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Offspring: Human Fertility Behavior in Biodemographic Perspective 7 An Evolutionary and Ecological Analysis of Human Fertility, Mating Patterns, and Parental Investment Hillard S. Kaplan and Jane B. Lancaster This chapter considers the evolutionary biology of human fertility, parental investment, and mating and is designed to provide a broad overview of the topic. It focuses on three themes. The first is the timing of life events, including development, reproduction, and aging. Second is the regulation of reproductive rates and its relationship to parental investment. Sexual dimorphism and its relationship to mating systems together are the third theme. Each of these themes is addressed from two perspectives: first, in a comparative cross-species context, and second, in terms of variation within and among human groups. Our primary goal is to introduce a new ecological framework for understanding variations in each of those domains and then to apply the framework to understanding both the special characteristics of our species in a comparative perspective and variations within and among human groups. A secondary goal is to discuss how evolutionary biology can be integrated with more traditional approaches to human demography and the new research questions such integration would generate. The first section of this chapter presents an introduction to life history theory and current thinking in evolutionary biology with respect to the three themes. Since the fitness consequences of alternative fertility and parental investment regimes depend on ecology and individual condition, both specialization and flexibility in life histories are considered. Building on this foundation, an ecological framework for understanding variation in each of those domains is then introduced. The second section discusses humans in a comparative context, with a particular emphasis on the hunter-and gatherer lifestyle because of its relevance to the vast majority of human
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Offspring: Human Fertility Behavior in Biodemographic Perspective evolutionary history. The third section applies the framework developed in the first two parts to understanding major historical trends in human fertility, parental investment, and mating regimes. The transition from hunting and gathering to farming and pastoralism is considered first. Land- and power-based stratified societies are then discussed, followed by an analysis of wage-based competitive labor markets and demographic transition. The chapter concludes with a discussion of the new research questions and approaches to research design suggested by this framework. THE THEORETICAL FRAMEWORK Fundamental Trade-Offs in Life History Theory Natural selection acts on variability in the traits of individual organisms within populations. Traits (and the genes that code for them) increase in frequency relative to other traits when their average effects on the individuals possessing those traits act to maximize their long-term production of descendents through time.1 Fertility is the most direct contributor to an organism’s fitness (i.e., the number of descendents it produces). In fact, all other fitness components, such as mortality, only affect fitness through their effects on fertility (e.g., mortality rates affect fitness by affecting the probability of living to the next reproductive event). All else constant, any increase in fertility increases an organism’s fitness. However, there are two trade-offs affecting natural selection on fertility. The first is the trade-off between present and future reproduction. An organism can increase its energy capture rates in the future by growing and thus increasing its future fertility. For this reason, organisms typically have a juvenile phase in which fertility is zero until they reach a size at which some allocation to reproduction increases fitness more than growth. Similarly, among organisms that engage in repeated bouts of reproduction (humans included), some energy during the reproductive phase is diverted away from reproduction and allocated to maintenance so that it can live to reproduce again. The general expectation is that natural selection on age of first reproduction and on the adult reproductive rate will tend to maximize total allocations of energy to reproduction over the life course. 1 Selection acts on the “inclusive fitness” of genes coding for traits. Inclusive fitness includes effects on both the reproductive success of the individual bearing the gene and other individuals, related by common descent, who also bear the gene. For example, selection on genes affecting alarm calls in response to predators depends both on their effects on the reproductive fitness of the caller (who may risk a greater threat of predation) and on relatives bearing those genes (whose lives may be saved by the call).
