Evolutionary perspectives on pregnancy: maternal age at menarche and infant birth weight

ARTICLE IN PRESS

Social Science & Medicine 57 (2003) 1771–1781

Evolutionary perspectives on pregnancy: maternal age at menarche and infant birth weight David A. Coall*, James S. Chisholm School of Anatomy and Human Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia

Abstract We present a novel evolutionary analysis of low birth weight (LBW). LBW is a well-known risk factor for increased infant morbidity and mortality. Its causes, however, remain obscure and there is a vital need for new approaches. Life history theory, the most dynamic branch of evolutionary ecology, provides important insights into the potential role of LBW in human reproductive strategies. Life history theory’s primary rationale for LBW is the trade-off between current and future reproduction. This trade-off underlies the prediction that under conditions of environmental risk and uncertainty (experienced subjectively as psychosocial stress) it can be evolutionarily adaptive to reproduce at a young age. One component of early reproduction is early menarche. Early reproduction tends to maximise offspring quantity, but parental investment theory’s assumption of a quantity–quality trade-off holds that maximizing offspring quantity reduces quality, of which LBW may be the major component. We therefore predict that women who experienced early psychosocial stress and had early menarche are more likely to produce LBW babies. Furthermore, the extension of parent–offspring conflict theory in utero suggests that the fetus will attempt to resist its mother’s efforts to reduce its resources, allocating more of what it does receive to the placenta in order to extract more maternal resources to increase its own quality. We propose that LBW babies born to mothers who experience early psychosocial stress and have early menarche are more likely to have a higher placental/fetal weight ratio. We review evidence in support of these hypotheses and discuss the implications for public health. r 2003 Elsevier Ltd. All rights reserved. Keywords: Birth weight; Age at menarche; Evolutionary theory; Psychosocial stress

Introduction Low birth weight (LBW) is a well-known risk factor for infant morbidity and mortality (e.g., McCormick, 1985; Henriksen, 1999) and probably contributes to several adult diseases (e.g., Phillips, 1998; Barker, 1999; Wahlbeck, Forsen, Osmond, Barker, & Eriksson, 2001). Nonetheless, the causes of LBW remain obscure and there is a vital need for new approaches (Kogan, 1995). The deductive use of evolutionary theory suggests that a woman’s age at menarche may influence her offspring’s birth weight, thereby offering a new perspective on the

*Corresponding author. Fax: +(08)-9380-1051. E-mail address: [email protected] (D.A. Coall).

causes of variability in birth weight and the possibility of novel intervention and prevention strategies. The causes, correlates and consequences of both age at menarche and birth weight have been studied extensively. The association between perinatal factors surrounding a girl’s birth and her subsequent age at menarche has also been studied (e.g., Persson et al., 1999; Adair, 2001). There has been little research, however, on links between a woman’s age at menarche and her children’s birth weight. Our goal is to stimulate such research by reviewing theory and evidence indicating that these links are real. The secular trend toward earlier menarche is usually explained at the population level as an indicator of improved health and nutrition (Tanner, 1962, 1968; Marshall & Tanner, 1986). Early menarche has also

0277-9536/03/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0277-9536(03)00022-4

ARTICLE IN PRESS 1772

D.A. Coall, J.S. Chisholm / Social Science & Medicine 57 (2003) 1771–1781

been associated with increased body weight, body fatness and body mass (Wellens et al., 1992; Merzenich, Boeing, & Wahrendorf, 1993), which persist into adulthood (Sherman, Wallace, Bean, & Schlabaugh, 1981; Garn, LaVelle, Rosenberg, & Hawthorne, 1986; Laitinen, Power, & Jarvelin, 2001). Body weight, body fatness and body mass are also associated with increased birth weight (Frisch, 1988). If early menarche indicates good maternal health and nutrition and a physique associated with increased birth weight, one might then assume that early menarche would be associated with positive reproductive outcomes (Frisch, 1988). However, Scholl et al. (1989) found that early menarche was associated with LBW through the specific mechanism of intra-uterine growth restriction (IUGR). Therefore, the secular trend toward earlier maturation may be a double-edged sword in relation to birth weight. While age at menarche is partly under genetic control, life history theory provides a powerful evolutionary rationale for expecting significant differences in the developmental environments of early and late maturers. We will therefore propose that LBW may be usefully viewed as part of an adaptive response to environmental risk and uncertainty rather than pathology.

Life history theory and the current–future trade-off Life history theory provides a conceptual framework that can in principle explain the relationship between a woman’s early environment, her age at menarche and her children’s birth weights. Life history theory is the branch of evolutionary ecology devoted to the study of survival, growth and development and reproduction (i.e. a life cycles) in an ecological context. Among the most

commonly investigated life history traits are size and number of offspring, age and size at sexual maturity and lifespan. Because each of our direct ancestors left descendants (culminating in us), by definition they did the work necessary to survive, grow and develop and reproduce. To do this work they had to consume resources. Because resources (e.g., energy, nutrients, safety, time, etc.) are always limited trade-offs are inevitable. For example, when a woman’s resources are limited they may be diverted from reproduction to survival, resulting in delayed menarche. Therefore, life history theory expects selection to favour phenotypic mechanisms (e.g., endocrine, developmental, psychological, etc.) that allocate finite resources between competing alternatives in a manner that ultimately results in greater fitness (Low, 1978; Stearns, 1992; Daan & Tinbergen, 1997; Chisholm, 1999; Hill & Kaplan, 1999). The most all-encompassing trade-off is that between current and future reproduction. Also known as the General Life History Problem (Schaffer, 1983), this model predicts the optimal allocation of resources to reproduction at a given age based on the assumption that there is a trade-off between current and future reproduction. Thus an individual’s short-term (current) reproduction may reduce his/her long-term (future) reproduction. This trade-off may occur via two pathways: increasing current reproduction (1) may require the current consumption of resources that would have produced greater fitness if utilised in the future and/or (2) may reduce the parent’s probability of surviving into the future to reproduce again (Borgerhoff Mulder, 1992; Stearns, 1992; Charnov, 1993). The phenotypic mechanisms that allocate resources between life history traits produce reproductive strategies. Fig. 1 is a schematic representation of the

Lineage A

Lineage B

High environmental risk and uncertainty

Low environmental risk and uncertainty

Generation G1 G2 G3 G4 Reproductive Success (RS) after generation 4 Maximum RS per generation Mean RS per generation Intergenerational variance in RS

Lineage A 9 Descendants 3 2 1

Lineage B 16 Descendants 2 2 0

Fig. 1. A schematic representation of the intergenerational trade-off between current and future reproductive strategies (adapted from Chisholm, 1993, 1995).

