667606

The Capital Economy in Hominin Evolution: How Adipose Tissue and Social Relationships Confer Phenotypic Flexibility and
Resilience in Stochastic Environments Author(s): Jonathan C. K. Wells Reviewed work(s): Source: Current Anthropology, Vol. 53, No. S6, Human Biology and the Origins of Homo (December 2012), pp. S466-S478 Published by: The University of Chicago Press on behalf of Wenner-Gren Foundation for Anthropological Research Stable URL: http://www.jstor.org/stable/10.1086/667606 . Accessed: 27/01/2013 10:58
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Current Anthropology Volume 53, Supplement 6, December 2012
The Capital Economy in Hominin Evolution

How Adipose Tissue and Social Relationships Confer Phenotypic Flexibility and Resilience in Stochastic Environments by Jonathan C. K. Wells
The global distribution of our species indicates a biology capable of adapting to an extraordinary range of ecosystems, generating interest in how such a biology evolved. Whereas much attention has been directed to genetic adaptation and developmental plasticity as adaptive strategies, ecological stochasticity within the life course may be addressed by additional strategies such as bet hedging and phenotypic exibility. Both social relationships and adipose tissue may be considered as energy capital conferring reversible phenotypic exibility across the life course. Evidence from primates and contemporary humans demonstrates the value of such energy capital in accommodating ecological uncertainty. The fact that Homo sapiens is characterized by high levels of both cooperative sociality and adiposity compared with extant apes suggests that ecological stochasticity may have been a key ecological stress in the evolution of our genus. The benets of phenotypic exibility for ecological risk management may have preceded and enabled the emergence of traits such as carnivory, encephalization, colonizing, and the maintenance of a single breeding species across diverse environments.
To understand the particular characteristics of extant humans, much work has focused on physical traits readily discernible in the fossil record, such as cranial capacity, dentition, and postcranial anatomy. Such investigation enables the reconstruction of trends in functional traits such as encephalization, locomotion, and reproduction (e.g., Anto n 2003; Bramble and Lieberman 2004; Bruner, Manzi, and Arsuaga 2003; DeSilva 2011; Rosenberg and Trevathan 2002). Evolutionary changes in such traits are typically considered physical or physiological solutions to ecological stresses, such as climate trends or shifts in the availability of resources (Klein and Edgar 2002; Vrba 1985), although neutral evolution and genetic drift may also contribute to phenotypic trends. Much attention has been directed, for example, to understanding what might have driven the trend toward bipedal locomotion in earlier hominins (e.g., Crompton, Sellers, and Thorpe 2010) or progressive encephalization in the genus Homo (e.g., Bruner, Manzi, and Arsuaga 2003). Dental analysis offers the capacity to reconstruct how hominins responded to changes in the availability of food sources (Organ et al. 2011), indicating, for example, a postaustralopithecine shift to a broader diet base (Ungar 2012). Although the emergence of the genus Homo
Jonathan C. K. Wells is Professor of Anthropology and Pediatric Nutrition at the Childhood Nutrition Research Centre, University College London Institute of Child Health (30 Guilford Street, London WC1N 1EH, United Kingdom [jonathan.wells@ucl.ac.uk]). This paper was submitted 12 XII 11, accepted 3 VII 12, and electronically published 23 X 12.
has generally been considered an integrated shift in many of these trends, this perspective is now undergoing reappraisal in the light of more comprehensive skeletal evidence (Anto n and Snodgrass 2012). The study of ecogeographical and temporal variability within contemporary humans plays a key role in these reconstructions. For example, substantial research has been conducted on the association between climate and morphology in humans (Hiernaux and Froment 1976; Katzmarzyk and Leonard 1998; Roberts 1953; Wells 2012b). Such work then informs understanding of past variability in hominin morphology (Perry and Dominy 2009; Ruff 2002). Similarly, variability in contemporary or recent human dentition can be used to infer past dietary stresses and to evaluate evolutionary patterns (Anto n, Carter-Menn, and DeLeon 2011; Kaifu et al. 2003). Although not addressed explicitly by all authors, nonpathological anatomical variation in the fossil record has traditionally tended to receive a genetic interpretation (e.g., Holliday 1997; though see Ruff 2002). First, phylogenetic analyses typically show good agreement between molecular and morphological data (Gibbs, Collard, and Wood 2000; Gilbert and Rossie 2007; Pilbeam 2000), potentially implying a similar scenario for within-species variability. Second, the long-standing attention directed to long-term ecological trends as key stresses (e.g., the savannah hypothesis; Dart 1925; Klein and Edgar 2002) would also match with a genetic model of adaptation. Consistent with such a perspective, climate has indeed been associated with genetic variability among contemporary humans (Hancock et al. 2010, 2011).
2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0016$10.00. DOI: 10.1086/667606
Wells The Capital Economy in Hominin Evolution
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More recently, however, the contribution of developmental plasticity to phenotypic variability has been recognized in extant primates and humans, suggesting that a similar approach is required for the fossil record (e.g., Ruff 2002). Experimental work on primates has demonstrated rapid transgenerational shifts in body proportions in populations exposed to novel thermal environments (Paterson 1996) or to shifts in the availability of energy (Price, Hyde, and Coe 1999), clearly demonstrating a contribution of plasticity to phenotypic change across generations. Similar work in humans has shown that both nutritional experience and psychosocial stress in early life can exert long-term effects on multiple aspects of phenotype (e.g., Bogin et al. 2002; Ellis et al. 2009). A more comprehensive approach must therefore assume that variability in the hominin fossil record reects the inuences of both genotype and developmental plasticity (Kuzawa and Bragg 2012; Ruff 2002; Wells and Stock 2007). The fundamental connection between contemporary human variability and past evolutionary change may also apply to phenotypic traits that leave, at best, weak signals in the fossil record. Recently, for example, much interest has been directed to why and when the unusual life history prole of humans (lengthy life spans and developmental periods but short interbirth intervals) emerged in our evolutionary history (Aiello and Key 2002; Anto n 2003; Hawkes 2006; Hrdy 2009). Life history variability among contemporary humans is assumed to incorporate adaptation to stresses such as energy availability and mortality risk, though the associations are complex (Ellis et al. 2009; Migliano and Guillon 2012; Perry and Dominy 2009; Walker and Hamilton 2008; Walker et al. 2006). In turn, humans per se have an unusually lengthy period of development, suggesting that the Homo niche favored a progressive reorganization of the tempo of development in response to diverse ecological pressures, some of them potentially compounded by hominin traits such as increasing brain size (Isler and van Schaik 2012; Robson, van Schaik, and Hawkes 2006; Schwartz 2012). Information on some life history traits can be gleaned from the fossil record, though others, such as interbirth interval and total fertility rate, may leave no material signal. For example, dental eruption patterns represent markers of maturation rate across species, though interpretation is complex (Schwartz 2012), while age at weaning can potentially be estimated from isotopic enrichment ratios (e.g., Herring, Saunders, and Katzenberg 1998). Furthermore, plasticity in such developmental traits may be revealed by traits such as body proportions; for example, leg length appears particularly vulnerable to poor childhood nutrition, and short leg length may therefore act as a skeletal marker for slowed development (e.g., Li, Dangour, and Power 2007), though other ecological stresses such as cold climates may generate similar effects (Katzmarzyk and Leonard 1998). This overall approach is thus proving very valuable for understanding both when and why human traits emerged and also how they have come to vary across ecological conditions
since the origin of our species. However, the interpretation of such phenotypic variation in the fossil record as adaptation is possible only because each adaptation of genotype and developmental plasticity may generate relatively irreversible phenotypic effects within the life course. Natural selection acts not on traits but on strategies (Houston and McNamara 1999), for example, not on tall height, but on growing faster or for longer. In contrast to the examples described above, some adaptive strategies are relatively reversible, which in turn tells us about the kind of ecological stresses that drive them. Such plasticity may relate either to the instability of phenotype within individuals or to phenotypic relationships between individuals. In this article, I rst describe how stochastic environments favor such phenotypic exibility, which may emerge in different formats. I then review how both primates and humans benet from such exible traits, focusing in particular on two generalized stores of energy. Finally, I consider what role such energy stores may have played in human evolution.
Modes of Adaptation
Phenotypic plasticity embraces many forms that can vary both in their relative speed of response to ecological stresses and in their degree of reversibility. At one extreme, developmental plasticity tends to be relatively irreversible, reecting interactions between genotype and environment in early life, whereas at the other extreme, some aspects of metabolism and behavior can alter on a second-by-second basis (Gabriel et al. 2005; Piersma and Drent 2003). In turn, the time lag of plastic response following the environmental cue may also vary (Gabriel et al. 2005). Most work has focused on the two extremes, using quantitative genetic models to address the norms of reaction underlying developmental plasticity or optimality theory to address behavioral ecology (Gabriel et al. 2005). Such variability in the form of plasticity reects variability in the frequency and regularity of ecological stresses relative to the life span of the organism (Piersma and Drent 2003). Although attention has traditionally been directed to longterm ecological shifts affecting hominin evolution, there is increasing interest in the diversity of ecological stresses, some of which are short-term but frequent and unpredictable (Bobe and Behrensmeyer 2004; Potts 1996, 2012). Genetic adaptations can develop over variable time spans. There is increasing recognition that specic traits underlying the complex life history prole of humans have a polygenetic basis (Elks et al. 2010; Hirschhorn and Lettre 2009; Yang et al. 2010); hence, phenotypic variability in such traits may derive in large part from variability in gene frequencies within and between populations (Hancock et al. 2010). Although often assumed to require hundreds of generations, genetic change can occur rapidly during periods of rapid population growth, and hence it may have been particularly important since the Neolithic revolution (Cochran and Harpending 2009).
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Developmental plasticity represents a faster mode of phenotypic change, theoretically capable of ne-tuning phenotype to more recent or local conditions (Stearns 1992; WestEberhard 2003). A key mechanism underlying such plasticity is epigenetic variability in gene expression in response to environmental factors occurring during early development (Youngson and Whitelaw 2008). Such epigenetic marks are then broadly maintained through the life course, though with progressive attrition over time (Fraga et al. 2005). It is tempting to assume that developmental plasticity is adaptive; however, in long-lived species there may be a systematic shift in ecological conditions between the life course periods of development and reproduction, potentially resulting in costly maladaptation. Many ecological stresses are not systematic, however, and occur irregularly through the life course while still exerting powerful effects on biology. Potts (2012) has argued that studies using single markers of past ecological change have tended to bias interpretation toward particular climatic trends (e.g., temperature or aridity) and that a more integrative approach emphasizes temporal uctuations in the overall level of ecological variability and hence shifts attention from ecological stress to ecological uncertainty. As the frequency of stochasticity accelerates relative to the duration of the life course and hence the level of uncertainty increases, systematic adaptations of the kind described above are neither especially valuable nor indeed easy to develop. At the simplest level, the environment may ip between two extremes, generating a dilemma for the organism: adapt to one, the other, or neither, in which case it will be maladapted in both situations. In unstable environments, therefore, commitment to any simple adaptive strategy is problematic, and a more sophisticated strategy is required. Already in early hominin evolution, australopithecines were able to tolerate substantial environmental variability between 3.4 and 2.9 mya, during which temperature and rainfall uctuated, and they appear to have done so without favoring one ecosystem over another (Bonnelle et al. 2004). The greater geographical range of early Homo suggests even greater capacity to tolerate diverse environments. What kinds of adaptive strategy could have enabled such versatility?
Evolutionary Economics
To investigate the challenge of ecological uncertainty, it is useful to draw on concepts from the discipline of economics. Economic ideas have long been widely used in biology, given implicit or explicit recognition of common ground between rational decision making and the process of natural selection (Vermeij 2004). Classic work addressed parental investment (Trivers 1972), evolutionary game theory (Maynard Smith 1982), and optimal foraging theory (MacArthur and Pianka 1966), but a second wave of evolutionary economics is now seeing a range of new ideas tested on biological phenomena (Hammerstein and Hagen 2005). Many of these ideas
explicitly address the concepts of risk and uncertainty, which to variable degrees challenge both organisms and nancial institutions. Such uncertainty requires decisions to be made on the basis of imperfect information. For biological organisms, such decisions are shaped by the forces of selection into a coherent adaptive strategy (Laubichler, Hagen, and Hammerstein 2005). Consider an environment that ips irregularly between two states of contrasting quality, such that the phenotypic traits that maximize tness in one environment are very different to those that maximize tness in the other. A number of responses are possible, depending on the timescale of change and the availability of cues. If the rate of ipping is low, each generation of organisms can search for cues of environmental quality and use these to guide ontogenetic development. Here, risk is addressed by acquiring up-to-date information. Such developmental plasticity is certainly important in promoting phenotypic variability, some of it potentially adaptive, among contemporary human populations, such as brain sparing in response to fetal undernutrition (Hales and Barker 1992). An enhanced level of such plasticity may plausibly have emerged during recent hominin evolution. This hypothesis remains untested, however, because of inadequate information on plasticity in nonhuman apes. If the rate of environmental ipping is high, another potential response of the organism is stochastic phenotype switching across generations, more commonly known as bet hedging (Beaumont et al. 2009; Philippi and Seger 1989). Here, no information is sought; rather, environmental randomness is addressed directly by phenotypic randomness. Bet hedging may be further subdivided into a conservative strategy (avoiding phenotypic extremes and opting for an intermediate phenotype) versus a diversied strategy (producing multiple phenotypes; Philippi and Seger 1989). In each case, the variance in parental tness is decreased by increasing the likelihood that at least a subset of offspring will prove adapted to whatever environment is encountered. Consistent with such theory, recent experiments in bacteria have demonstrated the emergence of bet-hedging phenotypes in populations exposed repeatedly to contrasting conditions (Beaumont et al. 2009). The success of developmental plasticity and bet hedging is inuenced by the rate of generation time relative to the rate of environmental ipping. In any ape or hominin past or present, requiring at least a decade to grow to reproductive maturity, neither developmental plasticity nor bet hedging are satisfactory solutions to high levels of ecological stochasticity. Information accessed in early life loses value because it cannot refer to the multiple ecological states that may occur in succession, while each of the bet-hedged variants may be selected out when in the wrong environment. This is not to suggest that bet hedging and developmental plasticity do not contribute to overall adaptive strategy in humans but simply that
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they do not comprise an adequate response to increasing ecological stochasticity. An additional strategy is therefore required by organisms with lengthy developmental periods if they are to tolerate environments with high levels of stochasticity. A key feature of this alternative strategy is reversibility; in other words, a reduction in life course commitment to any specic phenotypic state (Wells and Stock 2012). Phenotypic exibility meets this requirement by increasing the breadth of environmental tolerance, that is, the range of viable ecological conditions (Gabriel et al. 2005). In the following section, I discuss the generic role of capital, another concept derived from evolutionary economics, in conferring such phenotypic exibility.
The Evolutionary Economics of Capital

In seminal work, Kaplan and colleagues (Kaplan, Lancaster, and Robson 2003; Kaplan et al. 2000) proposed that development be considered as a process in which individuals and their parents invest in a stock of embodied capital (Kaplan et al. 2000:164). They (Kaplan et al. 2000:164) proposed that in a physical sense, embodied capital is organized somatic tissue. In a functional sense, embodied capital includes strength, immune function, coordination, skill, knowledge, and social networks, all of which affect the protability of allocating time and other resources to alternative activities such as resource acquisition, defense from predators and parasites, mating competition, parenting and social dominance. This broad approach is instrumental in integrating a variety of raw inputs and phenotypic outputs relevant to life history variability. I propose to build on this approach here by emphasizing two components of embodied capital representing energy stores. Previously, I differentiated illiquid and liquid capital specically to distinguish between components of embodied capital that represent commitment to a given phenotype and those that offer reversibility (Wells 2010b). Energy represents liquid capital that may be gained and lost from two primary stores, social capital and adipose tissue. Each of these stores allows the conversion of diverse raw substrates (e.g., discrete food parcels, behavioral interactions) into generalized energy currencies. While Kaplan and colleagues (Kaplan, Lancaster, and Robson 2003; Kaplan et al. 2000) discussed social networks as an example of embodied capital, they paid minimal attention to adipose tissue as a functional tissue in the same context. The capacity to store energy buffers strongly against uctuations in energy supply and demand (Pond 1998). Classically, life history strategy is assumed to comprise a series of trade-offs, most importantly between the functions of maintenance, growth, reproduction, and immune function, but also between current and future reproduction (Hill 1993; Zera and Harshman 2001). The traditional model of resource allocation assumes that investment in one function is at the cost of investment in another because of limited overall resources (van Noordwijk and de Jong 1986). Energy stores can
negate such negative correlations on an immediate basis, breaking down the simple association between phenotype and selection. By introducing a time lag between energy income and energy utilization, life history decisions may be detached from the immediacy of ecological stochasticity. It is the buffering of life history investment decisions from selective pressures that is key to the value of energy capital. While developmental plasticity primarily affects the rates of growth and maturation, phenotypic exibility is of particular importance for maintaining exibility in the trade-off between current and future reproduction in adult life. At the level of the cell, energy needs are relatively constant although still subject to inuences such as physical activity and infection. Cellular needs are maintained by regulatory processes that can balance shortfalls against reserves and hence maintain function even as the environment varies. Classically, for example, ecologists distinguish between income breeders, which capture the energy needed for reproductive effort from the environment on a daily basis, and capital breeders, which accumulate energy stores before breeding (Jo nsson 1997; Stearns 1992). The key difference is that capital breeders can breed in a range of ecological circumstances because they are buffered from uncertainty in energy availability (Pond 1984; Stearns 1992). Most attention has focused on adiposity as the primary source of capital for funding reproduction, but using the concept of the extended phenotype (Dawkins 1982), social networks likewise provide energy capital, as in the case of cooperative breeding (Hrdy 2009). Storing energy physically in the body and behaviorally in the social group represents complementary strategies with different implications for addressing uncertainty. Social capital stored in networks allows energy to be differentially distributed across a group of individuals. At any given time, a single individual may fail to achieve daily energy balance without experiencing penalties because of the role of others in subsidizing total energy requirements. For periods of high energy demand such as reproduction, this social distribution of energy supply reduces the need of any individual to capture directly from the environment or to store within the body the total energy required. However, such social stores also make possible social competition over access to energy. An assumed relationship of reciprocity might fail to materialize when most needed. Equally, an adverse ecological event might substantially reduce the energy content of an entire social network, placing all individuals at risk. Obligations or promises of producing energy might therefore become relatively worthless in a low-productivity environment. Adipose tissue offers greater individual control of energy by maintaining it in physical form but at the cost of having to transport it as additional body weight. This could increase the risk of predation as demonstrated empirically in some species and hypothesized for hominins (Speakman 2007). Lipid stores allow some functions, or tissues, to fail to achieve daily energy balance, their requirements being met instead
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through lipolysis in adipose tissue (Pond 1998). Somatic energy stores are essentially ring-fenced for individual use, though that does not preclude targeting them at particular social relationships, for example, investing in offspring. Increasing internal energy storage is favored when the energy needs of a social group are heterogeneous, so that the value of energy likewise differs between individuals. Generically, organisms occupying more stochastic environments are predicted to benet from such energy capital, leading to species differences in traits such as adiposity and sociality (Pond 1998). On the one hand, energy capital is a highly effective form of phenotypic exibility, allowing capital to be stored or invested in good conditions and used to buffer poor conditions. This reversibility reduces the need for expensive permanent traits that are only suited to particular ecological conditions. On the other hand, the magnitude of capital in any given individual may guide life history strategy, as demonstrated in other species (e.g., Liao et al. 2011; Zera and Zhao 2003). Energy capital may, for example, affect developmental plasticity but may further enable energy partitioning between different life history functions during adulthood, such as meeting the costs of immune function during infection and funding reproduction when infection is absent (Wells 2010a). As with other traits reviewed in the introduction, we can therefore consider how capital stores vary within and between contemporary populations and attempt to reconstruct the evolutionary history of capital stores in past populations.
Variability in Commitment across Species

The concepts of phenotypic reversibility versus irreversibility match closely with the more established terminology of plasticity and canalization. These latter traits are integrally related (Flatt 2005) precisely because the plasticity of some traits in the face of ecological stresses underlies the relatively invariant phenotype of others. In mammals, for example, growth of the brain is relatively protected from environmental stresses, and other traits are more plastic in response to nutritional or climatic stress (e.g., Barbiro-Michaely et al. 2007). Organisms are therefore more committed to brain growth than they are to other components of growth. Beyond such within-organism contrasts, species also vary among themselves in the extent of genetic specialization versus phenotypic plasticity, that is, in their commitment to specic niches. The lack of commitment in the human genome is already evident from comparisons with the genomes of other apes. Although subject to continued gene ow between populations, chimpanzees, gorillas, and orangutans have been considered to comprise two different species or subspecies despite occupying relatively small geographic ranges compared with humans (Becquet and Przeworski 2007; Hey 2010; Warren et al. 2001), and furthermore, the degree of genetic variability in each such species is greater than in the entire human genome (Gagneux et al. 1999; Kaessmann et al. 2001). Chim-
panzees have also been subject to more positive selection than humans (Bakewell, Shi, and Zhang 2007). While there is increasing evidence for multiple recent species of Homo (Homo neanderthalensis, Homo oriensis; Brown et al. 2004) and a new type recently reported from Siberia (Krause et al. 2010; Reich et al. 2010), only one species exists in the contemporary world. Although a reduced level of genetic variation is predicted in modern humans given our relatively recent speciation (Cann, Stoneking, and Wilson 1987) and potentially due to culturally mediated migration patterns (Premo and Hublin 2009), a proportion of the genetic variability of other Homo species is also assumed to have passed into our own species (Garrigan and Hammer 2006; Green et al. 2010; Reich et al. 2010). Regardless of the timescale and mode through which genetic variability might have accumulated, what is arguably most notable in humans is our relatively low level of genetic differentiation in proportion to the extraordinary diversity of habitats we now occupy. This contrasts markedly with much greater genetic differentiation in apes despite their inhabiting relatively homogeneous environments (Gagneux et al. 1999). The relative genetic unity in Homo sapiens implies continued interbreeding between regional populations even as they occupied diverse habitats and ecological niches. Indeed, some studies also suggest a degree of recent interbreeding with other contemporaneous Homo species (Green et al. 2010; Reich et al. 2010; though see Eriksson and Manica 2012). It is clear that some adaptive strategies have become incorporated into the human genome, such as the elongation of growth and its division into several distinct developmental periods (Bogin and Smith 1996), that therefore represent commitment to a generic human niche. Beyond this commitment, the within-population genetic variability that is evident in any human life history trait (e.g., stature, birth weight, age at menarche, longevity; see Wells and Stock 2011) may be considered to represent diversied bet hedgingthat is, the maintenance of phenotypic diversity among offspring to increase parental tness (Ellis et al. 2009; Wells 2009)while each of these life history traits also shows substantial plasticity (Wells and Stock 2011). However, my argument here is that the limited genetic commitment of humans is complemented not only by developmental plasticity but also by extensive use of energy stores that may be allocated exibly between competing phenotypic traits and between individuals and hence alleviate ecological stochasticity. The next section considers the contribution of energy capital to phenotypic exibility in nonhuman primates.
Capital and Flexibility in Nonhuman Primates

Primates have high levels of sociality, and their tendency to solve ecological problems in social ways is well established (Hrdy 2009; Lee 1999; Sussman, Garber, and Cheverud 2005). A review of primate activity budgets suggested the proportion of time directed to sociality ranged from 1% to 8% in pro-
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simians, from1% to 22% in New World monkeys, from 1% to 28% in Old World monkeys, and from 2% to 25% in apes (Sussman, Garber, and Cheverud 2005). Importantly, the majority of such social behavior was cooperative and afliative rather than antagonistic. Individuals may invest in social relationships and accumulate social capital that may be converted back into benecial physical resources (Isler and van Schaik 2009). For example, female chacma baboons who formed stronger and more stable social bonds with other female baboons had greater longevity (Silk et al. 2010) and also produced offspring who themselves had greater longevity through increasing the rates of offspring survival (Silk et al. 2009). Similarly, social relationships may benet male tness, as demonstrated in Assamese macaques, where strong bonds between males were linked to the formation of coalitions, dominance rank, and the number of offspring sired (Schulke et al. 2010). Such social investments make their maximal contribution to exibility when they enable cooperative breeding, a behavior evident in some primate species as well as other mammals and birds (Isler and van Schaik 2009) and involving a continuum of behavior ranging from carrying or protecting offspring to babysitting, provisioning, or suckling them (Hrdy 2004, 2009). Here, social capital contributes directly to the capacity of reproducing females to meet the total energy demands of their offspring. In Hanuman langurs, infants were observed to be carried by females other than the mother for up to half of daylight hours, which has sufcient effect on the maternal energy budget to reduce the time to the next conception (Hrdy 2004). Among marmosets and tamarins, males may carry offspring for the majority of the time and also supplement maternal milk in the offspring diet with small-prey items (Garber 1997). Collectively, maternal tness in these species is positively correlated with the number of male helpers, and in cotton-top tamarins, such help appears obligatory, with mothers lacking assistance tending to abandon their young (Hrdy 2004). Such cooperative behavior not only increases the exibility in provisioning offspring but also permits exibility in mating arrangements (Hrdy 2004). Such social interactions reduce the strength with which energy turnover is a function of a single organisms body size and instead increase the strength with which it reects social relationships (Kramer and Ellison 2010; Reiches et al. 2009). Recent exploration of such communal energy budgets has emphasized activity subsidies (e.g., babysitting) as well as redistributions of food and multiple and changing contributions from ascendant and descendant kin across the life course (Kramer and Ellison 2010; Reiches et al. 2009). By enabling energy dynamics to be temporarily invested extracorporeally, social relationships promote maximal exibility in reproductive energetics. Such energy transfers need not necessarily be maintained in social relationships and may instead be converted to physical capital, either extracorporeal, in the form of food hoards, or physiological, in the form of adipose tissue. Extracorporeal
food stores are known in some bird and mammal species, while adiposity is a widespread somatic adaptation to ecological uncertainty (Pond 1984, 1998). In primates, the use of adipose tissue to resolve seasonal uctuations in energy availability was elegantly demonstrated in a study of orangutans where urinary ketones indicated the metabolism of fat during periods of negative energy balance (Knott 1998). The highest levels of ketones were observed in pregnant or lactating females, highlighting the value of adipose tissue in buffering reproduction from ecological stochasticity. Greater adiposity or leptin levels have been reported in females compared with males in baboons (Rutenberg et al. 1987), macaques (Schwartz and Kemnitz 1992), chimpanzees (Bribiescas and Anestis 2010), and orangutans (Morbeck and Zihlman 1988), but information on adiposity and its regulatory effects remains surprisingly scarce in the primate literature considering how important the trait appears in hominin evolution (Wells 2010a). Intriguingly, the males of some marmoset and tamarin species have been shown to gain weight during their mates pregnancy, a strategy suggested as adaptive given their key alloparental role after delivery when they may carry offspring equivalent to 20% of their own body weight (Ziegler et al. 2006). Importantly, a rapidly growing literature has demonstrated that adipose tissue is not only a fuel store but also the source of numerous signaling molecules that coordinate energy trade-offs between competing biological functions such as growth, immune function, and reproduction (Wells 2010a). The role of adipose tissue in such functions has been demonstrated in a variety of species (Bartness, Demas, and Song 2002; Demas 2004; Pond 1998). Among the hormones secreted by adipose tissue is leptin, signaling the availability of energy to the brain, and studies in a variety of species have shown that it helps regulate the allocation of energy between competing functions (Demas and Sakaria 2005; Drazen, Demas, and Nelson 2001; Schneider 2004). Adipose tissue also provides both the energy and the molecular precursors for immune function, and it does so in tissue-specic fashion, indicating differential preparation of specic tissues for different types of pathogen (Pond 2003). The emergence of adipose tissue has been proposed to have aided control over the dynamics of energy supply and demand between tissues, for example, to allow high energy processes such as lactation to occur during periods of minimal energy intake in primitive mammals (Pond 1984). These data from primates and other mammals illustrate for both sexes how accumulating energy capital can confer diverse tness benets while increasing resilience to ecological factors operating at the level of the individual. However, how these strategic decisions are enacted at the molecular level in diverse species remains to be established in detail. Importantly, the use of energy capital by marmosets and tamarins affects not only immediate reproduction but also demography. These primates have a powerful ability to increase population size and colonize new niches (Hrdy 2009), indicating
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that the adaptive strategy of phenotypic exibility that can buffer individuals from energy stress in harsh conditions can furthermore drive population growth beyond that feasible in individual income breeders in good conditions.
Capital Investment and Humans

Recent work has highlighted a variety of ways in which the storage, mobilization, and transfer of capital within and between individuals confer signicant exibility in contemporary humans. Adipose tissue can supply energy for growth, reproduction, and immune function, and a number of hormones have been shown to contribute to this strategic partitioning of energy. Paradoxically, the evidence that leptin levels correlate with energy stores in humans and hence orchestrate such trade-offs is currently inconsistent and better supported in females than in males (Bribiescas 2001; Kuzawa, Quinn, and Adair 2007; Sharrock et al. 2008). It is likely that leptin makes up only one of a range of molecular signals involved in the regulation of biological functions (Schneider 2004); for example, insulin is increasingly recognized to play a key role in coordinating life history trade-offs (Harshman and Zera 2007; Watve and Yajnik 2007). The life course trajectory of human body composition indicates the changing value of fat during development, breeding, and aging. High neonatal adiposity of humans compared with other mammals has been hypothesized to buffer the obligatory energy demands of the large Homo brain (Kuzawa 1998). However, this need not represent the only or even the primary function of such adiposity. Unpublished data from Ethiopia (n p 255) show that over the rst 6 months, infants rst increase disproportionately in adiposity and then accrete disproportionately lean mass (Andersen, Friis, and Wells, unpublished data). The magnitude of infant energy stores may therefore guide the early accretion of lean tissue, which has less capacity to oscillate in response to energy uctuations. Adipose tissue may be important in supporting, regulating, and protecting each of somatic growth, immune function, and brain development during infancy when mortality risk is highest (Kelly 1995) while furthermore accommodating the initiation of sex differences in life history strategy. Because early energy supply derives primarily from the maternal budget, such regulatory effects of adipose tissue are ultimately a transgenerational maternal effect (Ong et al. 2007; Wells 2010b), as discussed below. During development, the two sexes show contrasting somatic capital accumulation, with adult males achieving greater height and relative lean mass and less fat mass than females (Wells 2007b). These differences in adiposity are particularly evident for fat distribution, with the enhanced peripheral fat of females both signaling reproductive capacity and meeting the energy costs of lactation (Wells 2010a). Humans are capital breeders and hence can breed across a range of ecological conditions and seasons, though in good conditions they use daily energy income rather than drawing on energy stores.
Through adulthood, gender differences in fat distribution slowly decrease, so that by old age the genders converge in body shape, and central adiposity in both sexes is increased relative to peripheral adiposity (Wells, Cole, and Treleaven 2008). Both sexes lose lean mass such that in later life the body becomes more economical (Zafon 2007). These shifts in fat distribution have been interpreted as life history strategy in which increased prioritization of central adiposity with increasing age promotes immune function at the expense of reproduction (Wells, Grifn, and Treleaven 2010). The ratio of fat to lean tissue therefore emerges as a key adaptive strategy in which growth can be tailored to ecological conditions under the transducing effect of maternal phenotype. The magnitude of lean mass has long-term implications for energy requirements, while the magnitude of adiposity can respond by providing appropriate risk management (Wells 2012c). For example, the low birth weight characteristic of contemporary Indian populations, poorly nourished for many generations, incorporates a low level of investment in lean mass balanced by an increased investment in adiposity (Yajnik et al. 2003). Collectively, these traits represent an economical and resilient phenotype capable of tolerating high uncertainty in infant energy supply. More broadly, many environmental factors generate variability in the fat-lean ratio, indicating that the strategy for accumulating and using energy capital is sensitive to multiple life course and ecological signals, including physical (e.g., climate), ecological (e.g., diet, disease), social (e.g., maternal rank), and demographic (e.g., parity, interbirth interval) factors (Wells 2011, 2012b). The magnitude of sexual dimorphism in adiposity has likewise further been shown to vary in relation to ecological factors (Wells 2012d). Capital acquisition also reects a multitude of dynamic social interactions in which energy is passed to and from individuals through a complex set of relationships. One might consider the high adiposity of infants as a temporary accumulation of capital favored by the sum total of maternal and alloparental provisioning during pregnancy, a source of income less guaranteed as the offspring matures. Thus, energy capital may be rapidly moved between individuals not only to boost the stores of some individuals but also as loans physically protected from those with competing interests. Research on diverse human populations has demonstrated an extraordinary degree of variability in the nature and structure of relationships that underlie the distribution of energy capital (Kaplan, Lancaster, and Robson 2003; Sear and Mace 2008). In 10 foraging societies, on average men acquired 68% of the calories and 88% of the protein and hence were by far the dominant supplier of calories to weaned offspring as well as protein and fat to women, though there was also variability between populations in these contributions (Kaplan et al. 2000). This highlights the sexual division of labor as another key component of human exibility in capital acquisition. Hrdy (2009) argued that while male provisioning is critical for cooperative breeding, the specic contribution of the father cannot be guar-
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anteed, resulting in a range of strategies for mothers to acquire additional fathers and hence bet-hedge across multiple male providers. Similarly, in relation to females, maternal grandmothers have been shown in several societies to be important alloparental provisioners of grandoffspring and hence to promote their survival (Hawkes, OConnell, and Blurton Jones 1989; Sear and Mace 2008). Cooperative breeding and pooled energy budgets therefore offer unprecedented exibility in humans as they impose minimal constraints on the social relationships generating energy supply at the individual level (Hrdy 2009; Reiches et al. 2009). More broadly, social capital may be distributed across multiple social relationships, which may be accumulated through the life course. No single social relationship may prove a reliable source of support in every circumstance; hence, bet hedging across multiple relationships may again prove the optimal strategy. Because a group of humans must inevitably compete for the sum total of available energy in the local environment, networks of social support can never be entirely benign but must rather contain a variety of different relationships, some based on kinship and others on political alliances. For example, studies of the !Kung bushmen of southern Africa show that relationships of reciprocity are key to the management of nutritional risk (Howell 2010), a scenario also observed in many other nonindustrialized societies (Couper-Johnston 2000). Such social capital distributes risk across rather than within individual bodies and hence buffers uncertainty in individual foraging returns. The combination of variable dynamics of cooperative breeding and life course exibility in adipose tissue stores means that humans are uniquely undercommitted to any specic niche, which helps us to understand our unusual capacity to colonize. Such undercommitment is backed up by other generalized subsistence strategies such as meat eating and cooking (Foley 2001; Sullivan, Hagen, and Hammerstein 2008), each of which reduces the need to adapt physiologically to specic diets. Social capital likewise underpins a wide variety of human relationships, including coalitions and alliances and other forms of cooperative behavior. In the context of ecological uncertainty, one could argue that energy capital is not for anything in particular. Its purpose might be seen instead as a way of avoiding committing energy to any specic function at any specic time, instead providing sophisticated risk management of life history strategy by integrating a cumulative array of individual signals from the physical and social environment. The brain and adipose tissues both play a part in such integrative regulation and hence emerge as important control centers for life history strategy (Wells 2010a, 2012c). Intriguingly, each of these organs acts strongly on the other (g. 1). With respect to the brain, recent research on the neuroendocrine basis of social behavior has demonstrated the effects of a range of hormones; for example, oxytocin plays a key role in cooperative behavior, while neuropeptide Y plays an equally fundamental role in the stress response (Hirsch and
Figure 1. Alternative and complementary strategies for accommodating ecological stochasticity. The brain integrates social and behavioral information, inuencing physiological regulatory systems. Adipose tissue integrates ecological information and inuences on neuroendocrine regulatory systems. Both of these organs provide risk management of life history strategy in the face of ecological stochasticity.
Zukowska 2012; Soares et al. 2010). Each of these hormones in turn affects adiposity and metabolic traits such as appetite (Hirsch and Zukowska 2012; Maejima et al. 2011). Thus, the brain contributes to the regulation of life history strategy and does so in response to social and ecological stresses. With respect to adipose tissue, hormones such as leptin and insulin signal the level and consistency of lipid stores to the brain (Benoit et al. 2004) and in doing so affect many life history functions, including reproductive behavior (Cunningham, Clifton, and Steiner 1999; Watve and Yajnik 2007). Preliminary evidence from rodents suggests that levels of adiposity may inuence oxytocin (Flak et al. 2011) and hence potentially social behavior. Thus, while further research is required, it is already apparent that adipose tissue likewise contributes to the regulation of life history strategy and again does so in response to diverse ecological stresses. Clearly these two risk-management systems differ in their receptivity to specic signals, their timescale of response, their degree of exibility, and their functional targets. Together, however, they represent an important link between the level of capital and life history strategy and thereby highlight the importance of capital from an evolutionary perspective.
Capital in Hominins
Reconstructing energy capital dynamics in hominins is at present difcult because of the potential transiency of energy capital per se and the lack of clear markers in the fossil record. Phenotypic exibility to some extent must remain hidden from preservation. Intriguingly, however, both adipose tissue and bone are
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increasingly being reinterpreted as dynamic rather than inert tissues, and growing awareness of endocrine links between these tissues may aid novel interpretation of the fossil record in due course. For example, bone is now known to contribute to the regulation of energy metabolism (Fernandez-Real and Ricart 2011), while leptin mediates skeletal turnover (Ducy et al. 2000). Osteocalcin, which can be recovered from some fossilized material (Nielsen-Marsh et al. 2002), shows an inverse correlation with adiposity in living humans (FernandezReal and Ricart 2011). Further work in this area may generate more robust ndings. Given that both adiposity and social capital vary substantially within and between contemporary human populations, we can assume that they represented dynamic adaptive strategies in Homo evolution, but the details remain to be established (see Wells 2010a for a preliminary estimation of adiposity in prehuman hominins). Both adiposity and social capital enable variation in the mode and breadth of environmental tolerance; that is, they can vary in relation to average environmental conditions (e.g., hot vs. cold climates) but also provide phenotypic exibility to buffer variability in any given environment. Recently, Navarrete, van Schaik, and Isler (2011) reported an inverse correlation across 100 mammal species between brain and adipose tissue masses. These authors suggested that storing information in the brain or energy in the body represent two alternative strategies for accommodating uncertainty in energy availability. The fact that our own species is a positive outlier for both traits offers a powerful indication that ecological stochasticity has been a key stress in the evolution of the genus Homo. In turn, the phenotypic exibility that emerged under such selective pressures appears to have conferred on Homo an extraordinary capacity to colonize new niches (Wells and Stock 2007). The energy capital that provides resilience against tough conditions also favors successful probing of novel niches and demographic expansion as demonstrated by rapid recovery from population crashes (Hill and Hurtado 1996). Through positive feedback loops, colonizing, with its population booms and busts, can become its own selective pressure, as shown in gure 2. Thus, withstanding ecological feast and famine may have made possible reproductive feast and famine. Cooperative breeding is also notable in many social carnivores (Smith et al. 2012), which likewise benet from a social means of buffering individuals risk of failure in capturing prey. According to this perspective, the emergence of energy capital as an adaptive response to ecological uncertainty in early Homo may have opened up carnivory as a new subsistence niche, making use of two types of bet hedging: across individuals (e.g., buffering variance in productivity between individual hunters or gatherers) and across the genders (diversifying the resources harvested by the whole group). Similarly, cooperative breeding may have made possible the funding of larger brains (Hrdy 2009; Isler and van Schaik 2012).
Figure 2. Positive feedback cycle in which the capacity to tolerate stochastic environments promotes the capacity to colonize new environments. Both social and physical forms of energy capital may have provided the necessary phenotypic exibility.
Capital and Transgenerational Effects

As discussed above, capital reduces exposure to ecological stresses and hence to selection, which aids in understanding our species limited local genetic commitment. However, the implications of energy capital in Homo go much further because of the particular sensitivity of developmental trajectory to environmental factors operating in early life. As in most mammals, hominin fetuses must initially experience ecological pressures under the transducing effect of maternal phenotype (Wells 2003, 2007c). Most perspectives on developmental plasticity emphasize how developing offspring adapt to the ecological environment (e.g., Bateson 2001; Kuzawa 2005). Some argue that offspring use environmental cues adaptively by anticipating the future environment in which breeding will occur (Gluckman and Hanson 2004; Gluckman, Hanson, and Beedle 2007). This model ts poorly with the observation that human mothers substantially buffer such cues through both physiological and social mechanisms (Wells 2003), and the anticipatory model has been criticized by several authors (Bogin, Varela Silva, and Rios 2007; Rickard and Lummaa 2007; Wells 2007a, 2011, 2012a). I have argued that given ecological stochasticity, offspring should respond not to short-term external cues but to maternal phenotype, which represents the cumulative effect of an extensive period of time, with short-term uctuations smoothed out to provide a more reliable rating of environmental quality (Wells 2003:152). This smoothing effect was subsequently labeled intergenerational inertia by Kuzawa (2005), but Kuzawas approach, like that of Gluckman and Hanson, does not address the dynamics deriving from parentoffspring conicts of interest (Haig 1993, 1997; Trivers 1974), which these authors reject (Gluckman et al. 2009). Clearly the offspring requires information in order to select a developmental trajectory, but in the absence of direct cues from the external environment, the offspring must use those deriving from maternal phenotype. In accepting such cues, however, the offspring must also submit to maternal strategy (Wells 2003, 2010a), and this strategy is particularly important
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in human life history because it initially falls to the mother to meet the high costs of offspring brain growth (Aiello and Key 2002; Martin 1983, 1989) and to allocate resources between several competing offspring during much of the reproductive career (Wells 2003). Closure of the critical window of physiological sensitivity in early infancy, despite the extended period of growth, results in the canalization of offspring growth trajectory in the second year of life (Smith et al. 1976) and allows the mother to x her own investment strategy in each offspring at the time of weaning (Wells 2003). The cues received by developing offspring before weaning therefore refer not to ecological conditions per se but to the magnitude of maternal capital (Wells 2010a), incorporating both social (i.e., extended phenotype) and physical dimensions. Receiving a given investment of capital need not imply any anticipation of future ecological conditions; it is simply what is available according to maternal resources and investment strategy. If developing offspring adapt to maternal phenotype rather than to ecological conditions, this further emphasizes a lack of long-term commitment in adaptation. Lineages, especially matrilines, may accumulate capital and transfer it across generations (see Smith et al. 2010 regarding transgenerational transmission of body weight in foragers) using the exibility of capital stores to buffer short-term ecological perturbations (Wells 2003, 2010a). Evolutionary models of transgenerational information transfer based entirely on external ecological signals offer insufcient explanation for the existence of phenotypic variability within a population at any given point in time and provide a simplistic model of the process of adaptation. In stochastic environments, developmental strategies selected in early life have a high risk of being maladaptive during some or all of adulthood. These potential costs may be alleviated in part by maternal buffering in early life and in part by reversible phenotypic plasticity subsequently conferred by adiposity and social strategies. Energy capital plays a key role in both processes.
Acknowledgments
I very much appreciate the invitation from Susan Anto n and Leslie Aiello to participate in this workshop and their critical comments on the manuscript as well as the comprehensive discussions with the other participants.
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Conclusions
Accumulating social and physiological capital represents two key modes of phenotypic exibility in which life history decisions may be buffered from ecological stochasticity. The two strategies also contrast in an intriguing way, with one pertaining to the brain and, over evolutionary time, to increasingly purposive strategy formation and the other to physiology, in which energy stores themselves enact strategic decisions across competing biological function. These traits that proved adaptive in resolving ecological uncertainty appear to have given rise subsequently to large brains and the capacity to colonize novel habitats, now recognized as two quintessential human traits. It is arguably such phenotypic exibility and the lack of genetic commitment that maintained modern humans as a single species across diverse ecologies.
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