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Offspring: Human Fertility Behavior in Biodemographic Perspective The second trade-off is between quantity and quality of offspring, where quality is a function of parental investment in offspring and reflects its ability to survive and reproduce. The general expectation is that natural selection on offspring number and investment per offspring will tend to maximize the long-term production of descendents; this may be estimated by the number of offspring that survive to reproduce themselves during an organism’s lifetime (Smith and Fretwell, 1974) or if fertility affects the production and survival of grandchildren, by more distant effects. Sexual reproduction, which most probably evolved as a means of increasing variability among offspring through the sharing of parents’ genetic material, complicates the trade-off between quantity and quality of offspring. This is because offspring share roughly equal amounts of their parents’ genetic material, yet parents may contribute unequally to their viability. In this sense, offspring may be considered as “public goods,” with each parent profiting from the investments of the other and having an incentive to divert resources to the production of additional offspring. This public goods problem tends to create conflicts of interest between the sexes (see Gangestad, this volume, for a treatment of such conflicts). In fact, an almost universal by-product of sexual reproduction is the divergent evolution of the two sexes. Sex is defined by gamete size, and the sex with the larger gametes is called female. Larger gametes represent greater initial energetic investment in offspring. With increased investment beyond energy in gametes, the divergence between the two sexes is often exaggerated but may also balance or even reverse. For example, females provide all investment to offspring in greater than 95 percent of mammalian species, but males provide similar amounts or more total investments among most altricial birds, male brooding fish, and some insects, such as katydids (see Clutton-Brock and Parker, 1992, for a review). To the extent that one sex invests more in offspring than the other, the one that does more investing sex is in short supply resulting in operational sex ratios greater than unity and competition for mates among members of the sex that does less investing. This public goods problem generates the third major trade-off: that between mating and parental effort. Sexual reproduction involves two components: finding a mate and achieving a mating, on the one hand, and investing in the resulting offspring to increase its viability, on the other. To the extent that there are gains from specialization in the two components, one sex will evolve to produce many small highly mobile gametes specialized to mating, and another will evolve to produce fewer larger gametes, specialized for energetic investments in offspring. Trivers (1972) recognized that these differences in relative parental investment affect the structure of mating markets and the characteristics of the more and less investing sexes. The more investing sex is selected to be choosy about when
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Offspring: Human Fertility Behavior in Biodemographic Perspective and with whom to mate, and the less investing sex is selected to possess characteristics that increase its mating opportunities. This leads to what economists call negative externalities, since male resources are wasted on costly displays or handicaps (Grafen, 1991) or on fighting, rather than in offspring production. The general expectation is that natural selection acts on mating and parenting effort in populations of males and females so that individual fitness tends to maximize in a competitive equilibrium (i.e., it tends to generate distributions of mating and parenting effort among males and females that cannot be “invaded” by alternative distributions). Ecology and Life History Evolution Variations across taxa and across conditions in optimal energy allocations and optimal life histories are shaped by ecological factors, such as food supply, mortality hazards, and the effects of body size on both energy capture and mortality hazards (Charnov, 1993; Kozlowski and Weigert, 1987; Werner, 1986). It is generally recognized that there are species-level specializations that result in bundles of life history characteristics, which, in turn, can be arrayed on a fast-slow continuum (Promislow and Harvey, 1990). For example, among mammals, species on the fast end exhibit short gestation times, early reproduction, small body size, large litters, and high mortality rates, with species on the slow end having opposite characteristics. It is also recognized that many, if not most, organisms are capable of slowing down or speeding up their life histories, depending on environmental conditions such as temperature, rainfall, food availability, density of conspecifics, and mortality hazards. Within-species variation in life history characteristics can operate over several different timescales. For example, there is abundant evidence that allocations to reproduction, as measured by fecundity and fertility, vary over the short term in relationship to food supply and energetic output among plants, birds, and humans (Hurtado and Hill, 1990; Lack, 1968). Extensive research on many bird species has shown that this phenotypic plasticity tracks fitness quite well (Godfray et al., 1991). Birds under variable conditions adjust clutch sizes in ways that tend to maximize the number of surviving young produced during the life course. The impact of the environment may operate over longer time intervals through developmental effects (Lummaa and Clutton-Brock, 2002). For example, calorie restriction of rats at young ages tends to slow down growth rates and leads to short adult stature, even when food becomes abundant later in the juvenile period (Shanley and Kirkwood, 2000). Some intraspecific variation operates at even longer timescales, mediated through differential selection on genetic variants in different habitats. For example, rates of senescence vary across different populations of grass-
