growth period.


Rapid weaning and an extended juvenile period rely heavily on a mother’s ability to redistribute the cost of their non-nutritionally dependent offspring to other members of her social system. By breeding cooperatively, human have extended their care network to include both affinial and consanguineous kin. Although grandmothers were likely to play a role in promoting the fitness of their kin, males and children cannot be discounted as important players in cooperative breeding leading to early weaning and decreased interbirth intervals.

Big Sister Helping Brother.jpg


2.) Longer childhoods do not necessarily permit the development of larger brains


According to the new grandmother hypothesis, the emergence of an extended juvenile period in humans has been associated with the role of grandmothers in our species evolution.


The social skill repertoire required as a member of a primate community is immense and is reflected in the juvenile period of primate and human lives. There is a positive correlation between the proportion of a primate’s lifespan spent as a juvenile and the relative size of the non-visual cortex; the area of the brain concerned with cognitive memory and social problem solving [36]. Extended growth continues to be important prior to sexual maturity in adolescence. This extra time enables young males and females to practice complex social skills prior to reproducing and may improve infant survivorship and the fitness of both parents [37].


According to the new grandmother hypothesis, grandmothers made possible an extended childhood period and this enabled the development of larger brains. Regardless of the importance of the childhood period, it is still unclear if childhood or larger brains evolved first. It is possible that the evolution of a larger brain and the need for more time to acquire knowledge, supported the evolution of an extended childhood.


3.) Post reproductive grandmothers were unlikely to existed in paleopopulations


In the new grandmother hypothesis, menopause arose from an extended life expectancy brought on by the fitness inducing qualities of maternal grandmothers. In this hypothesis, the maximum human lifespan surpassed the current age of menopause due to the influence of a post reproductive lifespan in human females. However, a causal relationship between grandmothering and increased lifespans is unable to be supported by the life expectancies and age structures in paleopopulations.


The manifestation of modern longevity in humans is critical in determining the timing and emergence of menopause. Due to the constraints of the fossil record it is difficult to precisely determine the timing of menopause in humans. However, research into ''Homo erectus'' suggests that menopause could be as early as 1.8 million years old [19]. However, data from paleopopulations suggests that it is unlikely that women regularly survived to a postmenopausal age until approximately 50,000 years ago [38]. Additional evidence using tooth wear serrations suggests that the most dramatic increase in longevity may have occurred closer to the Upper Paleolithic (approximately 30,000 year ago)[39]. This demographic transformation through increased human longevity coincides with an explosion of cultural complexity including symbolism, trade, technologies for gathering and storing food items, and markers of ethnic differences [40]. This work is unable to directly address the pattern of post reproductive success in humans, it does indicate that human longevity may be extremely recent in evolutionary terms.