ARTICLE IN PRESS D.A. Coall, J.S. Chisholm / Social Science & Medicine 57 (2003) 1771–1781

intergenerational trade-offs entailed for a strategy that maximises current reproduction (Lineage A) and one that maximises future reproduction (Lineage B). The two lineages are followed for the arbitrary period of four generations (asexual reproduction is used to simplify the illustration). Lineage A, which resides in an environment of high risk and uncertainty, maximises current reproduction by reproducing earlier and/or often. Because its environment is risky and uncertain many offspring die before they reproduce (represented by dashed lines). Lineage A’s adaptive challenge is to maximise the probability of having at least some offspring survive to reproduce, thereby minimising the probability of lineage extinction. Lineage B occupies a safe and predictable environment in which all offspring survive, which makes it adaptive to maximise future reproduction. Lineage B does this by delaying sexual maturity and reproduction, ultimately producing fewer offspring. Each of these offspring, however, receives relatively more parental investment. Because Lineage B’s environment is safe and predictable, parents and offspring alike are more likely to survive and offspring are better able to benefit from extended parental investment. The most important lesson of Fig. 1 is that each reproductive strategy is optimal in its particular environment. Maximising current reproduction under risky and uncertain conditions may at first seem maladaptive. How could it be adaptive to produce large quantities of low quality children, thereby further handicapping them in an already risky environment? Why aren’t individuals always selected to produce fewer young of higher quality, who receive high levels of investment and ultimately have a greater chance of survival? The answer is that in risky and uncertain environments parents may lack the resources to make much difference in their children’s chances of survival. When parents are unable to improve offspring quality it will often be evolutionarily rational to increase offspring quantity. One way to do this is to minimise the time before sexual maturity (i.e., early menarche), which maximises the probability of reproducing before dying. Moreover, producing many children maximises the probability that at least some will survive and reproduce. Age at menarche may, therefore, be a good indicator of the reproductive strategy being pursued. Menarche, of course, does not imply sexual activity, let alone early reproduction, but cross-cultural studies often find that age at menarche, age at first sexual intercourse and age at first birth are correlated (e.g., Udry & Cliquet, 1982).

Attachment and the development of alternative reproductive strategies If early reproduction is adaptive in risky and uncertain environments, the question then becomes,

1773

how do individuals detect environmental risk and uncertainty? In a novel synthesis of evolutionary biology and attachment theory (Bowlby, 1969), Belsky, Steinberg and Draper (1991) suggested that the degree of early psychosocial stress (roughly 0–7 years) is critical for the development of alternative reproductive strategies. They proposed that inconsistent or insensitive parenting increases risk for insecure attachment and that inconsistent and insensitive parenting would be more likely under conditions of environmental risk and uncertainty. They also proposed that the psychosocial stress associated with insecure attachment (as both cause and effect) would accelerate sexual maturity.1 While Belsky and colleagues first proposed that the early psychosocial stress of insecure attachment was important in the ontogeny of alternative reproductive strategies, Chisholm (1993, 1995, 1996, 1999) used life history theory as the basis for proposing an association between mortality rates, early stress and age at maturity.2 He argued that ultimately, the most consistent cause of insecure attachment would be the risky and uncertain environments that cause high mortality rates. Because children do not directly perceive mortality rates, Chisholm proposed that the attachment process functioned as a phenotypic mechanism enabling the child to gauge environmental risk and uncertainty indirectly. The negative emotions (e.g., anger, fear, despair) associated with risky and uncertain environments affect parents’ sensitivity and responsiveness to children’s signals, thereby contributing to insecure attachment. Because parents have always constituted children’s ‘‘environment of evolutionary adaptedness’’ (Bowlby, 1969, p. 50), the adaptive function of parental investment in buffering children against environmental risk and uncertainty also provides them with valuable information about their local environment. Thus the quality of a child’s attachment may be adaptive at least

1 Perhaps because chronic hypothalamic-pituitary-adrenal system activation results in chronic elevated cortisol levels, which may result in early activation of the hypothalamicpituitary-ovarian system (e.g., Herman-Giddens, Sandler, & Friedman, 1988; Worthman, 1999a, 1999b). 2 Comparative studies of mortality rates and variation in life history traits across mammalian species suggest that ‘‘mortality may be a unifying concept in explaining much of life history variation’’ (Promislow & Harvey, 1991, p. 126). It is also proposed that mortality rates are the major mediating factor between ecology and life history traits (Promislow & Harvey, 1990, 1991; Hill, 1993; Stearns, 1992). Experimental studies looking at mortality rates and life history traits have focused on invertebrates (Promislow & Harvey, 1991). In a comparative analysis across 48 mammalian species, Promislow and Harvey (1990) also found high mortality rates were correlated with early age at sexual maturity and other life history traits, which persisted after controlling for the effect of body weight.

ARTICLE IN PRESS 1774

D.A. Coall, J.S. Chisholm / Social Science & Medicine 57 (2003) 1771–1781

in part by entraining the development of its optimal reproductive strategy.

Attachment and health inequalities The overwhelming evidence that social inequality is associated with increased morbidity, mortality and diminished life expectancy (e.g., Davey-Smith, Wentworth, Neaton, Stamler & Stamler, 1996; DaveySmith, Neaton, Wentworth, Stamler & Stamler, 1996; Wilkinson, 1994, 1997; Acheson, 1998) means that social inequality is a major cause of environmental risk and uncertainty (e.g., Marris, 1996; Sen, 1992, 1999). The cumulative inequalities in health and well-being that are generated by social inequalities therefore become the causes and correlates of local mortality on which attachment may be partly dependent (Chisholm, 1999; Chisholm & Burbank, 2001). There is good evidence that insecure attachment is more prevalent in populations living under conditions of risk and uncertainty (i.e., poverty and inequality: Belsky, 1996; McEwen & Seeman, 1999; McLoyd, 1990; Repetti, Taylor & Seeman, 2002). When these conditions become chronic they may foster the intergenerational transmission of insecure attachment (Fonagy, 1996; Fonagy & Higgitt, 2000; Chisholm, 1999). Life history theory thus provides a framework capable of uniting the disparate disciplines of evolutionary theory, population health and developmental psychology. This suggests that our evolutionary model may have implications for social as well as public health policy— for ‘‘improving child development as a society’’ (Hertzman, 2000, p. 15). Early childhood interventions targeting health inequalities can have short and longterm benefits for both children and parents (Fonagy & Higgitt, 2000). Our model may therefore be useful in developing policy that improves not only individual, but also population level outcomes (which are too often neglected: Davey-Smith, Ebrahim & Frankel, 2001). Evolutionary public health provides a rational basis for expecting that reducing social inequality will reduce environmental risk and uncertainty at the population level and ultimately promote healthier communities.