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Offspring: Human Fertility Behavior in Biodemographic Perspective hoppers, with those at higher altitudes and earlier winters senescing faster than those at lower altitudes as a result of differential selection on genotypes (Tatar et al., 1997). Similarly, there is a great deal of evidence suggesting that male and female parental investments vary in relation to local ecology over both the short run and the long run (see Clutton-Brock and Parker, 1992 for a review). For example, among katydids, males provide females with a “nuptial gift” (a bolus of condensed food energy) to support offspring production. Experimental manipulation of food density, affecting the foraging time necessary for males to produce the food package, produces shifts in male and female mating effort. When the food supply is low, male inputs into reproduction require more time than female inputs, males are in short supply, and females actively compete for males; as food density increases, this trend is reversed and males compete for access to females (Clutton-Brock, 1991; Gwyne, 1991; Gwyne and Simmons, 1990). This mix of specialization and flexibility is fundamental to understanding human life histories and mating systems. On the one hand, it is generally agreed that the large human brain supports the ability to respond flexibly to environmental variation and to learn culturally. This suggests that humans may be most capable of short-term flexibility in the timing of life events and investment strategies. On the other hand, the commitment to a large brain and the long period of development and exposure to environmental information necessary to make it fully functional place important constraints on the flexibility of the human life course and require specializations for a slow life history. In fact, consideration of brain- and learning-intensive human adaptation reveals shortcomings in existing biological theory and inspires the development of a more general approach to life history evolution, which is the focus next. An Evolutionary Economic Framework A general explanatory framework for understanding our species must be able to account for both its distinctive features when compared to other species and the enormous range of variation exhibited by humans under different conditions, in different societies, and at different points in time. To account for these evolutionary trends, we have expanded existing models of life history evolution by explicitly modeling the three trade-offs discussed above using capital investment theory (Becker, 1975; Kaplan, 1996; Kaplan and Robson, 2002; Robson and Kaplan, 2003). The processes of growth, development, and maintenance are treated as investments in stocks of somatic or embodied capital. In a physical sense, embodied capital is organized somatic tissue—muscles, digestive organs, brains, and so forth. In
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Offspring: Human Fertility Behavior in Biodemographic Perspective a functional sense, embodied capital includes strength, speed, immune function, skill, knowledge, and other abilities. Since such stocks tend to depreciate with time, allocations to maintenance can also be seen as investments in embodied capital. Thus, the present-future reproductive trade-off can be understood in terms of optimal investments in own embodied capital versus reproduction, and the quantity-quality and mating-parenting trade-offs can be understood in terms of investments in the embodied capital of offspring versus their number. The central thesis of this chapter is that there are four major factors affecting the timing of reproduction in the life course, reproductive rates, and parental investment for each sex: (1) the important resources consumed and utilized in reproduction and the production process by which those resources are obtained; (2) risks of mortality and the “technology” of mortality reduction; (3) the extent of complementarity between the sexes in the production of offspring; (4) the degree of variation in resource production and capital holdings among individuals and within individuals over time. With respect to the first factor, the relative impacts of mass-based, brain-based, and extrasomatic physical capital on resource production are critical determinants (see Figure 7-1). What are the marginal effects of an increase in body size on acquisition and turnover rates for energy and other critical resources? What are the marginal effects of increases in brain size, brain complexity, knowledge, and skill on resource production? How does physical capital, such as land or a breeding territory, affect production? How do body mass, brain-based abilities, and extrasomatic physical capital combine in resource production? The general expectation is that, since investments in each of those forms of capital trade off against each other and against allocations to reproduction, natural selection will optimize those investments so as to maximize descendent production. The brain is a special form of embodied capital. On the one hand, neural tissue monitors the organism’s internal and external environment and induces physiological and behavioral responses to stimuli (Jerison, 1973; 1976). On the other hand, the brain has the capacity to transform present experiences into future performance. This is particularly true of the cerebral cortex, which specializes in the storage, retrieval, and processing of experiences. To the extent that capital investments in the brain generate rewards that are realized over time (e.g., an increased reproductive rate during adulthood), the payoffs to those investments depend on mortality rates, since they affect the length of time over which the return will be realized. Dynamic models of this process show that investments in embodied capital coevolve with investments affecting mortality and longevity (Kaplan and Robson, 2002; Robson and Kaplan, 2003). The longer the time spent growing and learning prior to reproducing, the more natural
