AN ENERGETICS-BASED APPROACH TO UNDERSTANDING THE MENSTRUAL CYCLE A N D MENOPAUSE Roberta L. Hall Oregon State University
To explain the menstrual cycle and menopause, human biologists during the past several decades have developed new models of the evolutionary origins and maintenance of female reproductive patterns that address both ultimate and proximate causation. Hypotheses proposed for these processes generally offer explanations for menstruation or for menopause, but not for both; ultimately, these explanations must be integrated. Reviewing current explanations, this paper offers an energetics-based evolutionary rationale compatible with past adaptations of Homo sapiens and with ecological patterns in small-scale, preindustrial social systems in which food resources vary and sometimes are scarce. KEYWORDS" Energetics; Menopause; Menstrual cycle
Systems of reproduction, which are integral to any species, must be examined in light of energy costs. Humans are large mammals that grow slowly, have long lives, and produce relatively few offspring. Potentially high metabolic costs are associated with reproduction in human females, whose reproductive systems are constrained by physical components inherited from mammalian a n d / o r primate ancestors. The physiology of living primate relatives and models of ecosystems of past members of the hominid lineage, along with studies of diverse m o d e m human populations and Received February 17, 2003; accepted May 28, 2003; revised version received July 3, 2003.
Address all correspondence to Roberta L. Hall, Department of Anthropology, Oregon State University, Corvallis OR 97331. Emaih [email protected] Copyright 2004 by Walter de Gruyter, Inc., New York
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archaeologically known populations, can provide an understanding of how the human female's reproductive system evolved. As Ellison (2001: 167) noted, "In general, there are two major constraints on a female mammal's ultimate reproductive success: energy and time." Research of the past few decades on hormonal and nutritional influences on the menstrual cycle has provided information about how the system is regulated and thus what selection can work on. These developments have made it possible now to ask why, in human females, there is a menstrual cycle involving loss of blood. And then, after 30+ years, why does cycling cease? Hypotheses proposed for these intimately related questions generally offer explanations for menstruation or for menopause, but not both. Ultimate evolutionary explanations for the cycling and for its cessation should complement each other, not only providing an understanding of the reproductive system of human females but also linking human reproductive ecology with the systems of our forebears; proximate mechanisms that offer answers to nitty-gritty "how" questions also must be addressed. This paper provides a review of recent research and proposes an energetics model, integrating the research of other scholars, to explain the origin and maintenance of the menstrual cycle and its cessation in adult hfe. The model is compatible with understandings of biocultural patterns in small-scale, preindustrial social systems that have economies in which food resources fluctuate and food is sometimes scarce. I do not present a full discussion of reproductive ecology, which is provided in Ellison (2001), but instead I provide a selective review of recent developments that underlie energetics theory linking the menstrual cycle and menopause in modern humans. The concept of energetics applies at two levels, the study of the flow of energy through an entire ecological community and the analysis of energy consumption at the individual level, including tradeoffs between potential investments. Both apply here, but my primary focus is on the individual. Examination of the dynamics underlying these processes permits-speculations concerning possible future trends in female reproductive ecology.
BACKGROUND: PHYSIOLOGICAL CONSTRAINTS
Energetics, ecology, and evolution provide a basis for understanding menstruation and menopause. At the most specific level, energetics refers to nutrient transformations of a physical, chemical, or biological system, and thus provides the metabolic cost of key adaptations (Leonard and Ulijaszek 2002). Ecology refers to the totality of relationships between organisms and their environment; by analyzing the flow of energy, ecological analysis can show how life-history patterns help humans fit within the
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ecosystem. At the most abstract level, evolution refers to changes in living beings over time, generally understood to occur as a result of adaptation within an ecological system. Life-history features shared with other primates include a relatively long childhood, extended longevity for at least some members of the population, and a kin-based social organization in which there is overlap between several generations. As in other primate societies, the resource demands of any one individual and of each gender and age group may impact the survival of a traditional human population. Human cultural patterns have been built upon reproductive systems from the primate heritage and have developed rituals (e.g., menarche comingof-age celebrations) that have elaborated as well as accommodated to them. The primate heritage provides the basic reproductive plan that extends to modern human females; for example, all catarrhine primates, including humans, possess elaborated placentas that provide high-quality nourishment of the fetus (Strassmann 1996a, 1996b; Bentley 1999). These placentas require a specialized and elaborated endometrium which represents a substantial metabolic investment that is made during each menstrual cycle and destroyed if an egg is not implanted. Although within each developing female fetus there are several million primitive germ cells, some of which go on to experience the first meiotic division in the second trimester, the number of potential functional eggs is reduced enormously before birth and this number continues to decrease until reproductive function ceases (Ellison 2001:233). This superabundance of germ cells makes it hard to argue that selection has placed a premium on the space that these cells take up, but at some level too much is too much. Perhaps more to the point, the deterioration of this enormous number of cells sets a limit on a woman's reproductive life. The as-yet-unanswered question is whether the pace of loss of egg cells--of follicular atresia--is based on the number of germ cells in the early fetal stage or is independent of it. Would having more germ cells result in additional months or years of reproductive function or would there simply be higher rates of atresia, so that the woman would reach menopause at the same age, regardless of the number of original cells? Some evidence for the latter perspective is that during a woman's reproductive years, the destruction of egg ceils appears to continue whether cycling occurs or is suspended due to pregnancy, nursing, or nutritional deficiencies. Earlier age of menopause appears statistically related to tobacco smoking as well as to other biobehavioral traits (Leidy 1994), suggesting that some negative influences on a woman's physiological status can speed up follicular atresia; what is not known is what, if anything, can slow it down. The tendency of women in a number of nonindustrial, noncontracepting societies to have their last child about age 40 (Lancaster and King 1985) is suggestive of a process of reproductive
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depletion, an effect on the woman's fecundity possibly through the effect of many pregnancies and the stresses to health that accrue in labor-intensive societies. Later I compare reproductive data from two noncontracepting populations that have different environmental stresses. Age-related impacts on egg quality as well as quantity are known. Because eggs deteriorate with age, increased fetal losses in early stages of pregnancy and a greater chance of genetic defects in infants are associated with greater mother's age (Ellison 2001; Holman, Wood, and Campbell 2000). These outcomes, among others associated with normal human aging, favor female reproduction in young adulthood. It is likely that during their first 20 years of reproductive life most of the human females living during the past 100,000 years experienced relatively few menstrual cycles because of pregnancy, lactation, and seasonally reduced food supplies (Strassmann 1996a; Ellison 2001). In part because there are relatively few cycles, benefits of the improved nourishment outweigh the metabolic costs of producing an enriched endometrium. Because of oocyte deterioration and resulting increases in early fetal losses, however, older females would be expected to have more rather than fewer menstruations. Continuation of menstrual cycling past the most fertile 20 years results in some live-born, healthy infants but fewer healthy offspring per conception than in young adult females. Menstrual cycling thus consumes calories for activities that otherwise could support survival of offspring and other family members. A series of 12 to 13 cycles per year adds about 4% to the annual calorie budget (Strassmann 1996b). Cessation of cycling provides a significant savings in energy and resources for m o d e m Third World women, who provide extant examples of nutritional stresses that likely affected prehistoric people (for examples of caloric stresses on women in contemporary nonindustrial societies, see Baer 1999; Jeliffe and Maddocks 1964; and Panter-Brick 1997). Cessation of cycling also reduces the chance of mortality in the pregnancy of an elder female who may be contributing important cultural knowledge as well as labor on behalf of offspring families--knowledge and effort that could promote their survival and welfare.
MENSTRUATION AND MENOPAUSE The Menstrual Cycle Menstrual bleeding has been called "the curse" in Western cultures and menstrual taboos abound in traditional societies as well (Delaney, Lupton, and Toth 1988). How women deal with menstruation and taboos associated with it has been the subject of much popular and scholarly literature.
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This is true even though most women experienced relatively few menstrual cycles until the past hundred years, when lowered infant and child mortality rates encouraged women in industrial countries to use the newly available contraceptives, and it is possible that the rarity of menstruation in traditional societies is one of the factors that produced society's interest in it. Some adaptive elements of menstruation have been hypothesized. Profet (1993) postulated that the blood flow itself was selected because it could cleanse the uterus of sperm-borne germs; an earlier adaptive hypothesis is that menstrual blood may have enhanced hominid females' reproductive options by serving as a signal of fertility. By contrast, an energetics-based theory offered by Beverly Strassmann (1996a, 1996b) sees the vaginal bleeding component of the menstrual cycle as a side effect of selection for an improved blood supply to nourish the developing fetus. Strassmann has drawn her energetics explanation for endometrial cycling, including menstrual bleeding, from research with the Dogon people of Mali and research reports concerning nonhuman primates. The reproductive system of Old World monkeys and apes involves an elaborated microvasculature that supplies the endometrium. Menstruation occurs in other primates and merely is more obvious, more copious, and more common in hominoid females, especially in humans. For Strassmann, the key question concerns why the endometrium is shed rather than maintained, and the solution is found in lesser energy costs involved in doing so. Physical constraints help to explain why the menstrual loss occurs; the specialized, thick-walled endometrium is thought to be too bulky and too differentiated a tissue to be easily resorbed (Ellison 2001:48). Strassmann sees regression of the endometrium as parallel to other tissue regressions, such as the reduction of breast tissue in non-lactating women, and atrophy of the gut and gonads in hibernating mammals. The strongest evidence for the energetics hypothesis of cycling exists in studies Strassmann cites concerning basal metabohc rate differences between women in different phases of the reproductive cycle. Women have higher metabolic rates during their menstrual cycle's luteal phase, when endometrial development occurs, than in their post-menses, pre-ovulatory phase. Postmenopausal women and those in their nonluteal phase have comparable, lower rates. Strassmann (1996a:205) concludes: "The coupling of female reproductive cycling to metabolic cycling is unlikely to be fortuitous. The menstrual/ovarian cycle revs up and revs down, economizing on the energy costs of reproduction." Gillian Bentley (1999) presents data showing how the reproductive physiology of humans and their primate cousins responds with sensitivity to environmental variation, making apparent trade-offs that contribute to reproductive success. She interprets as adaptive the reduced fecundity of humans and other primates that results from seasonal shortages of food
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or shortages by environmental downturns. By contrast, physicians tend to see such effects as reproductive dysfunction and are less likely to use an evolutionary model. Bentley's perspective on reproductive processes in primates, including humans, like Strassmann's, is based in energetics.
Menopause The evolutionary problem posed by menopause is more complex than that of menstruation because females in all mammal species require ovulation and some kind of cyclic reproductive potential in order to have any reproductive success at all--but all mammalian females can experience reproductive success without living long enough to experience menopause. Thus, the fitness question arises as it does in any adaptation that occurs following an organism's reproductive years. In examining menopause, it is essential to differentiate theories about its origins, which likely occurred when hominid life spans were shorter, from theories about selective pressures that maintain it. Related to this issue are disagreements about whether nonhuman species experience it and whether sufficient human females in prehistory experienced a postmenopausal stage to permit selection to favor it. Although much is known about menopausal processes, some of the most basic descriptive data, particularly concerning variability among women, are still being gathered (D. J. Holman, personal communication, 2002; O'Connor, Holman, and Wood 2001), and key concepts are still being defined (Pavelka and Fedigan 1991). For example, the convention is that premature infertility is that which occurs before age 40 (Leidy 1999:408); however, the timing of human menopause varies considerably, so setting any date as "premature" itself may be premature. Some evolutionary explanations of cessation of menses have viewed menopause as a discrete event rather than a process of gradual reduction in the probability of becoming pregnant and producing a live offspring (Austad 1994; Peccei 1995, 2001). Regarding the process as gradual, rather than as an all-or-nothing event, invites consideration of various physical features that produce age-related decline in fecundity (Holman, Wood, and Campbell 2000). Wood, Holrnan, and O'Connor (2001) and Ellison (2001) identify follicular depletion as the end point of a process of follicular depletion, which thus is the proximate cause of menopause. Lancaster and King (1985) raise many key issues concerning menopause, its origins and maintenance, including whether other species experience menopause and the extent to which women in the past experienced it. They recognize that the experience of m o d e m women is quite different than that of earlier women and women in nonindustrial societies because of the presence in m o d e m cultures of extended life expectancies, fewer pregnancies with more menstrual cycles, and less time involved in lacta-
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tion. Their review of prior demographic studies on diverse extant ethnographic populations, including Nancy Howell's (1979) detailed and seminal work with the !Kung, leads them to the opinion that a human life-history pattern that includes menopause could have existed long enough for selection maintaining it to occur. Whereas many researchers consider menopause the termination of menstrual cycling (Pavelka and Fedigan 1991), usually defined operationally by the passing of a full year with no menstruation, for Lancaster and King (1985:15) "the relevant statistic for establishing the end of the reproductive phase is not the end of menstrual cycling but the birth of the last child." They believe that the hormones and effects produced by extended lactation could dampen or mask some of the physiological indicators of menopause that Western physicians and women ascribe to the process. They cite studies in non-Western societies that indicate that noncontracepting, lactating women, such as the !Kung, have their last birth between ages 35 and 40. This observation corresponds to what I found in Oregon's Russian Old Believers, a noncontracepting high-fertility population that lived in marginal, small-farming conditions prior to its immigration to the United States in the late 1960s (Hall 1970, 1985). While to some observers of such high-fertility populations the cessation of pregnancy by age 40 is simply due to the women's disinterest in sexual behavior due to the desire to avoid more childbearing, it is also possible and perhaps more likely that high levels of reproduction speed up the agerelated changes in follicular atresia or in some other way impact hormones controlling the menstrual cycle. The plasticity of the reproductive system appears to facilitate different reproductive patterns that depend on the nutrition and health of the women as well as on their reproductive careers. Comparisons between reproductive data from the Old Believers in the1960s and the Hutterites in the 1940s support this perspective. These two groups invite comparisons as both are religious isolates as well as noncontracepting cultures for which detailed demographic data are available (Eaton and Mayer 1953; Hall 1970). Age-specific fertility rates of an 80% sample of the Hutterities from 1946-50 and of a 50% sample of the Old Believers covering the years 1965--68 are provided in Table 1. While the patterns in these two populations are strikingly similar, and both have very high fertility, there are a few pertinent differences. The Hutterite peak fertility rates come in their late twenties and early thirties while the Old Believers start earlier and peak in their early twenties. The Hutterite fertile period continues, although at a very reduced rate, through age 49, whereas no Old Believer births to women over 45 occurred. Differences can be explained by their different ecological situations as well as by different ages of marriage, the Old Believer women marrying as early as 16 while the Hutterites only rarely married before their early twenties. Equally
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Table 1. Age-Specific Birth Rates of Oregon Old Believers, 1965-68, and
Hutterites, 1946-50 Age Class
15-19 20-24 25-29 30-34 35-39 40-44 45-49
Old Believer Birth Rates
Hutterite Birth Rates
157 478 358 357 348 145 0
12 231 383 391 345 208 42
Ratesare standardized as number of births per 1,000women. Old Believerdata are fromHall 1970:79and Hutterite data are from Eaton and Mayer 1953:221.
importantly, the Hutterites, who immigrated in the 1880s, had considerably greater economic and social stability as well as better health care than the Old Believers, w h o had led very unsettled lives in the previous decades. During the twentieth century some had moved from Russia to China, to Hong Kong, to South America, and finally in the late 1960s to Oregon, while others traveled from Turkey to N e w York and then to Oregon. The Hutterite economy is communal whereas the Old Believer nuclear and extended families are responsible for their own welfare, and after all theft moves the men, women, and children were obliged to do farmwork and other labor-intensive jobs. This comparison between two noncontracepting groups that are in many respects similar illustrates the plasticity of reproductive function and suggests that the age of termination of childbearing capacity could be partially dependent both on the number of pregnancies and on life experiences, notably physical labor and various stresses. These observations conform to studies of variation in age of menopause (summarized in Leidy 1994) that statistically show the impact of specific biobehavioral factors on age of menopause. Maternal depletion is likely due in part to maternal exhaustion, which can be caused by a variety of physiological stresses. It would be difficult not to view this plasticity as adaptive; continuation of childbearing past the point of physical exhaustion certainly would threaten the mother's life and thus the welfare of children already born. Energetics is an integral part of the equation; easy availability of food resources during the reproductive years could extend the reproductive period, although in all populations reproduction exacts a toll. Among the Hutterites, Eaton and Mayer (1953) report that there were more men than women in all age groups over 40 and Hutterite males at all age groups had a higher life ex-
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pectancy than women, a finding that the authors attribute to the many pregnancies that women experience. Is Menopause a Medical Disorder, or an Adaptation?
The basis on which m o d e m medicine treats menopause as a medical problem for which treatment is necessary is the concept that menopause is an epiphenomenon that only exists because of recent increases in longevity and thus has no adaptive benefits. For example, Austad (1994) considers that the only adaptive benefit of menopause would be that it allows a woman a period in which to aid her older offspring without the risk of additional pregnancies: "all proposed adaptive advantages of reproductive cessation stem from the exceptional length and intensity of parental care required by human offspring" (1994:256). He rejects his own, narrowly drawn hypothesis because he thinks post-menopause survival is so recent in human history that selection could not have affected it: "Menopause is thus an artifact created by the relatively sudden lengthening of human life over the past several centuries due to improved nutrition and hygiene, plus the availability of effective medical services. Menopause under this scenario is similar to the situation in which wild animals, sheltered and coddled in zoos, routinely outlive their reproductive lives" (Austad 1994:257). While few anthropologists take so extreme a position that, among other problems, appears to stigmatize preindustrial societies, they agree with Austad's recognition that m o d e m female reproductive behavior in the affluent classes, if not among the poor, differs significantly from the condition of most women of prior eras. Along with greater longevity have come new health risks owing to additional estrogen exposure due to later age at first pregnancy, fewer pregnancies, and shorter duration of breast-feeding, all of which produce more cycles that therefore expose women to a heavier load of estrogen and to increased risk of breast cancer (McMichae12001). Since Austad's primary concern appears to be with the health risks that postmenopausal women have, his work by implication considers menopause, if not a full-blown disease, a syndrome in need of treatment. To Austad's credit, he suggests that behavior change (additional calcium in the diet and more physical activity), and not merely prescription drugs, could be part of the treatment. Seven years after his article was published, randomized trials of hormone replacement therapy (HRT) found that the most common menopausal intervention in industrial cultures poses some health risks and few benefits, if any, to women undergoing the transition to menopause or menopause itself (Writing Group for the Women's Health Initiative Investigators 2002; Hays et al. 2003; Wassertheil-Smoller et al. 2003).
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The adaptive view Austad noted is usually referred to as the mother or the grandmother hypothesis, depending on which generation the efforts are believed to enhance (Hawkes et al. 1989; Peccei 1995, 2001). Jocelyn Peccei (1995:83) posits a hypothesis for the evolution of menopause in early hominids that emphasizes energy costs to the extent that they affect "gestation, lactation and childcare that accompanied the continuing encephalization of early hominid offspring" but does not discuss energy costs that would accrue in the elderly w o m a n if endometrial cycling continued, with or without the production of live offspring. She recognizes that an adaptation can arise for one reason but be selected for maintenance for other reasons when the ecological adaptation of the species changes. In another paper (Peccei 2001) she considers the fitness costs of prolonged fertility and physiological constraints that favor pregnancies in early adulthood, recognizing along with other researchers (for example, Ellison 2001; Holman et al. 2000) that the probability of early fetal loss as well as of giving birth to children with chromosomal anomalies increases with the age of the mother. Peccei reviews positive and negative features of viewing menopause as an epiphenomenon and as an adaptation, and, without explicitly ruling out or favoring either paradigm, says that within the latter she favors the mother over the grandmother hypothesis. Lynette Leidy (1994, 1999) takes a broad view of possible adaptations of menopause, as she posits four different rationales supporting an adaptive, evolutionary model. In addition Leidy considers the possibility that menopause, at least as a phenomenon that many w o m e n experience, may be in some sense fortuitous. Menopause in her view firstly could be adaptive by ensuring that mothers are young enough to survive pregnancy, parturition, and the infancy of their offspring, and it also would reduce the probability of ovulation of abnormal oocytes. The grandmother hypothesis is a second possibility, while the third is that menopause is simply a byproduct of ovarian depletion and thus related to a physical constraint. The fourth and final possibility Leidy considers is that menopause is adaptive because it curtails estrogen exposure, a risk factor for breast cancer. Leidy (along with Lancaster and King 1985 and Pavelka and Fedigan 1991) takes issue with the view that menopause is a totally recent phenomenon and therefore a condition that in itself begs for medical treatment. Calling attention to the variation in age and characteristics of menopause that w o m e n experience, Leidy (1994, 1999), Leidy-Sievert (2001), and Peccei (1995, 2001) offer further contrasts with Austad's approach. Health and behavioral factors such as weight, alcohol use, stress levels, and smoking are among the environmental factors believed to affect age at menopause; ongoing cross-cultural research should identify more factors and how they are expressed. To the extent that genetic factors are involved in variation in the number of oocytes within the developing fetus or their rate of loss, there are possible openings where selection could affect the age of menopause.
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TESTING THE ENERGETICS HYPOTHESIS
Testing evolutionary hypotheses regarding processes that arose at times when life history circumstances were different must be indirect and inferential, Strassmann's (1996a, 1996b) tests of an energetics explanation for menstruation being an excellent example. Testing relied on an understanding of the reproductive system grounded in studies of living nonhuman primates as well as on analysis of the energy requirements of m o d e m human females during each phase of the menstrual cycle. This paper argues that at some point during the past several hundred thousand years, some women achieved an age at which their eggs were depleted and their waning reproductive capacity ceased. Selection favored continuation of its cessation even as larger numbers of women achieved that status because of the inclusive fitness benefits it conferred. Additionally, plasticity in the aging process allowed the specifics of the woman's physiological and ecological situation (i.e., number of pregnancies and nutritional and socioeconomic resources) to affect when that period occurred. Testing of adaptive hypotheses of menopause appears more difficult than testing hypotheses related to menstruation in that it appears to run counter to natural selection for fitness, but this objection disappears when inclusive fitness involving the number of children (or even grandchildren) who survive into their own reproductive period is the relevant measure rather than merely the number of live offspring produced. Analogously, evolutionary ecologists for years have understood that for all species there is an appropriate litter size, one that is neither too little nor too large and involves plasticity that facilitates adaptation to a range of environments. Obviously, studies need to be done to measure the life-expectancy and reproductive costs of having too many children and of the benefits of producing the right number. Carefully documented primate studies also can contribute. Jane Goodall's long-term study of Gombe's chimpanzees has provided an unforgettable image in the case study of the maternally successful Flo, a high-status female (Goodal11990). The offspring that Flo produced late in her life stressed her to the point that she could not discipline her next-youngest offspring, Flint. The result was that Flo and both offspring died. "If she had not conceived again, all would, I think, have gone well for Flint. But that last pregnancy drained so much strength and energy from Flo's aging body that she was simply not able to wean Flint" (Goodall 1990:193). In effect, Goodall is arguing that menopause would have benefitted Flo and Flint, and if Flint had lived to reproductive age, Flo's inclusive fitness also would have increased. Would energy depletion due to too many pregnancies reduce a m o d e m woman's total fitness, and does menopause thereby help to preserve a woman as a contributor to her own fitness as well as to the welfare of her
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family? Plasticity issues raised previously suggest that the number of pregnancies that is optimum depends on factors such as the calories available to the woman and her economic and health support systems. More data, as usual, are needed. Leonetti and colleagues' (2003) study of the effect of grandmothers' presence on fertility and survivorship in two quite different ethnic groups in northeast India suggests that grandmothers' efforts help survivorship if the social system is constructed in a way that facilitates grandmothers' contributions, and not when it does not. Her very detailed study of almost 1,400 households is a model of the kind of work that needs to be done to test the grandmother hypothesis--not only to determine whether it works but, if so, to determine the situations in which it works. Nutritional and metabolic assessments of the grandmothers, in comparison with premenopausal women who perform the same work, could add a test of the energetics hypothesis. Probably new research approaches are needed that make bridges between studies in noncontracepting cultures and those in which contraceptives are used to varying degrees. The Lancaster and King suggestion to use age at the birth of the last child to denote the end of the reproductive period would work in populations such as the Hutterities of the 1940s and the Old Believers of the 1960s, who do not use contraceptives and are sexually active, but could not be applied in populations in which some women use contraceptives. At the same time, the standard of a full year without cycling will not work in noncontracepting populations, especially if lactation is prolonged; direct comparisons between these groups are therefore not possible. Thus it would be useful to do large studies using sexually active subjects whose contraceptive use differs and is described and in which the reproductive and hormonal status of women is followed from age 35 on, until it is clear that cessation of cycling has occurred. Preferably these studies would take place cross-culturally and involve women who start their reproductive career early, late, or never. By ascertaining behavioral, economic, and nutritional data, plasticity could be examined. Longitudinal studies, of course, are expensive and difficult, but the answers probably cannot be found without them. CONCLUSIONS
Energetics Explanations The human menstrual cycle, embedded in our evolutionary past, shows an elaboration of trends of fetal nourishment begun in the early primate heritage and elaborated in hominoids. Physical constraints on egg numbers and quality explain the origin of cessation of the menstrual cycle in an ancient period when few individuals survived to experience it. Energy
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costs related to menstrual cycling and failed pregnancies provide insights into how natural selection maintained the menopausal system in m o d e m human ancestors when a significant number of women lived long enough to experience postreproductive life. Although this model provides a basis for understanding both the menstrual cycle and its cessation, energetics is clearly not the only factor involved, but is part of a larger view of all of the physical and ecological constraints acting on the reproductive system. More research needs to be done to document the variation that exists across cultures and environments and the results of different behavioral strategies on fitness. This perspective raises the question of w h y the energetics approach has only recently been considered for menstruation and why previous explanations of menopause have not included energetics even as one of several factors. Following are several ideas based in part on m y observations and experiences as an academic human biologist for 32 years and as a woman who gave birth to two children, experienced over two years in lactation, endured two miscarriages at 10 weeks, and had an easy, non-medicalized transition into menopause. In addition to doing a number of demographic studies I have also discussed these topics with other women and with health professionals, and have tried to balance my personal impressions with m y anthropological insights. There has been too little emphasis on the total menstrual cycle and too much of an emphasis on menstrual bleeding, perhaps because menstruation occurs so frequently in women in our own society and because it has been used to exclude women from certain social activities (Delaney et al. 1988). It has been difficult for Western-reared anthropologists to consider bleeding as merely an evolutionary side effect. As Leidy (1994, 1999) and others have shown, in the preceding century menopause has been considered a medical problem within the conventional medical tradition rather than as part of human life-history. As with menstruation, emphasis has been on those aspects of menopause that are of cultural concern in industrial societies. Anthropologists have not totally appreciated the great difficulties of the food quest in prehistoric populations and in contemporary Third World societies. Although we have observed and have taught about these issues as cultural and political problems, we have found it difficult to incorporate caloric issues into views of the biological evolution of our species. I believe that the difficulty results in large part from our own society's marginalization of anthropological studies; the discipline is looked upon as reporting quaint, if fascinating, studies of the past and of remote peoples but not offering relevance to contemporary or future societies. Clearly, evolutionary anthropologists need to devise a way to change this perception that would ultimately widen our own research programs and enhance their impact.
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Issues for the Future
Seeing evolution as operating today as it has in the past leads me to consider the impacts of recent changes in women's life styles and life histories upon their reproductive ecology. Over the past two centuries in industrial societies and to some extent in developing countries, although the life span of women has increased, their number of pregnancies has decreased. Thus, among affluent sedentary women, expanded food resources in menopausal life can be injurious to health or to self-esteem; rather than aiding survival, as the energy-saving effect of termination of cycling is theorized to have done in the past, it may become a handicap. Using an evolutionary medicine perspective that examines conditions under which adaptations evolved has led to proposals of exercise and dietary changes that could counteract weight gain and osteoporosis, significant risk factors associated with menopause in industrial societies. But the impact of modern society is not totally negative. Several features of industrial societies could alleviate some of the costs of older-age pregnancies and potentially could select for an extended reproductive period, and thus a later menopause. Obviously, additional food resources available in industrial societies can mitigate the energetics costs of higher rates of pregnancy loss that occur due to early spontaneous abortions arising from reduced egg quality. Medical support during the fetal period and at birth could reduce physical constraints that select for fewer rather than more oocytes in the developing female. In pregnancies involving older mothers, technologies such as prenatal testing can be used, if women wish to do so, to identify and either treat or eliminate those fetuses with chromosomal defects. Because there probably are genetic as well as environmental contributions to variation in age at menopause, selection possibly could increase the average age of menopause if the reproductive and energetics costs of delaying childbearing are reduced. In future societies, if mothers and grandmothers are older than has been typical in preindustrial cultures, but if the average life span increases, then the "mother or grandmother hypothesis" could apply even with a later menopause. Whether any of these possibilities is ever realized, however, is completely dependent on a continuation of current life style and life history trends in industrial societies--features such as increased food and economic resources, continuation of trends to later age of first pregnancy (which applies generally to affluent but not to impoverished classes), and extension of reproductive technologies (which is at risk owing to religious and political pressures). These trends may not continue, or may not be extended to all human populations. In the real world, a number of smoldering problems could make the previous century's rising expectations an illusion. These include threats of war (whether local, regional, or world-
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wide) and increased national expenditures for armaments; destabiliTation of health due to new or recurrent epidemics; global climate change that may affect food resources and disease vectors; and overpopulation with stable or diminishing resources. As is true in the past, the evolutionary changes of our species are dependent on contingencies over which individuals exert little control. The flexibility and adaptability of our species doubtless have been selected because of the delicate as well as dynamic interplay between the genetic and environmental forces that shape our destinies. H o w the human species responds to these pressures will affect our biology, including our reproductive ecology. This paper is an expansion of a poster paper presented at the 2002 Human Biology Association meetings in Buffalo, New York. I am grateful for the suggestions as well as the encouragement offered from a number of colleagues during that session. I also want to thank Don Alan Hall for his editing and his encouragement during the writing of this paper, Barry Hewlett for his insightful comments on the penultimate draft, and three anonymous reviewers and the editor of Human Nature for their helpful suggestions. Roberta L. Hall is professor of anthropology at Oregon State University. Her main interest is in evolutionary aspects of human biological variation. Current research involves body composition relationships with resting metabolic rate in males and females and climatic adaptions of nasal morphology. She also enjoys working with the Coquille Indian Tribe of southern Oregon on research concerning their prehistory and is studying ramifications of the coastal hypothesis of North American settlement.
REFERENCES
Austad, S. N. 1994 Menopause: An Evolutionary Perspective. Experimental Gerontology 29: 255-263. Baer, A. 1999 Health, Disease, and Survival. A Biomedicaland GeneticAnalysis of the Orang Asli of Malaysia. Subang Jaya, Malasia: Center for Orang Asli Concerns. Bentley, G. R. 1999 Aping Our Ancestors: Comparative Aspects of Reproductive Ecology. Evolutionary Anthropology 7:175--185 Delaney, J., M. J. Lupton, and E. Toth 1988 The Curse: A Cultural History of Menstruation, revised ed. Champaign, Illinois: University of Illinois Press. Eaton, J. W., and A. J. Mayer 1953 The Social Biology of Very High Fertility among the Hutterites: The Demography of a Unique Population. Human Biology 25:206-264.
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Ellison, P. T. 2001 On Fertile Ground. Cambridge: Harvard University Press. Goodall, J. 1990 Througha Window: My Thirty Years with the Chimpanzees of Gombe. Boston: Houghton Mifflin. Hall, R. L. 1970 Population Biology of the Russian Old Believers of Marion County, Oregon. Ph.D. dissertation, University Microfilms International, Ann Arbor. 1985 Issues for the Future. In Male-Female Differences, R. L. Hall with P. Draper, M. E. Hamilton, D. McGuinness, C. M. Otten, and E. A. Roth. Pp. 299-305. New York: Praeger. Hays, J., J. K. Ockene, R. L. Brunner, J. M. Kotchen, J. E. Manson, R. E. Patterson, A. K. Aragaki, S. A. Shumaker, R. G. Brzyski, A. Z. LaCroix, I. A. Granek, and B. G. Valanis 2003 Effects of Estrogen plus Progestin on Health-Related Quality of Life. The New England Journal of Medicine 348(19):1839-1854. Hawkes, K., J. E O'Connell, and N. G. Blurton Jones 1989 Hardworking Hadza Grandmothers. In Comparative Socioecology, V. Standen and R. A. Foley, editors. Pp. 341-366. Oxford: Blackwell Scientific. Holman, D. J., J. W. Wood, and K. L. Campbell 2000 Age-Dependent Decline of Female Fecundity Is Caused by Early Fetal Loss. In Female Reproductive Ageing, E. R. Velde, F. Broekmans, and P. Pearson, eds. Pp. 123-136. Studies in Profertility Series 9. Camforth, UK: Parthenon. Howell, N. 1979 Demography of the Dobe !Kung. New York: Academic Press. Jeliffe, D. B., and I. Maddocks 1964 Notes on Ecologic Malnutrition in the New Guinea Highlands. Clinical Pediatrics 3(7):432--438. Lancaster J. B., and B. J. King 1985 An Evolutionary Perspective on Menopause In In Her Prime, J. K. Brown and V. Kerns, eds. Pp. 13-20. South Hadley, Massachusetts: Bergin and Garvey. Leidy, L. E. 1994 Biological Aspects of Menopause: Across the Lifespan. Annual Review of Anthropology 23:231-253. 1999 Menopause in Evolutionary Perspective. In Evolutionary Medicine, W. R. Trevathan, E. O. Smith, and J. J. McKenna, eds. Pp. 407-427. New York: Oxford University Press. Leidy-Sievert, L. 2001 Menopause as a Measure of Population Health: An Overview. American Journal of Human Biology 13:429-433. Leonard, W. R., and S. J. Ulijaszek 2002 Energetics and Evolution: An Emerging Research Domain. American Journal of Human Biology 14:547-550. Leonetti, D. L., D. C. Nath, N. S. Hemam, and D. B. Neill 2003 Effect of Grandmother's Presence and Work Effort on Fertility, Survivorship, and Weight in Two Ethnic Groups in N. E. India. American Journal of Human Biology 15:270-271.
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McMichael, A. J. 2001 Human Frontiers, Environments and Disease: Past Patterns, Uncertain Futures. Cambridge: Cambridge University Press. O'Connor, K. A., D. J. Holman, and J. W. Wood 2001 Menstrual Cycle Variability and the Perimenopause. American Journal of Human Biology 13:465--478. Panter-Brick, Catherine 1997 Women's Work and Energetics: ACase Study from Nepal. In The Evolving Female: A Life-History Perspective, Mary Ellen Morbeck, Alison Galloway, and Adrienne L. Zihlman, eds. Pp. 233-241. Princeton: Princeton University Press. Pavelka, M. S. M., and L. M. Fedigan 1991 Menopause: A Comparative Life History Perspective. Yearbook of Physical Anthropology 34:13-38. Peccei, J. S. 1995 A Hypothesis for the Origin and Evolution of Menopause. Maturitas 21: 83-89. 2001 Menopause: Adaptation or Epiphenomenon? Evolutionary Anthropology 10:43-57. Profet, M. 1993 Menstruation as a Defense against Pathogens Transported by Sperm. Quarterly Review of Biology 68:335-386. Strassmann, B. I.
1996a The Evolution of Endometrial Cycles and Menstruation. Quarterly Review of Biology 71:181-220. 1996b Energy Economy in the Evolution of Menstruation. Evolutionary Anthropology 5:157-164. Wassertheil-Smoller, S., S. L. Hendrix, M. Limacher, G. Heiss, C. Kooperberg, A. Baird, T. Kotchen, J. D. Curb, H. Black, J. E. Rossouw, A. Aragaki, M. Safford, E. Stein, S. Laowattana, and W. J. Mysiw 2003 Effect of Estrogen Plus Progestin on Stroke in Postmenopausal Women. Journal of the American Medical Association 289(20):2673-2684. Wood, J. W., D. J. Holman, and K. A. O'Connor 2001 Did Menopause Evolve by Antagonistic Pleiotropy? In Homo: Unsere Herkunft und Zukunft, M. Schultz, ed. Pp. 483--490. Gottingen: Cuvillier Verlag. Writing Group for the Women's Health Initiative Investigators 2002 Risks and Benefits of Estrogen Plus Progestin in Healthy Postmenopausal Women. Journal of the American Medical Association 288:321-333.
To explain the menstrual cycle and menopause, human biologists during the past several decades have developed new models of the evolutionary origins and maintenance of female reproductive patterns that address both ultimate and proximate causation. Hypotheses proposed for these processes generally offer explanations for menstruation or for menopause, but not for both; ultimately, these explanations must be integrated. Reviewing current explanations, this paper offers an energetics-based evolutionary rationale compatible with past adaptations of Homo sapiens and with ecological patterns in small-scale, preindustrial social systems in which food resources vary and sometimes are scarce. KEYWORDS" Energetics; Menopause; Menstrual cycle
Systems of reproduction, which are integral to any species, must be examined in light of energy costs. Humans are large mammals that grow slowly, have long lives, and produce relatively few offspring. Potentially high metabolic costs are associated with reproduction in human females, whose reproductive systems are constrained by physical components inherited from mammalian a n d / o r primate ancestors. The physiology of living primate relatives and models of ecosystems of past members of the hominid lineage, along with studies of diverse m o d e m human populations and Received February 17, 2003; accepted May 28, 2003; revised version received July 3, 2003.
Address all correspondence to Roberta L. Hall, Department of Anthropology, Oregon State University, Corvallis OR 97331. Emaih [email protected] Copyright 2004 by Walter de Gruyter, Inc., New York
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archaeologically known populations, can provide an understanding of how the human female's reproductive system evolved. As Ellison (2001: 167) noted, "In general, there are two major constraints on a female mammal's ultimate reproductive success: energy and time." Research of the past few decades on hormonal and nutritional influences on the menstrual cycle has provided information about how the system is regulated and thus what selection can work on. These developments have made it possible now to ask why, in human females, there is a menstrual cycle involving loss of blood. And then, after 30+ years, why does cycling cease? Hypotheses proposed for these intimately related questions generally offer explanations for menstruation or for menopause, but not both. Ultimate evolutionary explanations for the cycling and for its cessation should complement each other, not only providing an understanding of the reproductive system of human females but also linking human reproductive ecology with the systems of our forebears; proximate mechanisms that offer answers to nitty-gritty "how" questions also must be addressed. This paper provides a review of recent research and proposes an energetics model, integrating the research of other scholars, to explain the origin and maintenance of the menstrual cycle and its cessation in adult hfe. The model is compatible with understandings of biocultural patterns in small-scale, preindustrial social systems that have economies in which food resources fluctuate and food is sometimes scarce. I do not present a full discussion of reproductive ecology, which is provided in Ellison (2001), but instead I provide a selective review of recent developments that underlie energetics theory linking the menstrual cycle and menopause in modern humans. The concept of energetics applies at two levels, the study of the flow of energy through an entire ecological community and the analysis of energy consumption at the individual level, including tradeoffs between potential investments. Both apply here, but my primary focus is on the individual. Examination of the dynamics underlying these processes permits-speculations concerning possible future trends in female reproductive ecology.
BACKGROUND: PHYSIOLOGICAL CONSTRAINTS
Energetics, ecology, and evolution provide a basis for understanding menstruation and menopause. At the most specific level, energetics refers to nutrient transformations of a physical, chemical, or biological system, and thus provides the metabolic cost of key adaptations (Leonard and Ulijaszek 2002). Ecology refers to the totality of relationships between organisms and their environment; by analyzing the flow of energy, ecological analysis can show how life-history patterns help humans fit within the
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ecosystem. At the most abstract level, evolution refers to changes in living beings over time, generally understood to occur as a result of adaptation within an ecological system. Life-history features shared with other primates include a relatively long childhood, extended longevity for at least some members of the population, and a kin-based social organization in which there is overlap between several generations. As in other primate societies, the resource demands of any one individual and of each gender and age group may impact the survival of a traditional human population. Human cultural patterns have been built upon reproductive systems from the primate heritage and have developed rituals (e.g., menarche comingof-age celebrations) that have elaborated as well as accommodated to them. The primate heritage provides the basic reproductive plan that extends to modern human females; for example, all catarrhine primates, including humans, possess elaborated placentas that provide high-quality nourishment of the fetus (Strassmann 1996a, 1996b; Bentley 1999). These placentas require a specialized and elaborated endometrium which represents a substantial metabolic investment that is made during each menstrual cycle and destroyed if an egg is not implanted. Although within each developing female fetus there are several million primitive germ cells, some of which go on to experience the first meiotic division in the second trimester, the number of potential functional eggs is reduced enormously before birth and this number continues to decrease until reproductive function ceases (Ellison 2001:233). This superabundance of germ cells makes it hard to argue that selection has placed a premium on the space that these cells take up, but at some level too much is too much. Perhaps more to the point, the deterioration of this enormous number of cells sets a limit on a woman's reproductive life. The as-yet-unanswered question is whether the pace of loss of egg cells--of follicular atresia--is based on the number of germ cells in the early fetal stage or is independent of it. Would having more germ cells result in additional months or years of reproductive function or would there simply be higher rates of atresia, so that the woman would reach menopause at the same age, regardless of the number of original cells? Some evidence for the latter perspective is that during a woman's reproductive years, the destruction of egg ceils appears to continue whether cycling occurs or is suspended due to pregnancy, nursing, or nutritional deficiencies. Earlier age of menopause appears statistically related to tobacco smoking as well as to other biobehavioral traits (Leidy 1994), suggesting that some negative influences on a woman's physiological status can speed up follicular atresia; what is not known is what, if anything, can slow it down. The tendency of women in a number of nonindustrial, noncontracepting societies to have their last child about age 40 (Lancaster and King 1985) is suggestive of a process of reproductive
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depletion, an effect on the woman's fecundity possibly through the effect of many pregnancies and the stresses to health that accrue in labor-intensive societies. Later I compare reproductive data from two noncontracepting populations that have different environmental stresses. Age-related impacts on egg quality as well as quantity are known. Because eggs deteriorate with age, increased fetal losses in early stages of pregnancy and a greater chance of genetic defects in infants are associated with greater mother's age (Ellison 2001; Holman, Wood, and Campbell 2000). These outcomes, among others associated with normal human aging, favor female reproduction in young adulthood. It is likely that during their first 20 years of reproductive life most of the human females living during the past 100,000 years experienced relatively few menstrual cycles because of pregnancy, lactation, and seasonally reduced food supplies (Strassmann 1996a; Ellison 2001). In part because there are relatively few cycles, benefits of the improved nourishment outweigh the metabolic costs of producing an enriched endometrium. Because of oocyte deterioration and resulting increases in early fetal losses, however, older females would be expected to have more rather than fewer menstruations. Continuation of menstrual cycling past the most fertile 20 years results in some live-born, healthy infants but fewer healthy offspring per conception than in young adult females. Menstrual cycling thus consumes calories for activities that otherwise could support survival of offspring and other family members. A series of 12 to 13 cycles per year adds about 4% to the annual calorie budget (Strassmann 1996b). Cessation of cycling provides a significant savings in energy and resources for m o d e m Third World women, who provide extant examples of nutritional stresses that likely affected prehistoric people (for examples of caloric stresses on women in contemporary nonindustrial societies, see Baer 1999; Jeliffe and Maddocks 1964; and Panter-Brick 1997). Cessation of cycling also reduces the chance of mortality in the pregnancy of an elder female who may be contributing important cultural knowledge as well as labor on behalf of offspring families--knowledge and effort that could promote their survival and welfare.
MENSTRUATION AND MENOPAUSE The Menstrual Cycle Menstrual bleeding has been called "the curse" in Western cultures and menstrual taboos abound in traditional societies as well (Delaney, Lupton, and Toth 1988). How women deal with menstruation and taboos associated with it has been the subject of much popular and scholarly literature.
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This is true even though most women experienced relatively few menstrual cycles until the past hundred years, when lowered infant and child mortality rates encouraged women in industrial countries to use the newly available contraceptives, and it is possible that the rarity of menstruation in traditional societies is one of the factors that produced society's interest in it. Some adaptive elements of menstruation have been hypothesized. Profet (1993) postulated that the blood flow itself was selected because it could cleanse the uterus of sperm-borne germs; an earlier adaptive hypothesis is that menstrual blood may have enhanced hominid females' reproductive options by serving as a signal of fertility. By contrast, an energetics-based theory offered by Beverly Strassmann (1996a, 1996b) sees the vaginal bleeding component of the menstrual cycle as a side effect of selection for an improved blood supply to nourish the developing fetus. Strassmann has drawn her energetics explanation for endometrial cycling, including menstrual bleeding, from research with the Dogon people of Mali and research reports concerning nonhuman primates. The reproductive system of Old World monkeys and apes involves an elaborated microvasculature that supplies the endometrium. Menstruation occurs in other primates and merely is more obvious, more copious, and more common in hominoid females, especially in humans. For Strassmann, the key question concerns why the endometrium is shed rather than maintained, and the solution is found in lesser energy costs involved in doing so. Physical constraints help to explain why the menstrual loss occurs; the specialized, thick-walled endometrium is thought to be too bulky and too differentiated a tissue to be easily resorbed (Ellison 2001:48). Strassmann sees regression of the endometrium as parallel to other tissue regressions, such as the reduction of breast tissue in non-lactating women, and atrophy of the gut and gonads in hibernating mammals. The strongest evidence for the energetics hypothesis of cycling exists in studies Strassmann cites concerning basal metabohc rate differences between women in different phases of the reproductive cycle. Women have higher metabolic rates during their menstrual cycle's luteal phase, when endometrial development occurs, than in their post-menses, pre-ovulatory phase. Postmenopausal women and those in their nonluteal phase have comparable, lower rates. Strassmann (1996a:205) concludes: "The coupling of female reproductive cycling to metabolic cycling is unlikely to be fortuitous. The menstrual/ovarian cycle revs up and revs down, economizing on the energy costs of reproduction." Gillian Bentley (1999) presents data showing how the reproductive physiology of humans and their primate cousins responds with sensitivity to environmental variation, making apparent trade-offs that contribute to reproductive success. She interprets as adaptive the reduced fecundity of humans and other primates that results from seasonal shortages of food
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or shortages by environmental downturns. By contrast, physicians tend to see such effects as reproductive dysfunction and are less likely to use an evolutionary model. Bentley's perspective on reproductive processes in primates, including humans, like Strassmann's, is based in energetics.
Menopause The evolutionary problem posed by menopause is more complex than that of menstruation because females in all mammal species require ovulation and some kind of cyclic reproductive potential in order to have any reproductive success at all--but all mammalian females can experience reproductive success without living long enough to experience menopause. Thus, the fitness question arises as it does in any adaptation that occurs following an organism's reproductive years. In examining menopause, it is essential to differentiate theories about its origins, which likely occurred when hominid life spans were shorter, from theories about selective pressures that maintain it. Related to this issue are disagreements about whether nonhuman species experience it and whether sufficient human females in prehistory experienced a postmenopausal stage to permit selection to favor it. Although much is known about menopausal processes, some of the most basic descriptive data, particularly concerning variability among women, are still being gathered (D. J. Holman, personal communication, 2002; O'Connor, Holman, and Wood 2001), and key concepts are still being defined (Pavelka and Fedigan 1991). For example, the convention is that premature infertility is that which occurs before age 40 (Leidy 1999:408); however, the timing of human menopause varies considerably, so setting any date as "premature" itself may be premature. Some evolutionary explanations of cessation of menses have viewed menopause as a discrete event rather than a process of gradual reduction in the probability of becoming pregnant and producing a live offspring (Austad 1994; Peccei 1995, 2001). Regarding the process as gradual, rather than as an all-or-nothing event, invites consideration of various physical features that produce age-related decline in fecundity (Holman, Wood, and Campbell 2000). Wood, Holrnan, and O'Connor (2001) and Ellison (2001) identify follicular depletion as the end point of a process of follicular depletion, which thus is the proximate cause of menopause. Lancaster and King (1985) raise many key issues concerning menopause, its origins and maintenance, including whether other species experience menopause and the extent to which women in the past experienced it. They recognize that the experience of m o d e m women is quite different than that of earlier women and women in nonindustrial societies because of the presence in m o d e m cultures of extended life expectancies, fewer pregnancies with more menstrual cycles, and less time involved in lacta-
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tion. Their review of prior demographic studies on diverse extant ethnographic populations, including Nancy Howell's (1979) detailed and seminal work with the !Kung, leads them to the opinion that a human life-history pattern that includes menopause could have existed long enough for selection maintaining it to occur. Whereas many researchers consider menopause the termination of menstrual cycling (Pavelka and Fedigan 1991), usually defined operationally by the passing of a full year with no menstruation, for Lancaster and King (1985:15) "the relevant statistic for establishing the end of the reproductive phase is not the end of menstrual cycling but the birth of the last child." They believe that the hormones and effects produced by extended lactation could dampen or mask some of the physiological indicators of menopause that Western physicians and women ascribe to the process. They cite studies in non-Western societies that indicate that noncontracepting, lactating women, such as the !Kung, have their last birth between ages 35 and 40. This observation corresponds to what I found in Oregon's Russian Old Believers, a noncontracepting high-fertility population that lived in marginal, small-farming conditions prior to its immigration to the United States in the late 1960s (Hall 1970, 1985). While to some observers of such high-fertility populations the cessation of pregnancy by age 40 is simply due to the women's disinterest in sexual behavior due to the desire to avoid more childbearing, it is also possible and perhaps more likely that high levels of reproduction speed up the agerelated changes in follicular atresia or in some other way impact hormones controlling the menstrual cycle. The plasticity of the reproductive system appears to facilitate different reproductive patterns that depend on the nutrition and health of the women as well as on their reproductive careers. Comparisons between reproductive data from the Old Believers in the1960s and the Hutterites in the 1940s support this perspective. These two groups invite comparisons as both are religious isolates as well as noncontracepting cultures for which detailed demographic data are available (Eaton and Mayer 1953; Hall 1970). Age-specific fertility rates of an 80% sample of the Hutterities from 1946-50 and of a 50% sample of the Old Believers covering the years 1965--68 are provided in Table 1. While the patterns in these two populations are strikingly similar, and both have very high fertility, there are a few pertinent differences. The Hutterite peak fertility rates come in their late twenties and early thirties while the Old Believers start earlier and peak in their early twenties. The Hutterite fertile period continues, although at a very reduced rate, through age 49, whereas no Old Believer births to women over 45 occurred. Differences can be explained by their different ecological situations as well as by different ages of marriage, the Old Believer women marrying as early as 16 while the Hutterites only rarely married before their early twenties. Equally
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Table 1. Age-Specific Birth Rates of Oregon Old Believers, 1965-68, and
Hutterites, 1946-50 Age Class
15-19 20-24 25-29 30-34 35-39 40-44 45-49
Old Believer Birth Rates
Hutterite Birth Rates
157 478 358 357 348 145 0
12 231 383 391 345 208 42
Ratesare standardized as number of births per 1,000women. Old Believerdata are fromHall 1970:79and Hutterite data are from Eaton and Mayer 1953:221.
importantly, the Hutterites, who immigrated in the 1880s, had considerably greater economic and social stability as well as better health care than the Old Believers, w h o had led very unsettled lives in the previous decades. During the twentieth century some had moved from Russia to China, to Hong Kong, to South America, and finally in the late 1960s to Oregon, while others traveled from Turkey to N e w York and then to Oregon. The Hutterite economy is communal whereas the Old Believer nuclear and extended families are responsible for their own welfare, and after all theft moves the men, women, and children were obliged to do farmwork and other labor-intensive jobs. This comparison between two noncontracepting groups that are in many respects similar illustrates the plasticity of reproductive function and suggests that the age of termination of childbearing capacity could be partially dependent both on the number of pregnancies and on life experiences, notably physical labor and various stresses. These observations conform to studies of variation in age of menopause (summarized in Leidy 1994) that statistically show the impact of specific biobehavioral factors on age of menopause. Maternal depletion is likely due in part to maternal exhaustion, which can be caused by a variety of physiological stresses. It would be difficult not to view this plasticity as adaptive; continuation of childbearing past the point of physical exhaustion certainly would threaten the mother's life and thus the welfare of children already born. Energetics is an integral part of the equation; easy availability of food resources during the reproductive years could extend the reproductive period, although in all populations reproduction exacts a toll. Among the Hutterites, Eaton and Mayer (1953) report that there were more men than women in all age groups over 40 and Hutterite males at all age groups had a higher life ex-
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pectancy than women, a finding that the authors attribute to the many pregnancies that women experience. Is Menopause a Medical Disorder, or an Adaptation?
The basis on which m o d e m medicine treats menopause as a medical problem for which treatment is necessary is the concept that menopause is an epiphenomenon that only exists because of recent increases in longevity and thus has no adaptive benefits. For example, Austad (1994) considers that the only adaptive benefit of menopause would be that it allows a woman a period in which to aid her older offspring without the risk of additional pregnancies: "all proposed adaptive advantages of reproductive cessation stem from the exceptional length and intensity of parental care required by human offspring" (1994:256). He rejects his own, narrowly drawn hypothesis because he thinks post-menopause survival is so recent in human history that selection could not have affected it: "Menopause is thus an artifact created by the relatively sudden lengthening of human life over the past several centuries due to improved nutrition and hygiene, plus the availability of effective medical services. Menopause under this scenario is similar to the situation in which wild animals, sheltered and coddled in zoos, routinely outlive their reproductive lives" (Austad 1994:257). While few anthropologists take so extreme a position that, among other problems, appears to stigmatize preindustrial societies, they agree with Austad's recognition that m o d e m female reproductive behavior in the affluent classes, if not among the poor, differs significantly from the condition of most women of prior eras. Along with greater longevity have come new health risks owing to additional estrogen exposure due to later age at first pregnancy, fewer pregnancies, and shorter duration of breast-feeding, all of which produce more cycles that therefore expose women to a heavier load of estrogen and to increased risk of breast cancer (McMichae12001). Since Austad's primary concern appears to be with the health risks that postmenopausal women have, his work by implication considers menopause, if not a full-blown disease, a syndrome in need of treatment. To Austad's credit, he suggests that behavior change (additional calcium in the diet and more physical activity), and not merely prescription drugs, could be part of the treatment. Seven years after his article was published, randomized trials of hormone replacement therapy (HRT) found that the most common menopausal intervention in industrial cultures poses some health risks and few benefits, if any, to women undergoing the transition to menopause or menopause itself (Writing Group for the Women's Health Initiative Investigators 2002; Hays et al. 2003; Wassertheil-Smoller et al. 2003).
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The adaptive view Austad noted is usually referred to as the mother or the grandmother hypothesis, depending on which generation the efforts are believed to enhance (Hawkes et al. 1989; Peccei 1995, 2001). Jocelyn Peccei (1995:83) posits a hypothesis for the evolution of menopause in early hominids that emphasizes energy costs to the extent that they affect "gestation, lactation and childcare that accompanied the continuing encephalization of early hominid offspring" but does not discuss energy costs that would accrue in the elderly w o m a n if endometrial cycling continued, with or without the production of live offspring. She recognizes that an adaptation can arise for one reason but be selected for maintenance for other reasons when the ecological adaptation of the species changes. In another paper (Peccei 2001) she considers the fitness costs of prolonged fertility and physiological constraints that favor pregnancies in early adulthood, recognizing along with other researchers (for example, Ellison 2001; Holman et al. 2000) that the probability of early fetal loss as well as of giving birth to children with chromosomal anomalies increases with the age of the mother. Peccei reviews positive and negative features of viewing menopause as an epiphenomenon and as an adaptation, and, without explicitly ruling out or favoring either paradigm, says that within the latter she favors the mother over the grandmother hypothesis. Lynette Leidy (1994, 1999) takes a broad view of possible adaptations of menopause, as she posits four different rationales supporting an adaptive, evolutionary model. In addition Leidy considers the possibility that menopause, at least as a phenomenon that many w o m e n experience, may be in some sense fortuitous. Menopause in her view firstly could be adaptive by ensuring that mothers are young enough to survive pregnancy, parturition, and the infancy of their offspring, and it also would reduce the probability of ovulation of abnormal oocytes. The grandmother hypothesis is a second possibility, while the third is that menopause is simply a byproduct of ovarian depletion and thus related to a physical constraint. The fourth and final possibility Leidy considers is that menopause is adaptive because it curtails estrogen exposure, a risk factor for breast cancer. Leidy (along with Lancaster and King 1985 and Pavelka and Fedigan 1991) takes issue with the view that menopause is a totally recent phenomenon and therefore a condition that in itself begs for medical treatment. Calling attention to the variation in age and characteristics of menopause that w o m e n experience, Leidy (1994, 1999), Leidy-Sievert (2001), and Peccei (1995, 2001) offer further contrasts with Austad's approach. Health and behavioral factors such as weight, alcohol use, stress levels, and smoking are among the environmental factors believed to affect age at menopause; ongoing cross-cultural research should identify more factors and how they are expressed. To the extent that genetic factors are involved in variation in the number of oocytes within the developing fetus or their rate of loss, there are possible openings where selection could affect the age of menopause.
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TESTING THE ENERGETICS HYPOTHESIS
Testing evolutionary hypotheses regarding processes that arose at times when life history circumstances were different must be indirect and inferential, Strassmann's (1996a, 1996b) tests of an energetics explanation for menstruation being an excellent example. Testing relied on an understanding of the reproductive system grounded in studies of living nonhuman primates as well as on analysis of the energy requirements of m o d e m human females during each phase of the menstrual cycle. This paper argues that at some point during the past several hundred thousand years, some women achieved an age at which their eggs were depleted and their waning reproductive capacity ceased. Selection favored continuation of its cessation even as larger numbers of women achieved that status because of the inclusive fitness benefits it conferred. Additionally, plasticity in the aging process allowed the specifics of the woman's physiological and ecological situation (i.e., number of pregnancies and nutritional and socioeconomic resources) to affect when that period occurred. Testing of adaptive hypotheses of menopause appears more difficult than testing hypotheses related to menstruation in that it appears to run counter to natural selection for fitness, but this objection disappears when inclusive fitness involving the number of children (or even grandchildren) who survive into their own reproductive period is the relevant measure rather than merely the number of live offspring produced. Analogously, evolutionary ecologists for years have understood that for all species there is an appropriate litter size, one that is neither too little nor too large and involves plasticity that facilitates adaptation to a range of environments. Obviously, studies need to be done to measure the life-expectancy and reproductive costs of having too many children and of the benefits of producing the right number. Carefully documented primate studies also can contribute. Jane Goodall's long-term study of Gombe's chimpanzees has provided an unforgettable image in the case study of the maternally successful Flo, a high-status female (Goodal11990). The offspring that Flo produced late in her life stressed her to the point that she could not discipline her next-youngest offspring, Flint. The result was that Flo and both offspring died. "If she had not conceived again, all would, I think, have gone well for Flint. But that last pregnancy drained so much strength and energy from Flo's aging body that she was simply not able to wean Flint" (Goodall 1990:193). In effect, Goodall is arguing that menopause would have benefitted Flo and Flint, and if Flint had lived to reproductive age, Flo's inclusive fitness also would have increased. Would energy depletion due to too many pregnancies reduce a m o d e m woman's total fitness, and does menopause thereby help to preserve a woman as a contributor to her own fitness as well as to the welfare of her
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family? Plasticity issues raised previously suggest that the number of pregnancies that is optimum depends on factors such as the calories available to the woman and her economic and health support systems. More data, as usual, are needed. Leonetti and colleagues' (2003) study of the effect of grandmothers' presence on fertility and survivorship in two quite different ethnic groups in northeast India suggests that grandmothers' efforts help survivorship if the social system is constructed in a way that facilitates grandmothers' contributions, and not when it does not. Her very detailed study of almost 1,400 households is a model of the kind of work that needs to be done to test the grandmother hypothesis--not only to determine whether it works but, if so, to determine the situations in which it works. Nutritional and metabolic assessments of the grandmothers, in comparison with premenopausal women who perform the same work, could add a test of the energetics hypothesis. Probably new research approaches are needed that make bridges between studies in noncontracepting cultures and those in which contraceptives are used to varying degrees. The Lancaster and King suggestion to use age at the birth of the last child to denote the end of the reproductive period would work in populations such as the Hutterities of the 1940s and the Old Believers of the 1960s, who do not use contraceptives and are sexually active, but could not be applied in populations in which some women use contraceptives. At the same time, the standard of a full year without cycling will not work in noncontracepting populations, especially if lactation is prolonged; direct comparisons between these groups are therefore not possible. Thus it would be useful to do large studies using sexually active subjects whose contraceptive use differs and is described and in which the reproductive and hormonal status of women is followed from age 35 on, until it is clear that cessation of cycling has occurred. Preferably these studies would take place cross-culturally and involve women who start their reproductive career early, late, or never. By ascertaining behavioral, economic, and nutritional data, plasticity could be examined. Longitudinal studies, of course, are expensive and difficult, but the answers probably cannot be found without them. CONCLUSIONS
Energetics Explanations The human menstrual cycle, embedded in our evolutionary past, shows an elaboration of trends of fetal nourishment begun in the early primate heritage and elaborated in hominoids. Physical constraints on egg numbers and quality explain the origin of cessation of the menstrual cycle in an ancient period when few individuals survived to experience it. Energy
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costs related to menstrual cycling and failed pregnancies provide insights into how natural selection maintained the menopausal system in m o d e m human ancestors when a significant number of women lived long enough to experience postreproductive life. Although this model provides a basis for understanding both the menstrual cycle and its cessation, energetics is clearly not the only factor involved, but is part of a larger view of all of the physical and ecological constraints acting on the reproductive system. More research needs to be done to document the variation that exists across cultures and environments and the results of different behavioral strategies on fitness. This perspective raises the question of w h y the energetics approach has only recently been considered for menstruation and why previous explanations of menopause have not included energetics even as one of several factors. Following are several ideas based in part on m y observations and experiences as an academic human biologist for 32 years and as a woman who gave birth to two children, experienced over two years in lactation, endured two miscarriages at 10 weeks, and had an easy, non-medicalized transition into menopause. In addition to doing a number of demographic studies I have also discussed these topics with other women and with health professionals, and have tried to balance my personal impressions with m y anthropological insights. There has been too little emphasis on the total menstrual cycle and too much of an emphasis on menstrual bleeding, perhaps because menstruation occurs so frequently in women in our own society and because it has been used to exclude women from certain social activities (Delaney et al. 1988). It has been difficult for Western-reared anthropologists to consider bleeding as merely an evolutionary side effect. As Leidy (1994, 1999) and others have shown, in the preceding century menopause has been considered a medical problem within the conventional medical tradition rather than as part of human life-history. As with menstruation, emphasis has been on those aspects of menopause that are of cultural concern in industrial societies. Anthropologists have not totally appreciated the great difficulties of the food quest in prehistoric populations and in contemporary Third World societies. Although we have observed and have taught about these issues as cultural and political problems, we have found it difficult to incorporate caloric issues into views of the biological evolution of our species. I believe that the difficulty results in large part from our own society's marginalization of anthropological studies; the discipline is looked upon as reporting quaint, if fascinating, studies of the past and of remote peoples but not offering relevance to contemporary or future societies. Clearly, evolutionary anthropologists need to devise a way to change this perception that would ultimately widen our own research programs and enhance their impact.
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Issues for the Future
Seeing evolution as operating today as it has in the past leads me to consider the impacts of recent changes in women's life styles and life histories upon their reproductive ecology. Over the past two centuries in industrial societies and to some extent in developing countries, although the life span of women has increased, their number of pregnancies has decreased. Thus, among affluent sedentary women, expanded food resources in menopausal life can be injurious to health or to self-esteem; rather than aiding survival, as the energy-saving effect of termination of cycling is theorized to have done in the past, it may become a handicap. Using an evolutionary medicine perspective that examines conditions under which adaptations evolved has led to proposals of exercise and dietary changes that could counteract weight gain and osteoporosis, significant risk factors associated with menopause in industrial societies. But the impact of modern society is not totally negative. Several features of industrial societies could alleviate some of the costs of older-age pregnancies and potentially could select for an extended reproductive period, and thus a later menopause. Obviously, additional food resources available in industrial societies can mitigate the energetics costs of higher rates of pregnancy loss that occur due to early spontaneous abortions arising from reduced egg quality. Medical support during the fetal period and at birth could reduce physical constraints that select for fewer rather than more oocytes in the developing female. In pregnancies involving older mothers, technologies such as prenatal testing can be used, if women wish to do so, to identify and either treat or eliminate those fetuses with chromosomal defects. Because there probably are genetic as well as environmental contributions to variation in age at menopause, selection possibly could increase the average age of menopause if the reproductive and energetics costs of delaying childbearing are reduced. In future societies, if mothers and grandmothers are older than has been typical in preindustrial cultures, but if the average life span increases, then the "mother or grandmother hypothesis" could apply even with a later menopause. Whether any of these possibilities is ever realized, however, is completely dependent on a continuation of current life style and life history trends in industrial societies--features such as increased food and economic resources, continuation of trends to later age of first pregnancy (which applies generally to affluent but not to impoverished classes), and extension of reproductive technologies (which is at risk owing to religious and political pressures). These trends may not continue, or may not be extended to all human populations. In the real world, a number of smoldering problems could make the previous century's rising expectations an illusion. These include threats of war (whether local, regional, or world-
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wide) and increased national expenditures for armaments; destabiliTation of health due to new or recurrent epidemics; global climate change that may affect food resources and disease vectors; and overpopulation with stable or diminishing resources. As is true in the past, the evolutionary changes of our species are dependent on contingencies over which individuals exert little control. The flexibility and adaptability of our species doubtless have been selected because of the delicate as well as dynamic interplay between the genetic and environmental forces that shape our destinies. H o w the human species responds to these pressures will affect our biology, including our reproductive ecology. This paper is an expansion of a poster paper presented at the 2002 Human Biology Association meetings in Buffalo, New York. I am grateful for the suggestions as well as the encouragement offered from a number of colleagues during that session. I also want to thank Don Alan Hall for his editing and his encouragement during the writing of this paper, Barry Hewlett for his insightful comments on the penultimate draft, and three anonymous reviewers and the editor of Human Nature for their helpful suggestions. Roberta L. Hall is professor of anthropology at Oregon State University. Her main interest is in evolutionary aspects of human biological variation. Current research involves body composition relationships with resting metabolic rate in males and females and climatic adaptions of nasal morphology. She also enjoys working with the Coquille Indian Tribe of southern Oregon on research concerning their prehistory and is studying ramifications of the coastal hypothesis of North American settlement.
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