Early psychosocial stress and age at menarche To our knowledge no studies have directly tested Belsky et al.’s (1991) prediction of an association between insecure attachment per se and age at menarche. On the other hand, many studies report a relationship between various measures of early psychosocial stress and age at menarche, including: father absence (Surbey, 1990; Moffit, Caspi, Belsky, & Silva, 1992; Campbell & Udry, 1995); fathers’ investment in

the family (Ellis, McFadyen-Ketchum, Dodge, Pettit, & Bates, 1999); number of major life events (Surbey, 1990; Coall & Chisholm, 1999); family conflict (Moffit et al., 1992; Graber, Brooks-Gunn, & Warren 1995); marital conflict (Wierson, Long, & Forehand, 1993; Kim, & Smith, 1998, 1999); and negative family relationships (Kim, Smith, & Palermiti, 1997; Ellis & Garber, 2000). Despite some exceptions (Campbell & Udry, 1995; Graber, et al., 1995), the majority of studies show that childhood psychosocial stress is associated with earlier menarche. As mentioned, investigators examine a multitude of variables under the rubric of stress. We consider stress to be the general response to stressors found in all vertebrate species (Sapolsky, Romero & Munck, 2000), namely the activation of the hypothalamic-pituitaryadrenal (HPA) axis. While stress is difficult to define (McEwen, 1995), and may result from physical abuse (Hart, Gunnar, & Cicchetti, 1996), insecure childhood attachment (Hertsgaard, Gunnar, Erickson, & Nachmias, 1995), low socio-economic status (Lupien, King, Meaney & McEwen, 2000), family composition (Flinn, 1999), and more, the final common pathway involves activation of the HPA system. Therefore, when we refer to psychosocial stress we are referring to the final common pathway - activation of the HPA axis. It is important, however, to distinguish between psychosocial stress and nutritional or disease stress. The association between poverty, malnutrition and delayed menarche is well-known (Tanner, 1962, 1968; Dreizen, Spirakis, & Stone, 1967; Marshall & Tanner, 1986). And it makes good evolutionary sense to grow slowly and delay maturation during lean times and to accelerate development when resources are available (Ellison, 1990; Worthman, 1999a). In this case earlier reproduction translates into greater fitness because offspring will also begin to reproduce at a younger age, taking full advantage of resource availability (Cole, 1954). How then, can it make evolutionary sense to mature early and reproduce early in risky and uncertain environments? The answer, as we have seen, is that in such environments (experienced subjectively as psychosocial stress) early reproduction minimises the chances of lineage extinction. The question then becomes, how are these developmental pathways differentially entrained? The evidence suggests a response hierarchy. Women who lack the energy and nutrients to support pregnancy and lactation don’t reproduce—early or late. However, women with at least adequate energy and nutrients—who also face sufficient social risk and uncertainty—do seem to reproduce early. The metabolic demands of survival and pregnancy and lactation thus take precedence over psychosocial influences on age at menarche. The adaptation in this case is the evolved capacity to develop the most locally appropriate reproductive strategy.

ARTICLE IN PRESS D.A. Coall, J.S. Chisholm / Social Science & Medicine 57 (2003) 1771–1781

The current—future trade-off and low birth weight Because the alternative is lineage extinction, when conditions are sufficiently risky and uncertain it can be evolutionarily rational to pay extreme reproductive costs. The costs of maximising current reproduction can be intergenerational (borne by offspring) as well as intragenerational (borne by parents) (Borgerhoff Mulder, 1992; Chisholm, 1999; Harpending, Draper, & Pennington, 1990; Stearns, 1992). Accordingly, women who are following a strategy for maximising current reproduction—evidenced by high levels of early psychosocial stress and early menarche—might be expected to have LBW children. And there is evidence that they do. In a sample of 1516 pregnant women aged 17–19, Scholl et al. (1989) found that early menarche was associated with LBW through IUGR (not short gestation), even after controlling for parity, fetal sex, maternal ethnic group, smoking, prepregnancy BMI and gynaecological age (period between mother’s age at menarche and at childbirth). Additional studies, with wider maternal age ranges and larger more diverse samples report similar results (Petridou, Trichopoulos, Revinthi, Tong, & Papathoma, 1996; Kirchengast & Hartmann, 2000). On the other hand, two studies have found the opposite (Strobino, Ensminger, Kim, & Nanda, 1995; Hennessy, & Alberman, 1998). Interestingly, several studies of the association between age at menarche and birth weight have been conducted in developing countries (DaVanzo, Habicht & Butz, 1984; Xu, Jarvelin, Lu, Xu, & Rimpela, 1995; Xu, Jarvelin, Xu, Wang, Qin and Rimpela, 1997), but none support the evolutionary perspective presented here. How to account for these seemingly disparate findings regarding mothers’ age at menarche and children’s birth weight? We believe that our earlier distinction between biological and psychosocial stressors may be relevant. The non-Western studies support the premise that early menarche reflects good childhood nutrition and that early maturers have heavier babies simply because they are healthier. This is most salient in the Xu et al. (1997) study, where only thin mothers exhibited an effect of menarche on birth weight. As these mothers gave birth in 1992, were mostly in their twenties and had an approximate mean age at menarche of 14 years,3 they would have reached menarche in the early 1980s (deduced from a mean menarche-first birth interval of about 10 years [see Morabia, Constanza & the WHO Collaborative Study of Neoplasia and Steroid Contraceptives, 1998]). As the secular decrease in age at menarche is accepted as having continued in China at least until 1979 (Low, Kung, & Leong, 1982), poor early nutrition and/or disease may well have played a role in 3 Other Chinese studies around the same time report a similar age at menarche (e.g., Lin et al., 1992).

1775

the association between late menarche and LBW in this population. Not until resources for gestation and lactation are available would the proposed relationship between early psychosocial stress and thus early menarche and LBW be evident. While scarcely conclusive, the balance of evidence supports Scholl et al.’s finding of a link between early menarche and LBW. This is consistent with our evolutionary model: women who experience early menarche as a consequence of early environmental risk and uncertainty are more likely to have LBW babies.

Parent–offspring conflict theory and placental/fetal weight ratio Our synthesis of life history theory and parental investment theory predicts that women who experience higher levels of early psychosocial stress are more likely to mature at a younger age and have lower birth weight babies. This is an intergenerational trade-off in that the child is paying part of the cost of her mother’s early reproduction. However, because mother and fetus are not genetically identical and thus do not have the same inclusive fitness interests (Hamilton, 1964), parent– offspring conflict theory (Trivers, 1972, 1974) provides the rationale for the prediction that mothers and fetuses will tend to ‘‘disagree’’ about the optimal trade-off between offspring quantity and quality. Haig (1993, 1996, 1999) has developed a sophisticated application of parent–offspring conflict theory for modelling maternalfetal interaction (see Fig. 2). Because resources are always limited, any maternal investment in a fetus entails a trade-off - i.e., for every benefit (B in Fig. 2) a fetus gains from maternal resources there will be a correlated cost (C in Fig. 2) to its existing or future siblings. Because the mother is equally related to all her offspring, current and future, it is evolutionarily rational

Fig. 2. Representation of the trade-off between maternal investment in current fetus vs. siblings [reproduced from Haig (1996) with permission r 1996 Munksgaard International Publishers Ltd. Copenhagen, Denmark]

ARTICLE IN PRESS 1776

D.A. Coall, J.S. Chisholm / Social Science & Medicine 57 (2003) 1771–1781

for her to invest equally in each according to their capacity to benefit from the resources invested. Therefore, the mother is expected to seek the best possible balance between the benefit to the existing fetus and the cost to its existing or future siblings. In other words, after a point (X1 in Fig. 2) the increased benefit to the current fetus of her continuing the same high rate of investment will be outweighed by detracting from the resources she could invest in existing or future offspring. At that point the mother is expected to begin diverting resources from the fetus to existing or future children. From the fetus’ perspective, however, things look different. While its mother has a 50% genetic interest in all her children, the fetus has a 100% genetic interest in itself, but only a 50% genetic interest in existing and future siblings (even less if by a different father). It is therefore evolutionarily rational for the fetus to maximise the amount of resources it receives from mother (Xo in Fig. 2), even to elicit more resources from the mother than she is prepared to provide. Most often this parent–offspring conflict results in a compromise where neither party achieves its optimal target. The theory of parent–offspring conflict suggests that if the mother attempted to restrict her flow of resources to the fetus the fetus would attempt to resist. One mechanism by which the fetus might resist is via ‘‘a facultative response to relative starvation by increasing its absolute allocation to placental growth’’ (Haig, 1993, p. 500). Growing a larger placenta increases the ratio of the weight of the placenta to that of the fetus (the placental-fetal weight [P/FW] ratio). This prediction makes physiological sense as placental weight is associated with placental function (Robinson, Seamark, & Owens, 1994) and there is an association between accelerated placental growth and increased capillary volume late in IUGR pregnancies (Kingdom, Huppertz, Seaward, & Kaufmann, 2000). The implications of parent–offspring conflict theory for P/FW ratio are even greater when it is recognised that increased P/FW ratio is associated with higher blood pressure throughout childhood (Moore et al., 1996) and into adulthood (Moore, Cockington, Ryan, & Robinson, 1999) and may predispose individuals to hypertension, glucose intolerance, blood coagulation disorders and coronary heart disease as adults (Barker, Bull, Osmond, & Simmonds, 1990; Law, Barker, Bull, & Osmond, 1991; Barker 1994, 1997; see Godfrey, 2002 for review).4 This ‘‘fetal origins of adult disease’’ perspective 4

The evidence regarding placental weight and adult disease is not conclusive and some studies have found no significant associations (Matthews, Lewis, & Bethel, 1994; Leon et al., 1996). It may be that a relatively larger placenta is not on the causal pathway to adult disease, rather it may be an indicator of other factors taking effect throughout gestation ((Robinson et al., 1995).

holds that maternal under-nutrition during pregnancy leads to placental enlargement. In a natural experiment Lumey (1998) reported that women conceiving or in the first trimester of pregnancy during the Dutch famine winter of 1944–45 had babies with relatively heavy placentas, while birth weights remained static. Lumey interpreted this as compensatory placental growth in response to reduced maternal nutrition. Both animal (Robinson, Owens, de Barro, Lok, & Chidzanga, 1994) and human models (Wheeler et al., 1994) support this interpretation. We believe that our evolutionary model of LBW shows that the current emphasis of the ‘‘fetal origins of adult disease’’ perspective on maternal nutrition as an antecedent of adult disease may not be necessary. While the impact of maternal nutrition on fetal and placental growth is clearly complicated (Robinson, et al. 1994), investigations of nutrient intake and subsequent fetal and placental weights at birth have provided mixed results (Godfrey, Robinson, Barker, Osmond, & Cox, 1996; Mathews, Yudkin, & Neil, 1999). Our model suggests that the effect of maternal nutrition on P/FW ratio is not only a consequence of maternal nutrient intake, but that the flow of resources from the uterus to the fetus is ‘‘negotiated’’ by mother and fetus. This may explain some of the inconsistencies in the studies of fetal antecedents of adult disease (see Kramer & Joseph, 1996; Kramer, 2000). While our emphasis so far has been on proximate biological mechanisms, psychosocial factors can also affect P/FW ratio. In a prospective cohort study in Australia, for example, Williams, Evans and Newnham (1997) found that lower socio-economic status was associated with a higher P/FW ratio. To reiterate, we predict that women who experience high levels of early psychosocial stress and earlier menarche are more likely to have LBW babies with relatively large placentas. While menarcheal age seems never to have been studied in this context, we believe that our model clearly establishes its potential health significance. One reason why age at menarche has not been studied in this context, we suspect, may be some misconceptions of the causes, correlates and consequences of early menarche. To foster research in this new context, we address two potential misconceptions.

Mother’s age at menarche and child’s birth weight: a missing link? As mentioned, the secular decrease in age at menarche is usually explained in terms of improved health and nutrition. On this view women with early menarche must be healthier and more likely to have heavier babies; the possibility that early menarche might be associated with low birth weight would thus not be an obvious one. The most common context in which mothers’ age at

ARTICLE IN PRESS D.A. Coall, J.S. Chisholm / Social Science & Medicine 57 (2003) 1771–1781

menarche has been linked to their children’s birth weight is when it is used as a measure of maternal childhood nutrition (e.g., DaVanzo, et al., 1984; Xu, et al., 1997). But if early menarche is due to improved health and nutrition and healthy, well-nourished women have heavier babies, why has not there been any hint of a secular increase in birth weight to accompany the secular decrease in age at menarche? While age at menarche has decreased fairly steadily for 150 years, birth weights have not increased. For example, European birth weights similar to today’s were reported in the mid1700s (Robinson, Moore, Owens, & McMillen, 2000). And Cole argues in his recent review of secular trends in growth that ‘‘Birth weight has fallen, remained static or risen at times unrelated to the timing of height and menarche trends’’ (Cole, 2000, p. 320). In sum, the relation between mothers’ age at menarche and children’s birth weight is more complex than the goodnutrition explanation of the secular decrease in age at menarche might lead one to expect. Additionally, the potential effect of age at menarche on birth weight may often have been hidden in the wellknown correlation between maternal age and birth weight. Given the resources devoted to understanding the antecedents and consequences of both age at menarche (‘‘perhaps the most studied pubertal event’’ [(Graber, et al., 1995, p. 347]) and birth weight (see Kramer, 1987), it is surprising that so few studies have explored the association between these two critical variables. Scholl et al. (1989) suggest that the effect of mothers’ age at menarche on birth weight may be lost in its common covariation with maternal age and birth weight. Women with early menarche tend to be younger at first intercourse (Udry, 1979; Andersson-Ellstrom, Forssman, & Milsom, 1996), first pregnancy and birth of first child (Ryder & Westoff, 1971; Udry & Cliquet, 1982; Roosa, Tein, Reinholtz, & Angelini, 1997). And although maternal age per se is not an important independent determinant of birth weight, young mothers are at increased risk for delivering LBW babies (Kramer, 1987). In sum, the effect of early menarche on birth weight may be overlooked because it is subsumed in young maternal age effects. Our evolutionary model of LBW is based on a synthesis of life history theory, parental investment theory and parent–offspring conflict theory. It suggests that women who develop in environments high in risk and uncertainty, and experience high levels of psychosocial stress as a result, are more likely to have early menarche and LBW babies. It highlights the need to examine factors that contribute to environmental risk and uncertainty (e.g., family environment, SES, stressful life events) in relation to the antecedents of age at menarche and LBW. This perspective also provides a framework for generating novel and testable hypotheses for future research. Emphasising the intergenerational

1777

influences of early psychosocial stress and age at menarche on LBW, our model may also lead to novel intervention and prevention strategies. We believe that when evolutionary theory is directed to public health concerns more of its full value will become apparent.

Acknowledgements The preparation of this paper was supported in part by a grant from the Australian Research Council. Earlier versions of this paper were presented at the annual meeting of the Human Behavior and Evolution Society at University College London, June 2001 and the Institute of Advanced Studies at The University of Western Australia workshop, Advances in Evolutionary Ecology, July 2001.

References Acheson, D. (1998). Independent inquiry into inequalities in health. London: Stationary Office. Andersson-Ellstrom, A., Forssman, L., & Milsom, I. (1996). Age of sexual debut related to life-style and reproductive health factors in a group of Swedish teenage girls. Acta Obstetricia et Gynecologica Scandinavia, 75(5), 484–489. Adair, L. S. (2001). Size at birth predicts age at menarche. Pediatrics, 107(4), e59–e65. Barker, D. J. P. (1994). Mothers, babies, and disease in later life. London: BMJ Publishing Group. Barker, D. J. P. (1997). The fetal origins of coronary heart disease. Acta Paediatrica Supplement, 422, 78–82. Barker, D. J. P. (1999). Fetal origins of cardiovascular disease. Annals of Medicine, 31(Suppl. 1), 3–6. Barker, D. J. P., Bull, A. R., Osmond, C., & Simmonds, S. J. (1990). Fetal and placental size and risk of hypertension in adult life. British Medical Journal, 301, 259–262. Belsky, J. (1996). Parent, infant, and social-contextual determinants of attachment security. Developmental Psychology, 32, 905–914. Belsky, J., Steinberg, L., & Draper, P. (1991). Childhood experience, interpersonal development, and reproductive strategy: An evolutionary theory of socialization. Child Development, 62, 647–670. Borgerhoff Mulder, M. (1992). Reproductive decisions. In E. A. Smith, & B. Winterhalder (Eds.), Evolutionary ecology and human behaviour (pp. 339–373). New York: Walter de Gruyter. Bowlby, J. (1969). Attachment and loss. Vol. 1: Attachment. New York: Basic Books. Campbell, B. C., & Udry, J. R. (1995). Stress and age at menarche of mothers and daughters. Journal of Biosocial Science, 27, 127–134. Charnov, E. L. (1993). Life history invariants: some explorations of symmetry in evolutionary ecology. Oxford: Oxford University Press.

ARTICLE IN PRESS 1778

D.A. Coall, J.S. Chisholm / Social Science & Medicine 57 (2003) 1771–1781

Chisholm, J. S. (1993). Death, hope, and sex: Life-history theory and the development of reproductive strategies. Current Anthropology, 34, 1–24. Chisholm, J. S. (1995). Life history theory and lifestyle choice: Implications for Darwinian medicine. In L. Schmitt, & L. Freedman (Eds.), Perspectives in human biology. Nedlands: Centre for Human Biology, University of Western Australia, and River Edge, New Jersey: World Scientific Publishing. Chisholm, J. S. (1996). The evolutionary ecology of attachment organisation. Human Nature, 7(1), 1–38. Chisholm, J. S. (1999). Death, hope, and sex. Cambridge: Cambridge University Press. Chisholm, J. S., & Burbank, V. K. (2001). Evolution and inequality. International Journal of Epidemiology, 30, 206–211. Coall, D. A., & Chisholm, J. S. (1999). Childhood psychosocial stress accelerates age at menarche: A Test of Belsky, Steinberg and Draper’s model. Paper presented at the 11th Annual Meeting of the Human Behavior and Evolution Society. Salt Lake City, Utah, June. Cole, L. (1954). The population consequences of life history phenomena. Quarterly Review of Biology, 29, 103–137. Cole, T. J. (2000). Secular trends in growth. Proceedings of the Nutrition Society, 59, 317–324. Daan, S., & Tinbergen, J. M. (1997). Adaptation of life histories. In J. R. Krebs, & N. B. Davies (Eds.), Behavioural ecology: An evolutionary approach (pp. 311–333). Oxford: Blackwell Science Ltd. DaVanzo, J., Habicht, J-P., & Butz, W. P. (1984). Assessing socioeconomic correlates of birthweight in peninsular Malaysia: Ethnic differences and changes over time. Social Science & Medicine, 18(5), 387–404. Davey-Smith, G., Ebrahim, S., & Frankel, S. (2001). How policy informs the evidence: ‘‘evidence based’’ thinking can lead to debased policy making. British Medical Journal, 322, 184–185. Davey-Smith, G., Neaton, J. D., Wentworth, D., Stamler, R., & Stamler, J. (1996). Socioeconomic differentials in mortality risk among men screened for the Multiple Risk Factor Intervention Trial: I. White men. American Journal of Public Health, 86(4), 486–496. Davey-Smith, G., Wentworth, D., Neaton, J. D., Stamler, R., & Stamler, J. (1996). Socioeconomic differentials in mortality risk among men screened for the Multiple Risk Factor Intervention Trial: II. Black men. American Journal of Public Health, 86(4), 497–504. Dreizen, S., Spirakis, C. N., & Stone, R. E. (1967). A comparison of skeletal growth and maturation in undernourished and well-nourished girls before and after menrache. Journal of Pediatrics, 70(2), 256–263. Ellis, B. J., & Garber, J. (2000). Psychosocial antecedents of variation in girls’ pubertal timing: Maternal depression, stepfather presence, and marital and family stress. Child Development, 71(2), 485–501. Ellis, B. J., McFadyen-Ketchum, S., Dodge, K. A., Pettit, G. S., & Bates, J. E. (1999). Quality of early family relationships and individual differences in the timing of pubertal maturation in girls: A longitudinal test of an evolutionary model. Journal of Personality and Social Psychology, 77(2), 387–401.

Ellison, P. T. (1990). Human ovarian function and reproductive ecology: New hypotheses. American Anthropologist, 92, 933–952. Flinn, M. V. (1999). Family environment, stress, and health during childhood. In C. Panter-Brick, & C. M. Worthman (Eds.), Hormones, health, and behavior: A socio-ecological and lifespan perspective (pp. 105–138). Cambridge: Cambridge University Press. Fonagy, P. (1996). The significance of the development of metacognitive control over mental representations in parenting and infant development. Journal of Clinical Psychoanalysis, 5(1), 67–86. Fonagy, P., & Higgitt, A. (2000). Early influences on development and social inequalities: an attachment theory perspective. In A. R. Tarlov, & R. F. St. Peter (Eds.), The society and population health reader: Volume II A state and community perspective (pp. 104–130). New York: The New Press. Frisch, R. E. (1988). Fatness and fertility. Scientific American, 258, 88–95. Garn, S. M., LaVelle, M., Rosenberg, K. R., & Hawthorne, V. M. (1986). Maturational timing as a factor in female fatness and obesity. American Journal of Clinical Nutrition, 43, 879–883. Godfrey, K. M. (2002). The role of the placenta in fetal programming—A review. Placenta, 23(Suppl. A, Trophoblast Research 16), S20–S27. Godfrey, K., Robinson, S., Barker, D. J. P., Osmond, C., & Cox, V. (1996). Maternal nutrition in early and late pregnancy in relation to placental and fetal growth. British Medical Journal, 312, 410–414. Graber, J. A., Brooks-Gunn, J., & Warren, M. P. (1995). The antecedents of menarcheal age: Heredity, family environment, and stressful life events. Child Development, 66, 346–359. Haig, D. (1993). Genetic conflicts in human pregnancy. The Quarterly Review of Biology, 68, 495–532. Haig, D. (1996). Altercation of generations: Genetic conflicts of pregnancy. American Journal of Reproductive Immunology, 35, 226–232. Haig, D. (1999). Genetic conflicts of pregnancy and childhood. In S. Stearns (Ed.), Evolution in health and disease (pp. 77–90). Oxford: Oxford University Press. Hamilton, W. D. (1964). The genetic evolution of social behaviour. I. Journal of Theoretical Biology, 7, 1–16. Harpending, H., Draper, P., & Pennington, R. (1990). Culture, evolution, parental care, and mortality. In A. Swedland, & G. Armelagos (Eds.), Disease in populations in transition. South Hadley, MA: Bergin and Garvey. Hart, J., Gunnar, M., & Cicchetti, D. (1996). Altered neuroendocrine activity in maltreated children related to symptoms of depression. Development & Psychopathology, 8(1), 201–214. Hennessy, E., & Alberman, E. (1998). Intergenerational influences affecting birth outcome. I. Birthweight for gestational age in the children of the 1958 British Birth Cohort. Paediatric and Perinatal Epidemiology, 12(Suppl. 1), 45–60. Henriksen, T. (1999). Foetal nutrition, foetal growth restriction and health later in life. Acta Paediatrica Supplement, 429, 4–8.

ARTICLE IN PRESS D.A. Coall, J.S. Chisholm / Social Science & Medicine 57 (2003) 1771–1781 Herman-Giddens, M., Sandler, A., & Friedman, N. (1988). Sexual precocity in girls: An association with sexual abuse? American Journal of Diseases of Children, 142, 431–433. Hertsgaard, L., Gunnar, M., Erickson, M. F., & Nachmias, M. (1995). Adrenocortical responses to the Strange Situation in infants with disorganised/disoriented attachment relationships. Child Development, 66(4), 1100–1106. Hertzman, C. (2000). The case for an early childhood development strategy. Isuma: Canadian Journal of Policy Research, 1(2), 11–18. Hill, K. (1993). Life history theory and evolutionary anthropology. Evolutionary Anthropology, 2(3), 78–88. Hill, K., & Kaplan, H. (1999). Life history traits in humans: Theory and empirical studies. Annual Review of Anthropology, 28, 397–430. Kim, K., & Smith, P. K. (1998). Retrospective survey of parental marital relations and child reproductive development. International Journal of Behavioral Development, 22(4), 729–751. Kim, K., & Smith, P. K. (1999). Family relations in early childhood and reproductive development. Journal of Reproductive and Infant Psychology, 17(2), 133–148. Kim, K., Smith, P. K., & Palermiti, A-L. (1997). Conflict in childhood and reproductive development. Evolution and Human Behaviour, 18, 109–142. Kingdom, J., Huppertz, B., Seaward, G., & Kaufmann, P. (2000). Development of the placental villous tree and its consequences for fetal growth. European Journal of Obstetrics and Gynecology and Reproductive Biology, 92, 35–43. Kirchengast, S., & Hartmann, B. (2000). Association between maternal age at menarche and newborn size. Social Biology, 47(1-2), 114–126. Kogan, M. (1995). Social causes of low birth weight. Journal of the Royal Society of Medicine, 88(11), 611–615. Kramer, M. S. (1987). Determinants of low birth weight: Methodological assessment and meta-analysis. Bulletin of the World Health Organisation, 65(5), 663–737. Kramer, M. S. (2000). Invited commentary: Association between restricted fetal growth and adult chronic disease: Is it causal? Is it important? American Journal of Epidemiology, 152(7), 606–608. Kramer, M. S., & Joseph, K. S. (1996). Enigma of fetal/infantorigins hypothesis. Lancet, 348(9037), 1254–1255. Laitinen, J. C., Power, C., & Jarvelin, M. R. (2001). Family social class, maternal body mass index, childhood body mass index, and age at menarche as predictors of adult obesity. American Journal of Clinical Nutrition, 74(3), 287–294. Law, C. M., Barker, D. J. P., Bull, A. R., & Osmond, C. (1991). Maternal and fetal influences on blood pressure. Archives of Disease in Childhood, 66, 1291–1295. Leon, D. A., Koupilova, I., Lithell, H. O., Berglund, L., Mohsen, R., Vagero, D., Lithell, U. B., & McKeigue, P. M. (1996). Failure to realise growth potential in utero and adult obesity in relation to blood pressure in 50 year old Swedish men. British Medical Journal, 312(7028), 401–406. Lin, W-S., Chen, A. C. N., Su, J. Z. X., Zhu, F-C., Xing, W-H., Li, J-Y., & Ye, G-S. (1992). The menarcheal age of Chinese girls. Annals of Human Biology, 19(5), 503–512.

1779

Low, B. S. (1978). Environmental uncertainity and the parental strategies of marsupials and placentals. The American Naturalist, 112(983), 197–213. Low, W. D., Kung, L. S., & Leong, J. C. Y. (1982). Secular trend in the sexual maturation of Chinese girls. Human Biology, 54(3), 539–551. Lumey, L. H. (1998). Compensatory placental growth after restricted maternal nutrition in early pregnancy. Placenta, 19, 105–111. Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2000). Child’s stress hormone levels correlate with mother’s socioeconomic status and depressive state. Biological Psychiatry, 48, 976–980. Marris, P. (1996). The politics of uncertainty: attachment in private and public life. London: Routledge. McCormick, M. C. (1985). The contribution of low birth weight to infant mortality and childhood morbidity. New England Journal of Medicine, 312, 82–90. McEwen, B.S. (1995). Stressful experience, brain, and emotions: Developmental, genetic, and hormonal influences. In: M.S. Gazzangia (Ed), The cognitive neurosciences. Cambridge: MIT Press. McEwen, B.S., & Seeman, T. (1999). Protective and damaging effects of mediators of stress. In N.E. Adler, M. Marmot, B.S. McEwen & J. Stewart (Eds), Socioeconomic status and health in industrialized nations. New York: New York Academy of Science. McLoyd, V. C. (1990). The impact of economic hardship on black families and children: Psychological distress, parenting, and socio-emotional development. Child Development, 61, 311–346. Marshall, W., & Tanner, J. (1986). Puberty. In F. Falkner & J.M. Tanner (Eds), Human growth: A comprehensive treatise. New York: Plenum Press. Mathews, F., Yudkin, P., & Neil, A. (1999). Influence of maternal nutrition on outcome of pregnancy: Prospective cohort study. British Medical Journal, 319, 339–343. Matthews, J. W. A., Lewis, P. A., & Bethel, J. A. (1994). Relation between birth weight at term and systolic blood pressure in adolescence. British Medical Journal, 308, 1074–1077. Merzenich, H., Boeing, H., & Wahrendorf, J. (1993). Dietry fat and sports activity as determinants for age at menarche. American Journal of Epidemiology, 138(4), 217–224. Moffit, T. E., Caspi, A., Belsky, J., & Silva, P. A. (1992). Childhood experience and the onset of menarche: A test of a sociobiological model. Child Development, 63, 47–58. Moore, V. M., Miller, A. G., Boulton, T. J., Cockington, R. A., Craig, I. H., Magarey, A. M., & Robinson, J. S. (1996). Placental weight, birth measurements, and blood pressure at age 8 years. Archives of Disease in Childhood, 74(6), 538–541. Moore, V. M., Cockington, R. A., Ryan, P., & Robinson, J. S. (1999). The relationship between birth weight and blood pressure amplifies from childhood to adulthood. Journal of Hypertension, 17(7), 883–888. Morabia, A., Constanza, M.C., & the World Health Organisation Collaborative Study of Neoplasia and Steroid Contraceptives. (1998). International variability in ages at menarche, first livebirth, and menopause. American Journal of Epidemiology, 148 (12), 1195–1205.

ARTICLE IN PRESS 1780

D.A. Coall, J.S. Chisholm / Social Science & Medicine 57 (2003) 1771–1781

Persson, I., Ahlsson, F., Ewald, U., Tuvemo, T., Qingyuan, M., von Rosen, D., & Proos, L. (1999). Influence of perinatal factors on the onset of puberty in boys and girls: Implications for interpretation of link with risk of long term diseases. American Journal of Epidemiology, 150(7), 747–755. Petridou, E., Trichopoulos, D., Revinthi, K., Tong, D., & Papathoma, E. (1996). Modulation of birthweight through gestational age and fetal growth. Child: Care, Health and Development, 22(1), 37–53. Phillips, D. I. (1998). Birth weight and the future development of diabetes: A review of the evidence. Diabetes, Care, 21(Suppl 2), B150–B155. Promislow, D., & Harvey, P. H. (1990). Living fast and dying young: A comparative analysis of life-history variation in mammals. Journal of the Zoological Society of London, 220, 437–471. Promislow, D., & Harvey, P. H. (1991). Mortality rates and the evolution of mammal life histories. Acta Oecologica, 12(1), 119–137. Repetti, R. L., Taylor, S. E., & Seeman, T. E. (2002). Risky families: Social environments and the mental and physical health of offspring. Psychological Bulletin, 128(2), 330–366. Robinson, J., Chidzanja, S., Kind, K., Lok, F., Owens, P., & Owens, J. (1995). Placental control of fetal growth. Reproduction, Fertility and Development, 7, 333–344. Robinson, J. S., Moore, V. M., Owens, J. A., & McMillen, I. C. (2000). Origins of fetal growth restriction. European Journal of Obstetrics and Gynecology and Reproductive Biology, 92, 13–19. Robinson, J.S., Owens, J.A., de Barro, T., Lok, F., & Chidzanga, S. (1994). Maternal nutrition and fetal growth. In R.H.T. Ward, S.K. Smith & D. Donnai (Eds), Early fetal growth and development. London: RCOG Press. Robinson, J. S., Seamark, R. F., & Owens, J. A. (1994). Placental function. Australian and New Zealand Journal of Obstetrics and Gynaecology, 34(3), 240–246. Roosa, M. W., Tein, J., Reinholtz, C., & Angelini, P. J. (1997). The relationship of childhood sexual abuse to teenage pregnancy. Journal of Marriage and the Family, 59, 119–130. Ryder, N. B., & Westoff, C. F. (1971). Reproduction in the United States 1965. New Jersey: Princeton University Press. Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21(1), 55–89. Schaffer, W. M. (1983). The application of optimal control theory to the general life history problem. The American Naturalist, 121, 418–431. Scholl, T. O., Hediger, M. L., Vasilenko III, P., Ances, I. G., Smith, W., & Salmon, R. W. (1989). Effects of early maturation on fetal growth. Annals of Human Biology, 16(4), 335–345. Sen, A. (1992). Inequality reexamined. New York: Harvard University Press. Sen, A. (1999). Development as freedom. New York: Knopf. Sherman, B., Wallace, R., Bean, J., & Schlabaugh, I. (1981). Relationship of body weight to menarcheal and menopausal age: Implications for breast cancer risk. Journal of Clinical Endocrinology and Metabolism, 52, 488–493.

Stearns, S. C. (1992). The evolution of life histories. Oxford: Oxford University Press. Strobino, D. M., Ensminger, M. E., Kim, Y. J., & Nanda, J. (1995). Mechanisms for maternal age differences in birth weight. American Journal of Epidemiology, 142(5), 504–514. Surbey, M. K. (1990). Family composition, stress, and the timing of puberty. In T. E. Ziegler, & F. B. Bercovitch (Eds.), Socioendocrinology of primate reproduction (pp. 11–32). New York: Wiley-Liss. Tanner, J. M. (1962). Growth at adolescence: with a general consideration of the effects of hereditary and environmental factors upon growth and maturation from birth to maturity (2nd ed.). Oxford: Blackwell Scientific Publications. Tanner, J. M. (1968). Earlier maturation in man. Scientific American, 218(1), 21–27. Trivers, R. L. (1972). Parental investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man (pp. 52–97). Chicago: Aldine. Trivers, R. L. (1974). Parent–offspring conflict. American Zoologist, 14, 249–264. Udry, J. R. (1979). Age at menarche, at first intercourse, and at first pregnancy. Journal of Biosocial Science, 11, 433–441. Udry, J. R., & Cliquet, R. L. (1982). A cross-cultural examination of the relationship between ages at menarche, marriage, and first birth. Demography, 19(1), 53–63. Wahlbeck, K., Forsen, T., Osmond, C., Barker, D. J. P., & Eriksson, J. G. (2001). Association of schizophrenia with low maternal body mass index, small size at birth, and thinness during childhood. Archives of General Psychiatry, 58, 48–52. Wellens, R., Malina, R. M., Roche, A. F., Chumlea, W. C., Guo, S., & Siervogel, R. M. (1992). Body size and fatness in young adults in relation to age at menarche. American Journal of Human Biology, 4, 783–787. Wheeler, T., Sollero, C., Alderman, S., Landen, J., Anthony, F., & Osmond, C. (1994). Relation between maternal haemoglobin and placental hormone concentrations in early pregnancy. Lancet, 343, 511–513. Wierson, M., Long, P. J., & Forehand, R. L. (1993). Toward a new understanding of early menarche: The role of environmental stress in pubertal timing. Adolescence, 28(112), 913–924. Wilkinson, R. G. (1994). Unhealthy societies: The afflictions of inequality. London: Routledge. Wilkinson, R. G. (1997). Health inequalities: Relative or absolute material standards? British Medical Journal, 314, 591–595. Williams, L. A., Evans, S. F., & Newnham, P. J. (1997). Prospective cohort study of factors influencing the relative weights of the placenta and the newborn infant. British Medical Journal, 314, 1864–1868. Worthman, C. (1999a). Evolutionary perspectives on the onset of puberty. In W. Trevathan, E. Smith, & J. McKenna (Eds.), Evolutionary medicine (pp. 135–163). Oxford: Oxford University Press. Worthman, C. (1999b). The epidemiology of development. In C. Panter-Brick, & C. Worthman (Eds.), Hormones, health and behavior (pp. 47–104). Cambridge: Cambridge University Press.

ARTICLE IN PRESS D.A. Coall, J.S. Chisholm / Social Science & Medicine 57 (2003) 1771–1781 Xu, B., Jarvelin, M-R., Lu, H., Xu, X., & Rimpela, A. (1995). Maternal determinants of birth weight: A population-based sample from Qingdao, China. Social Biology, 42(3-4), 175–184. Xu, B., Jarvelin, M. R., Xu, X., Wang, Z., Qin, H., & Rimpela, A. (1997). Maternal menstrual history and small-forgestational-age births in a population-based Chinese birth cohort. Early Human Development, 49(3), 183–192.

David A. Coall is a Ph.D. student in the School of Anatomy and Human Biology at The University of Western Australia. His main research interest is the application of evolutionary theory within an epidemio-

1781

logical framework specifically focusing on the antecedents of low birth weight. James S Chisholm is Professor in The School of Anatomy and Human Biology at The University of Western Australia. He is a biological anthropologist whose interests lie in the fields of human behavioural biology, evolutionary ecology and life history theory, where he focuses on infant social-emotional development, the development of reproductive strategies and the integration of evolutionary and cultural psychology. His latest book, Death, Hope, and Sex was published by Cambridge University Press (1999).