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Offspring: Human Fertility Behavior in Biodemographic Perspective FIGURE 7-1 Production as a function of the capital stock. NOTE: The relationship between production and each form of capital varies with ecology and the resources produced. Capital may be size-based, brain-based, or extrasomatic. More or less initial investment may be required before returns increase, and with further increases in investment, returns may diminish rapidly or slowly. selection favors investments in staying alive to reap the benefits of those investments. Similarly, any investments that produce increased energy capture rates later in life, such as learning, select for additional investments to reach those older ages. In addition to the production of energy, organisms can allocate energy and/or invest in forms of capital that reduce risks of mortality. While most biological models treat mortality as essentially exogenous, observed mortality is best understood in terms of an interaction between exogenous risks (environmental assaults) and endogenous responses designed to reduce mortality in the face of those risks. The technology of mortality reduction (the immune system, the ability to run, protective coverings such as shells, defensive weapons) also affects the likelihood of dying from environmental assaults. Models of embodied capital also show that ecological features or investments that increase the probability of survival to older ages also produce selection for greater investments in income-related embodied capi-
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Offspring: Human Fertility Behavior in Biodemographic Perspective FIGURE 7-2 Offspring viability isoclines (indifference curves) as a function of male and female inputs. tal. These coevolutionary effects appear to have been particularly important in human life history evolution. With respect to the third factor, complementarity, each parent in sexually reproducing species contributes approximately half the offspring’s genes and some amount of parental investment. The fitness of offspring is likely to be some function of the genetic material and the investments received from each parent. Each of these inputs may act as substitutes or complements, as illustrated in Figure 7-2. Stated simply, complementarity occurs when the value of male investment in offspring depends positively on the amount given by females and vice versa (with fitness held constant).2 In 2 Technically, complementarity occurs when marginal rates of substitution along fitness isoclines or indifference curves change as the ratio of the two inputs changes, making those curves convex to the origin.
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Offspring: Human Fertility Behavior in Biodemographic Perspective contrast, male and female inputs are substitutes when the relative values of the two inputs are independent of the amount provided by the other sex (again holding fitness constant). Thus, there are four axes of potential complementarity (e.g., between mother’s and father’s genes, between mother’s and father’s investment, and between each parent’s genes and their own and the other parent’s investments). Gains from specialization in parenting and/or mating effort and complementarity between genes and investment are forces favoring sexual dimorphism, with females typically specializing in parenting effort and males specializing in mating effort. Complementarity between the investments of each sex is the force favoring decreased sexual dimorphism and increased male parental investment. This kind of complementarity can occur when both direct care and resources are important to offspring viability and when the provisioning of each conflicts with, or is incompatible with, the provisioning of the other. For example, protection and feeding of nestlings are incompatible among many flying bird species. Protection of the young by one parent complements provisioning by the other parent, since food is only valuable to offspring that have not been preyed on. This ecology favors biparental investment and taking turns in feeding and nest protection by males and females. Among grazing mammals, however, offspring follow their mothers, who are able to nurse and protect them simultaneously. Investments by males in this case are less complementary and would only substitute for the investments of females. Mate choice criteria and mating “market” characteristics are expected to result from the variance among and within individuals over time with respect to the resources critical for reproduction. When females provide all the parental investment in response to the conditions discussed above, they are expected to exercise choice among males in terms of their genetic quality, and males are expected to compete with other males for access to fecund females, either through physical competition or appeals to female choice. As support from males increases in value with a resultant increase in their contribution to reproduction, we expect female choice to respond to variation in male offers of investment and in their ability to acquire resources utilized in reproduction. Males, in turn, as their investments in offspring increase, are expected to exert choice with respect to variation in female quality and to compete with other males for access to the resources utilized in reproduction. Ecological variability affecting the variance among males and females in resource access or access to mates is expected to exert a significant influence on mating market dynamics and in male and female investments in parenting and mating effort. Intertemporal variation in productivity within individuals is also likely to affect their mate value because it increases the likelihood of shortfalls.