References

  1. World Health Organization (WHO). 1981. Research on the menopause. WHO technical Report Series, NO 670. Geneva: World Health Organization.
  2. 2.0 2.1 2.2 2.3 Kirkwood TBL. 2002. Evolution of aging. Mechanisms of ageing and development. 123:737-745.
  3. 3.0 3.1 Abbott A. 2004. Growing old gracefully. Nature. 428:116-118.
  4. 4.0 4.1 4.2 Pavelka MSM, Fedigan LM. 1999. Reproductive termination in female Japanese monkeys: a comparative life history perspective. American Journal of Physical Anthropology. 109:455–464.
  5. 5.0 5.1 5.2 Robbins AM, Robbins MM, Gerald-Steklis N, Steklis HD. 2006. Age-related patterns of reproductive success among female mountain gorillas. American Journal of Physical Anthropology. 131:511-521.
  6. Hawkes K, O’Connell JF, Jones NG, Alvarez H, Charnov EL. 1998. Grandmothering, menopause and the evolution of human life histories. Procedures Natural Academy Science. 95:1336-1339.
  7. Harley D. 1990. Aging and reproductive-performance in langur monkeys (Semnopithecus entellus). American Journal of Physical Anthropology. 83:253-261.
  8. Packer C, Tatar M, Collins A. 1998. Reproductive cessation in female mammals. Nature. 392:807-811.
  9. 9.0 9.1 Sear R, Mace R, McGregor IA. 2000. Maternal grandmothers improve nutritional status and survival of children in rural Gambia. Proceedings of the Royal Society. 267:1641-1647.
  10. O’Connell JF, Hawkes K and Jones NG. 1999. Journal of Human Evolution. 36:461-485.
  11. Hawkes K, O’Connell JF, Jones NG, Alvarez H, Charnov EL. 1998. Grandmothering, menopause and the evolution of human life histories. Procedures Natural Academy Science. 95:1336-1339.
  12. Hamilton WD. 1966. The molding of senescence by natural selection. Journal of Theoretical Biological. 12: 12-45.
  13. Lahdenperä M, Lummaa V, Russell AF. 2004. Menopause: why does fertility end before life? Climacteric. 7:327-332.
  14. Jamison CS, Cornell LL, Jamison PL, Nakazato H. 2002. Are all grandmothers equal? A review and a preliminary test of the “Grandmother Hypothesis” in Tokugawa Japan. American Journal of Physical Anthropology. 119:67-76.
  15. Voland E, Beise J. 2002. Opposite effects on maternal and paternal grandmothers on infant survival in historical Krummhörn. Behav Ecol Sociobiology. 52:435-443.
  16. 16.0 16.1 16.2 Mace R, Sear R. 2005. Are humans communal breeders? In: Grandmotherhood: The Evolutionary Significance of the Second Half of Female Life. Voland E, Chasiotis A, Schiefenhövel, eds. Rutgers University Press, New Brunswick.
  17. 17.0 17.1 Sear R, Steele F, McGregor IA and Mace R. 2002. The effects of kin on child mortality in rural Gambia. Demography. 39:43-63.
  18. Cassidy CM. 1980. Benign neglect and toddler malnutrition. In: Social and Biological Predictions of Nutritional Status, Physical Growth and Neurological Development. Edited by LS Greene and FE Johnston. New York: Academic Press.
  19. 19.0 19.1 19.2 19.3 19.4 19.5 Peccei JS. 2001. Menopause: adaptation or epiphenomenon? Evolutionary Anthropology. 10:43-57.
  20. Jolly M, Sebire N, Harris J, Robinson S, Regan L. 2000. The risks associated with pregnancy in women aged 35 years or older. Human Reproduction. 15:2433-2437.
  21. Wood JW. 1994. Dynamics of Human Reproduction: Biology, Biometry, Demography. Aldine De Gruyter, New York.
  22. Gaulden ME. 1992. Maternal age effect: the enigma of Down Syndrome and other trisomic conditions. Mutat Res. 296:69-88.
  23. Rogers AR. 1993. Why menopause? Evolutionary Ecology. 7:406-420.
  24. Hill K, Hurtado AM. 1991. The evolution of premature reproductive senescence and menopause in human females: an evaluation of the “grandmother hypothesis.” Human Nature. 2:313-350.
  25. Hawkes K and O’Connell JF. 2005. How old is human longevity? Journal of Human Evolution. 49:650-653.
  26. Potts R. 1987. Reconstruction of early hominid socioecology: a critique of primate models. In WG Kinzey (Ed). The evolution of human behavior: primate models (pp 28-47) Albany: Suny Press.
  27. Wrangham RW. 1987. The significance of African apes for reconstructing human social evolution. In: The Evolution of Human Behavior: Primate Models, ed. Kinzey W. SUNY Press, Albany. pp 51-71.
  28. Jensen-Seaman MI, Deinard AS, Kidd KK. 2001. Modern African ape populations as genetic and demographic models of the last common ancestor of humans, chimpanzees, and gorillas. The American Genetic Association. 92:475-480.
  29. Kaplan H, Hill K, Lancaster J, Hurtado AM. 2000. A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol. 9:156-185.
  30. Bird DW and Bird RB. 2000. The ethnoarchaeology of juvenile foragers: shellfishing strategies among Meriam children. Journal of Anthropological Archaeology. 19: 461-476.
  31. 31.0 31.1 31.2 Kramer KL. 2005. Children’s help and the pace of reproduction: cooperative breeding in humans. Evolutionary Anthropology. 14:224-237.
  32. Knott C. 2001. Female reproductive ecology of the apes: Implications for human evolution. In Ellison Reproductive Ecology and Human Evolution. Aldine de Gruyter, NY. Pp 429-463.
  33. White FJ, Churchill SE. 1997. Hawkes K, O’Connell JF, Blurton Jones NG. 1997. Hazda women’s time allocation, offspring provisioning, and the evolution of long post-menopausal life spans.
  34. Knott C. 2001. Female reproductive ecology of the apes: Implications for human evolution. In Ellison Reproductive Ecology and Human Evolution. Aldine de Gruyter, NY. Pp 429-463.
  35. Dufour DL and Sauther ML. 2002. Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation. Am. J. Hum. Biol. 14:584-602.
  36. Joffe TH. 1997. Social pressures have selected for an extended juvenile period in primates. J. Hum. Ev. 32:593-605.
  37. Bogin B. 1999. Evolutionary Perspectives of human growth and development. Ann. Rev. Anthrop. 28: 109-153.
  38. Gage TB. 1988. Mathematical hazard models of mortality: an alternative to model life tables. American Journal of Physical Anthropology. 76: 429-441.
  39. Caspari R and Lee S. 2004. Older age becomes common late in human evolution. PNAS. 101:10895-10900.
  40. Rosenberg K. 2004. Living longer: Information revolution, population expansion, and modern human origins. PNAS. 101:10847-10848.