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Offspring: Human Fertility Behavior in Biodemographic Perspective Our proposal is that human evolution has resulted in a specialized life history that is due to a particular constellation of the factors discussed above. This constellation derives from the hunter-gatherer way of life, which characterized the vast majority of human evolutionary history. While, as discussed in the next section, there are some universal features associated with this way of life, there is significant ecological variability across habitats. We also propose that as a result of exposure to such variation, human psychology and physiology have evolved to respond in systematic ways to variations in the four factors discussed above. Finally, the domestication of plants and animals and subsequent economic transformations produced new socioecological conditions to which people responded in radical shifts in parenting and mating practices. HUMAN LIFE HISTORIES IN A COMPARATIVE CONTEXT Relative to other mammalian orders, the primate order is slow growing, slow reproducing, long lived, and large brained. Humans are at the extreme of the primate continuum. Compared to other primates, there are at least four distinctive characteristics of human life histories: (1) an exceptionally long life span, (2) an extended period of juvenile dependence, resulting in families with multiple dependent children of different ages, (3) multigenerational resource flows and support of reproduction by older postreproductive individuals, and (4) male support of reproduction through the provisioning of females and their offspring. The brain and its attendant functional abilities are also extreme among humans. Our theory (Kaplan et al., 2000; Kaplan and Robson, 2002; Robson andd Kaplan, 2003) is that these extreme values with respect to brain size and longevity are coevolved responses to an equally extreme commitment to learning-intensive foraging strategies and a dietary shift toward high-quality, nutrient-dense, difficult-to-acquire food resources. The following logic underlies our proposal. First, high levels of knowledge, skill, coordination, and strength are required to exploit the suite of high-quality, difficult-to-acquire resources that humans consume. The attainment of those abilities requires time and a significant commitment to development. This extended learning phase during which productivity is low is compensated for by higher productivity during the adult period, with an intergenerational flow of food from old to young. Since productivity increases with age, the time investment in skill acquisition and knowledge leads to selection for lowered mortality rates and greater longevity because the returns on the investments in development occur at older ages. Second, the feeding niche specializing on large valuable food packages, and particularly hunting, promotes cooperation between men and women and high levels of male parental investment, because it favors sex-specific
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Offspring: Human Fertility Behavior in Biodemographic Perspective specialization in embodied capital investments and generates a complementarity between male and female inputs. The economic and reproductive cooperation between men and women facilitates provisioning of juveniles, which both bankrolls their embodied capital investments and acts to lower mortality during the juvenile and early adult periods. Cooperation between males and females also allows women to allocate more time to child care and improves nutritional status, increasing both survival and reproductive rates. The nutritional dependence of multiple young of different ages favors sequential mating with the same individual, since it reduces conflicts between men and women over the allocation of food. Finally, large packages also appear to promote interfamilial food sharing. Food sharing assists recovery in times of illness and reduces the risk of food shortfalls due to both the vagaries of foraging luck and the variance in family size due to stochastic mortality and fertility. These buffers against mortality also favor a longer juvenile period and higher investment in other mechanisms to increase life span. Thus, we propose that the long human life span, lengthening of the juvenile period, increased brain capacities for information processing and storage, intergenerational resource flows, and cooperative biparental investment in offspring coevolved in response to this dietary shift and the new production processes it entailed. It is not yet possible to know many vital statistics and behavioral characteristics from paleontological and archeological remains. It must be recognized that modern hunter-gatherers are not living replicas of our Stone Age past, and global socioeconomic forces affect them all. Furthermore, many foragers today live in marginalized habitats that underreward male hunting efforts. Yet despite the variable historical, ecological, and political conditions affecting them, there is remarkable similarity among foraging peoples, and even the variation often makes adaptive sense. Comparisons between foraging peoples and other modern primates are an important source of information about the life histories of our ancestors and the selection pressures acting on them, the subject of the next sections. Mortality and Production The age-specific mortality profile among chimpanzees is relatively V-shaped, decreasing rapidly after infancy to its lowest point (about 3 percent per year) at about age 13, the age of first reproduction for females, and increasing sharply thereafter. In contrast, mortality among human foragers decreases to a much lower point (about 0.5 percent per year) and remains low with no increase between about 15 and 40 years of age. Mortality then increases slowly, until there is a very rapid rise in the 60s and 70s. The pattern is much more block U-shaped. The strong similarities in the mortal-
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Offspring: Human Fertility Behavior in Biodemographic Perspective cially acquired, understanding cultural diffusion is critical. Evolutionary logic provides a framework for analysis of the active role that people play in determining which ideas they choose to adopt. ACKNOWLEDGMENTS This paper was written with support from the National Institute on Aging. The authors also wish to acknowledge the contributions of Kim Hill to the datasets and their analyses on the comparative diets and demography of chimpanzees and foragers published in a previous paper (Kaplan et al., 2000). We also thank Kim Hill and Magdalena Hurtado for their data on resource acquisition by age and sex among Hiwi and Ache. These datasets and analyses formed a critical base for part of this paper. We also wish to thank Monique Borgerhoff Mulder for her careful and extensive suggestions for revision of a draft of this paper. REFERENCES Anderson, K., H. Kaplan, D. Lam, and J. Lancaster 1999a Paternal care by genetic fathers and stepfathers II: Reports by Xhosa High School students. Evolution and Human Behavior 20:433-452. Anderson K.G., H. Kaplan, and D. Lam 2001 Grade repetition, schooling attainment and family background in South Africa. Unpublished manuscript. Population Studies Center, University of Michigan, Ann Arbor. Anderson, K.G., H. Kaplan, and J. Lancaster 1999b Paternal care by genetic fathers and stepfathers I: Reports from Albuquerque men. Evolution and Human Behavior 20:405-432. Bailey, R.C., M.R. Jenike, P.T. Ellison, G.R. Bentley, A.M. Harrigan, and N.R. Peacock 1992 The ecology of birth seasonality among agriculturalists in Central Africa. Journal of Biosocial Science 24:393-412. Becker, G.S. 1975 Human Capital. New York: Columbia University Press. Becker, G.S., and R.J. Barro 1988 A reformulation of the economic theory of fertility. Quarterly Journal of Economics 103:1-25. Bentley, G.R., R.R. Paine, and J.L. Boldsen 2001 Fertility changes with the prehistoric transition to agriculture. Pp. 203-232 in Reproductive Ecology and Human Evolution. P.T. Ellison, ed. Hawthorne, NY: Aldine de Gruyter. Betzig, L. 1986 Despotism and Differential Reproduction: A Darwinian View of History. Hawthorne, NY: Aldine de Gruyter. 1992a Roman monogamy. Ethology and Sociobiology 13:351-383. 1992b Roman polygyny. Ethology and Sociobiology 13:309-349.
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Representative terms from entire chapter: