Mother knows best: Epigenetic inheritance, maternal effects, and the evolution of human intelligence

Developmental Review 26 (2006) 213–242 www.elsevier.com/locate/dr

Mother knows best: Epigenetic inheritance, maternal eVects, and the evolution of human intelligence David F. Bjorklund ¤ Department of Psychology, 777 Glades Road, Florida Atlantic University, Boca Raton, FL 33431, USA Received 10 August 2005; revised 26 September 2005 Available online 19 April 2006

Abstract Contemporary evolution biology has recognized the role of development in evolution. Evolutionarily oriented psychologists have similarly recognized the role that behavioral plasticity, particularly early in development, may have had on the evolution of species, harking back to the ideas of Baldwin (the Baldwin eVect). Epigenetic theories of development provide a framework for interpreting the interacting roles of experience and genetics both in ontogeny and phylogeny and the transmission of nongenetic characteristics across generations (epigenetic inheritance). In mammals in particular, diVerences in maternal behavior may contribute substantially to epigenetic inheritance. Changes in early rearing experiences may have been especially important for humans’ ancestors, leading to the acquisition of symbolic functioning. Such representational changes were most inXuential in social cognition and led to new selective pressures furthering the evolution of symbolic abilities. Research with great apes is presented to suggest that our last common ancestor with chimpanzees likely had the behavioral plasticity and sociocognitive precursors to modify their behavior and cognition via maternal eVects toward a more human-like social intelligence. © 2006 Elsevier Inc. All rights reserved. Keywords: Epigenetic inheritance; The Baldwin eVect; Maternal eVects; Plasticity

Evolutionary developmental psychology is concerned mainly with applying evolutionary theory to achieve a better understanding of human development (see Bjorklund & Pellegrini, 2002; Burgess & MacDonald, 2005; Ellis & Bjorklund, 2005; Geary, 1998; Hernández Blasi & Bjorklund, 2003). However, developmental facts and theory can also be *

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applied to elucidate evolutionary processes (e.g., de Beer, 1958; Gottlieb, 1992; Gould, 1977). Evolution can be viewed not simply as a parade of adult ancestors changing in response to selection pressures over geological time, but as a progression of ontogenies. What evolved, in any species, are patterns of development. In the words of West-Eberhard, “The evolution of the phenotype is synonymous with the evolution of development” (2003, p. 89). Natural selection has had as much inXuence or more on the early stages of development as it has had on later stages, and as a consequence, changes in infant or juvenile phenotypes establish new contexts for further selection. From this perspective, changes in ontogeny, particularly early ontogeny, may have had signiWcant impact on the selection pressures an organism faced, and thus on the eventual evolution of the species. That is, developmental mechanisms responsive to both genetic and environmental inXuences produce phenotypic variation that selection might then act upon. At Wrst blush, there may seem nothing controversial about stating that the ontogeny of a species had an eVect on its phylogeny. However, after only brief reXection one may realize that such a statement is anathema to conventional wisdom in modern biology (or at least was until quite recently). In the middle part of the last century, Darwinian theory was integrated with Mendalian genetics, producing the Modern Synthesis, or neoDarwinism (Dobzhansky, 1937; Mayr, 1942; Simpson, 1944). Basically, natural selection was fused with a genetic theory of inheritance. Darwin himself was stymied by the lack of a coherent theory of inheritance. (His theory of pangenesis was wrong, and he even relied on Lamarck’s idea of inheritance of acquired characteristics.) Although also ignorant of genetic theory, August Weismann in 1892 recognized that biological inheritance could occur only through the germ line. In sexually reproducing species, only information in the gametes was transferred between generations. Changes in the body (somatic cells) could not be inherited and thus could not inXuence evolution (see Fig. 1). The direct implication of this revelation was that development was an epiphenomenon of evolution; it may have great consequences for the individual, but it is inconsequential for phylogeny. Weismann’s insights were quickly adopted by biologists and, particularly with the rediscovery of Mendel’s work in 1900, led to the downfall of nongenetic accounts of inheritance. Lamarck and his theory of acquired characteristics served as a whipping boy for nongenetic theories of evolution. A blacksmith can no more pass along his well-developed musculature to his oVspring as can a bleach-blond her artiWcial-hair color to her children. This eVectively led to the separation of developmental biology and embryology from evolutionary biology. There were occasional theorists over the course of the 20th century who

Phenotype

Genes

Phenotype

Genes

Phenotype

Genes

Fig. 1. Genocentric view of inheritance (from Weismann, 1892 and the canonical view of the Modern Synthesis).

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attempted to integrate (or more appropriately, re-integrate) these two Welds (e.g., de Beer, 1958; Garstang, 1922; Gould, 1977; Montagu, 1962), but for the most part, the two disciplines went their separate ways. And perhaps the greatest insult one could throw at an evolutionary scientist was that he or she was a Lamarckian (closet or otherwise). Although neoDarwinism remains the dominant paradigm in biology, it has begun to incorporate development into evolutionary accounts. The Weld of evolutionary developmental biology, or Evo-Devo, explicitly investigates the role of development (especially developmental genetics) in evolution across a wide range of species (e.g., Carroll, Grenier, & Weatherbee, 2005; RaV, 1996; West-Eberhard, 2003). Psychologists with an evolutionary bent have also entered the picture, proposing that changes in behavior early in development can lead the way to evolutionary changes (e.g., Bjorklund & Rosenberg, 2005; Gottlieb, 1987, 1998, 2002; Harper, 2005; Ho, 1998; Lickliter & Schneider, in press; Oyama, 2000; see papers in Oyama, GriYths, & Gray, 2001). Individuals that display a high degree of behavioral plasticity, deWned as the ability to modify behavior as a result of environmental input, are better able to adapt to novel environments than less plastic individuals. This increased adaptedness permits organisms to enter new environments, where they experience selection pressures that move these individuals in diVerent phylogenetic directions than their less Xexible peers. Such accounts are referred to as epigenetic inheritance, or epigenetic theories of evolution (e.g., Ho, 1998; Jablonka, 2001; Jablonka & Lamb, 1995; Mameli, 2004).1 I begin this article with a discussion of an epigenetic model of gene–environment interaction that describes the emergence of structure and function both in ontogeny and phylogeny. Central to epigenetic theories is the idea that there is substantial plasticity in behavior, particularly early in development. I then examine the role of plasticity in generating novel behavior that can serve as the basis for epigenetic inheritance, focusing initially on the Baldwin eVect. I propose that likely sources of novel phenotypes are maternal eVects—nongenetic inheritance transmitted from mother to oVspring. I argue that such maternal eVects may have been particularly important for our big-brained and symbolusing ancestors, and I provide some evidence from human-reared great apes to bolster my argument. SpeciWcally, I review research showing that enculturated chimpanzees, reared much as human children are reared, display aspects of human social cognition that resemble those shown by human children, and that this suggests that humans’ common ancestor with chimpanzees likely also possessed this degree of cognitive plasticity, which could have paved the way for the evolution of the modern human mind. Epigenesis and the generation of structure and function Epigenesis can be deWned as “an emergent process by which an organism’s structure and function change from relatively undiVerentiated states to increasingly specialized, diVerentiated forms throughout ontogeny” (Miller, 1998, p. 105). From this perspective, one cannot partition biologic from environmental eVects on the organisms, for genes, hormones, neurons, maternal care, and the physical and social environment all contribute dynami1 Jablonka (2001) uses the term Epigenetic Inheritance System to refer to systems underlying (nongenetic) cellular heredity and the term Behavioral Inheritance System to refer to systems responsible for the (nongenetic) transgenerational transmission of behavior. I use the term epigenetic inheritance more generally to refer to any form of nongenetic transgenerational transmission, although most of the examples provided herein would be best classiWed as reXecting Jablonka’s Behavioral Inheritance System.

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Environment1

Environment2

Environment3

Phenotype1

Phenotype2

Phenotype3

Genetic Expression 1

Genetic Expression 2

Genetic Expression 3

Fig. 2. An epigenetic view of inheritance.

cally to produce behavior. Development occurs as the result of the continuous and bidirectional interaction between various components of developmental systems—including, but not limited to genetic activity, structural maturation, activity emanating from structures (or function), and the environment, broadly construed. Genes are not given special privilege, but are viewed as an integral part of a developmental system, with no greater import than other aspects of the system. Gottlieb (1998, 2002) has diVerentiated two types of epigenesis: predetermined and probabilistic. Predetermined epigenesis describes the unidirectional relation between structure and function: genes ! structural maturation ! function (activity and experience). In contrast, Probabilistic epigenesis describes the bidirectional relationship between structure and function. In this relationship, each level interacts with each adjacent level: genes M structural maturation M function, producing increasingly complex organization over the course of development (see Fig. 2). The concept of probabilistic epigenesis may have been controversial in the recent past, but advances in genetics have made it clear that genes are always expressed in some context (i.e., environment). Each somatic cell in an animal’s body contains the full complement of genes, but a diVerent complement of genes may be expressed by speciWc organs, and only a handful are expressed at any one time in development. Genetic activity is determined by the environment in which the genes Wnd themselves, beginning with the cytoplasmic environment provided by the mother’s ovum (DNA cannot “communicate” eVectively with RNA to make proteins without the biochemical machinery that is maternally inherited) and continuing through the broader physical and social environment in which an organism lives. Genes cannot be viewed as the directors of development, with the genome serving as a blueprint for building body and mind. Although this perspective acknowledges the necessary role of genes in inXuencing structure and function, it also recognizes the impotence of genes in the absence of appropriate environmental context. From a probabilistic epigenetic perspective, there should be substantial plasticity in development, which makes the speciWc path that ontogeny will take for any individual nearly impossible to predict.2 How is it, given the dynamic nature of gene–environment interaction, 2

In fact, this has been a criticism by evolutionary psychologists (e.g., Buss & Reeve, 2003; Chiappe & MacDonald, 2005; Tooby, Cosmides, & Barrett, 2003) of one prominent theoretical perspective that advocates such a substantial degree of plasticity, developmental systems theory (Gottlieb, 1992, 1997, 1998, 2002; Lickliter & Honeycutt, 2003; Oyama, 2000; Oyama et al., 2001).

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that members of a species show remarkable resemblance to one another? The reason for this is that an animal inherits not only a species-typical genome but also a species-typical environment. In fact, some aspects of the environment are unvarying (e.g., gravity, patterned light) and are more reliably inherited across generations than are genes. Because of the lack of variation in gravity, for instance, it may play no role in diVerential reproduction and survival, the sine qua non of Darwinian explication; but gravity nonetheless aVects how organisms develop and is a central aspect to the developmental system. With respect to mammals, species-typical environments include gestation in a uterus (with all the attendant prenatal “experiences” that entails), a lactating mother, and, for social species, interactions among conspeciWcs over the course of ontogeny. It is the inheritance of a species-typical environment as well as a speciestypical genome that produces reliably developing organisms of any species. Nonetheless, should a critical part of the species-typical environment be changed, while holding genes constant, one should witness species-atypical form or function. Although it is impossible for an organism to experience an inWnite range of environments to determine the phenotypic outcome in each, it is not reasonable to expect a genome to be responsive to an overly broad range of environments. Ontogeny is constrained both by genes and environment. Gene–environment relations are highly structured and conserved over evolution, and as a result, predictable patterns of ontogeny emerge. Furthermore, although all behavior emerges via the bidirectional relation between genes and experience (broadly deWned), some aspects of behavior are more highly canalized than others, emerging in all but the most extreme conditions (the absence of gravity, for instance, see Ronca & Alberts, 2000), whereas others display a higher degree of plasticity. For example, consistent with the tenets of mainstream evolutionary psychology, Geary (2005a, 2005b, Geary and HuVman, 2002) proposed that information-processing mechanisms that evolved to deal with invariant aspects of the environment should be domainspeciWc and modular in nature and expressed in a reliable way in most environments. Yet, when environmental conditions are variable, more domain-general and plastic mechanisms should also evolve, enabling an individual to modify its behavior in reaction to an unpredictable environment (see also Bjorklund & Pellegrini, 2002; Chiappe & MacDonald, 2005). In a similar vein, Bjorklund, Ellis, and Rosenberg (in press) introduced the concept of evolved probabilistic cognitive mechanisms, deWned as information-processing mechanisms evolved to solve recurrent problems in ancestral environments. However, consistent with an epigenetic viewpoint of development, these mechanisms are expressed in a probabilistic manner in each individual, based on the continuous and bidirectional interaction over time at all levels of organization, from the genetic through the cultural. These mechanisms emerge in a species-typical fashion when an individual experiences a species-typical environment, but are subject to modiWcation as a result of perturbations in development. In each of these accounts, some part of an individual’s genome is sensitive to some features of the external environment at particular times in development. Although the course of development is highly predictable for some aspects of behavior, it is dependent on species-typical experiences (i.e., experiences and environments similar to those experienced by ancestral generations) for its expression. Moreover, in addition to the existence of domain-general abilities, there is plasticity within the modular domains (at least in humans), which aVords substantial cognitive and behavioral Xexibility for an organism living in environments that vary over lifetimes and generations (see Geary, 2005a). Such plasticity may also provide the raw material upon which natural selection can work and evolutionary change is realized.

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Plasticity and morphological change The genomes of many animals show truly amazing plasticity, at least from the typical mammalian perspective. For example, whereas male and female mammals are diVerentiated genetically/chromosomally (i.e., XX for females, XY for males), for some reptiles, sex is determined by the temperature at which eggs are incubated (Bull, 1980). Temperature also determines the camouXaging pattern on the wings of some butterXies. For example, the butterXy Bicyclus anynana develops wings with many eyespots in the warm, wet season, which helps it blend into the lush summer environment. Animals from this same species develop wings with fewer or no spots in the cooler, dry season, which helps them blend into the mostly brown leaf litter (BrakeWeld et al., 1996); laboratory research has shown that butterXies raised at lower temperatures express fewer proteins associated with the gene (Distal-less) responsible for eyespots (described in Carroll, 2005). In some Wsh, the composition of the social group is the proximal stimulus for animals to change their sex from female to male (Black & Grober, 2003). Other animals develop radically diVerent morphologies depending on their early diet. For example, the moth Nemoria arizonia lays its eggs on oak trees. Based on its diet during the Wrst few days after hatching, the caterpillars develop one of two morphologies. The spring brood feeds on oak catkins and quickly comes to resemble the catkins, whereas the summer brood feeds on oak leaves and resembles oak twigs. In each case, their morphology helps them blend in with their surroundings, protecting them from predators (Greene, 1996). In all of these examples, genetically identical organisms develop morphologies based on diVerences in their environment. Some genes evolved to be sensitive to variations in a particular aspect of the environment that has been associated with success during the species’ natural selective history, what Boyce and Ellis (2005) refer to as conditional adaptations. The products of speciWc genes determine the morphology of animals, but it is variation in the environment, not in the genome, that is responsible for important aspects of an animal’s physical self. Plasticity of behavior Some clear examples of developmental behavioral plasticity, speciWcally of how alterations of species-typical experiences can modify species-typical behavior, can be seen in research in auditory learning in birds. For example, although precocial birds (e.g., ducks, geese, and quail) typically approach the maternal call of their species shortly after hatching, research has shown that auditory experience in the egg is necessary for such “imprinting” to occur (e.g., Gottlieb, 1997), and that post-hatching approach behavior can be aVected by prehatching perceptual experience. For instance, bobwhite quail who receive visual stimulation while still in the egg fail to show a preference for their species’ maternal call (Lickliter, 1990), or for a call they heard while still in the egg (Lickliter & Hellewell, 1992). The “unexpected” visual stimulation competed with the auditory stimulation these animals typically receive, interfering with development (Turkewitz & Kenny, 1982). Normally, neurological maturation and perceptual experience are coordinated, with sensory input being correlated with gene-inXuenced maturation. When the timing of sensory experiences and aspects of neurological maturation are uncoupled, the system is perturbed and species-atypical development results. In other cases, precocial birds that hear the calls from other avian species prior to hatching, approach the call of that species instead of the call of

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a conspeciWc, illustrating the plasticity of what is traditionally viewed as “instinctive” behavior, and reXecting the role of embryonic auditory experience on post-hatching behavior (see Gottlieb, 1997). Other examples come from research with parasitic songbirds that lay their eggs in the nests of other species. Parasitic birds need to learn in which hosts’ nests to lay their eggs. Such imprinting is not “in the genes,” but, in some species such as the whydahs (Vidua macroura), is accomplished by the nestlings identifying the markings of their foster parents (i.e., the birds that feed them) so that, as adults, they “know” in which nests to lay their eggs. But females must also identify a mate that was raised by the same host species, insuring their oVspring will have the right markings so the host will feed them. This is accomplished in the whydahs via auditory imprinting. The song of the male whydahs consists of two parts, one of which is based on the vocalization of the host species. As a nestling, the female whydahs are imprinted to the foster-father’s song, so when it is time to mate, she selects a male whydahs with the “right” song (see Avital & Jablonka, 2001). Again, a pliable learning system, sensitive to particular aspects of the environment, permits these animals to identify with the “right” host species and also to know which members of their own species are suitable mates. An example of plasticity helping animals deal with rapidly changing environments comes from recent research with great tits (Parus major) from the Netherlands (Nussey, Postma, Gienapp, & Visser, 2005). The birds feed on caterpillars, which, due to global warming, have been appearing about two weeks earlier than they did 20 years ago. Most birds, therefore, hatch too late to feed on the caterpillars, and as a result fewer oVspring survive. Some females, however, eVectively timed their reproduction so their chicks hatched when the caterpillars were most plentiful, and as a result had twice as many oVspring as those birds not able to adjust their reproduction to the changing environment. Data from this population have only been collected for 32 years, precluding any statement about the long-term consequences of the role of phenotypic plasticity on survival; but the results indicate that individuals more able to modify their reproductive behavior produce broods that are in synchrony with the food supply. This suggests that reproductive plasticity may be favored by natural selection and increase in frequency in future generations. Plasticity is not limited to birds, of course, but is also witnessed in mammals, including primates and humans. For instance, classic research by Suomi and Harlow (1972) demonstrated that monkeys raised in social isolation for 6-months—a context that usually results in permanent social/emotional and sexual dysfunction—could be rehabilitated, given the “right” therapist. In this case, the successful therapist was a 3-month-old group-reared monkey, who interacted with the isolate for an hour every day, breaking down the isolate’s self-directed behavior and later facilitating the development of normal social interaction. Analogously, research with children who spent their Wrst years in stultifying institutions has shown that, when adopted, they often show remarkable recovery of intellectual and social/emotional functioning (e.g., JuVer & IJzendoorn, 2005; O’Connor et al., 2000; Skeels, 1966). This plasticity is aVorded by an immature brain that continues to grow at a rapid rate and to modify its synaptic patterns well into childhood (e.g., Greenough, Black, & Wallace, 1987; Johnson, 1998, 2000). (Human brains continue to be plastic into adulthood, of course; but the extent to which the eVects of deleterious early experience can be reversed is lessened with age, see O’Connor et al., 2000.) But plasticity is not inWnite. Development also constrains some outcomes, so that once a course has been traveled, alternative pathways are blocked. This is easily seen in early

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morphological development; for example, the generation of four limbs makes it unlikely that subsequent limbs can be added or deleted. Even whales, for instance, possess vestigial hind limbs. It is also true for behavior. Once behavioral patterns have been established early in development, they can be diYcult to reverse, or in the words of Scott (1968), “organization inhibits reorganization.” These developmental constraints are also a result of the dynamic interaction of genes and environment. Gene–environment interactions Most examples I have provided to this point of gene–environment interaction come from studies of nonhuman animals and focus on the prenatal or perinatal periods of life. Researchers and theorists primarily concerned with human development have also assumed that genes and rearing environments interact dynamically to produce postnatal behavior, but unimpeachable scientiWc evidence for such interactions for important human psychological characteristics are hard to come by, mainly because of the diYculty of isolating speciWc genes and/or identifying speciWc environments. An exception is work by Caspi and his colleagues (2002, 2003). In one study, Caspi et al. (2002) examined the relationship between childhood maltreatment and the possession of a particular allele for the enzyme Monoamine oxidase A (MAOA). MAOA metabolizes several types of neurotransmitters, and levels of MAOA, which are governed by diVerent alleles of a gene located on the X chromosome, have been shown to be associated with levels of aggression (low levels of MAOA are associated with high levels of aggression). Data from a New Zealand sample indicated that boys with low MAOA levels showed elevated amounts of antisocial behavior, but only if they experienced maltreatment in childhood. Levels of antisocial behavior for boys with low levels of MAOA were actually slightly below those of boys with high MAOA levels when the children came from homes without maltreatment. In another study, similar patterns were found between children who had variants of the 5-HTT Serotonin transporter gene, childhood rearing environment, and depression (Caspi et al., 2003). There was no relation between recent depression and earlier maltreatment for individuals with one version of the gene (LL). In contrast, there was a relation between childhood maltreatment and depression for individuals with either the LS or SS version of the 5-HTT gene, with children experiencing stressful early environments being more likely to report depressive episodes in young adulthood than those not experiencing stressful early environments (see also Ellis, Jackson, & Boyce, this issue; Flinn, this issue). These Wndings are consistent with the position that patterns of child rearing moderate genetic eVects, altering the phenotype and possibly setting up new gene–environment relationships that, potentially, could be maintained over generations (see discussion below). As important and groundbreaking as these studies are, they are still correlational in nature. Children do not choose to be in abusive homes, and parental behavior may naturally vary with genotype, obfuscating actual gene–environment interactions. Such confounds can be overcome using animal studies, and research by Steven Suomi and his colleagues has addressed these issues working with rhesus monkeys (see Suomi, 2004 for review). In one line of research, Suomi and his colleagues investigated the relation between diVerent alleles of the 5-HTT gene (LL, or “long” allele, versus LS, or “short” allele), aggression, and patterns of mothering (Bennett et al., 2002). Peer-raised monkeys (i.e., raised without a mother) showed high levels of aggression if they possessed the LS allele,

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but not if they possessed the LL allele. No relation was found between allelic variation and aggression for mother-reared monkeys, suggesting a maternal-buVering eVect. Similar maternal-buVering eVects for possessing the short version of the 5-HTT allele were reported for hypothalamic–pituitary–adrenal (HPA) responses to social separation (Barr et al., 2004) and for neonatal neurobehavioral development (Champoux et al., 2002). Suomi (2004) suggested that these and related Wndings have considerable implications for the potential cross-generational transmission of certain biobehavioral characteristics. Earlier research had shown that maternal attachment behavior is transmitted across generations, even when monkeys are foster reared (Suomi, 1999). If maternal behavior can mediate genetic eVects across generations, “then having had mothers develop a secure attachment relationship with their own mothers when they were infants themselves might well provide the basis for a nongenetic means of transmitting its apparently adaptive consequences to that new generation of monkeys” (Suomi, 2004, p. 218). The Baldwin eVect and epigenetic inheritance Epigenetic theories of evolution view a developing organism’s response to environmental changes as a mechanism for phylogenetic change. Natural selection still plays an important role in evolution, but it is the developmental plasticity of an organism that provides the creative force for evolution (e.g., Gottlieb, 1987, 2002; Lickliter & Schneider, in press; West-Eberhard, 2003). According to West-Eberhard (2003), “New phenotypic subunits begin and evolve as products of developmental plasticityƒ They originate when an environmental or genetic perturbation causes a shift in gene expression, and they are consolidated under selection for improved regulation and form” (p. 129). From this perspective, natural selection serves not as the generator of novelty, but as sieve through which novel phenotypes (or neophenotypes, Kuo, 1976) must pass. Developmental variation and natural selection are sometimes erroneously seen as competing explanations for evolved form but should rather be viewed as two aspects of a single process (West-Eberhard, 2003). A combination of genetic and experiential inXuences create variation in developing phenotypes, and if individual diVerences in these phenotypes are correlated with individual diVerences in survival or reproductive outcomes, then the genes that responded to these developmental experiences will increase in frequency as a result of this selective advantage. In other words, any mechanism, including developmental experiences, that results in phenotypic variation creates the grist upon which natural selection acts. Variants of such theories have been around since the latter part of the 19th century (e.g., Baldwin, 1896, 1902) and surfaced from time to time over the last century (e.g., Bateson, 1988; Gottlieb, 1987; Wyles, Kunkel, & Wilson, 1983). Until recently, however, mainstream evolutionary biologists have been reluctant to take such proposals seriously, fearing the specter Lamarckism. The oldest and most familiar account of this type is known as the Baldwin eVect, proposed in the last decade of the 19th century by psychologist James Mark Baldwin. (The ethologist Conway Lloyd Morgan and the paleontologist H.F. Osborn simultaneously made similar proposals, but it is Baldwin’s name that became associated with the theory, see Depew, 2003.) Baldwin proposed that animals could contribute to their own evolution via learning, particularly in social settings. Animals that had suYcient plasticity to acquire new behaviors in response to new environments would be better adapted than their less-plastic brethren. These better-adapted animals would presumably breed with one another, and, so long as the precipitating environment remained stable, their

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oVspring would continue to have a selective advantage. Eventually, through a process he termed organic selection, the once-acquired behavior would become part of the genetic make-up of the animal and expressed in all members of the population. Thus, high levels of behavioral plasticity generate adaptive behavior that are selected for over generations but eventually lose their plasticity and are expressed inXexibly. More than half a century later, the British biologist Conrad Waddington demonstrated experimentally that a characteristic initially elicited only by extreme environments (e.g., lack of veins in the wings of fruit Xies as a result of heat shock) could be expressed in later generations of selectively bred Xies in the absence of the originally invoking stimulus: after 14 generations of Xies exposed to heat shock and selectively breed for survival and the absence of veins in the wings, the no-vein phenotype was expressed in the absence of heat shock (see Waddington, 1975). A trait that had originally been expressed only under stressful conditions was now expressed in the absence of environmental stressors. Waddington referred to this phenomenon as genetic assimilation. (For other examples and replications of Waddington’s work, see Waddington, 1975 and Gibson & Hogness, 1996). The explanation typically provided for these phenomena is that organisms possess substantial unexpressed genetic variability. Extreme or novel environments activate some latent genes (or perhaps de-active genes, or cause some genes to become expressed earlier, later, or for diVerent durations), resulting in novel morphology (as in Waddington’s fruit Xies) or novel behaviors (as in Baldwin’s proposal).3 With respect to behaviors, animals put themselves in new organism-environment relationships, which may include invasions of new territory, geographic (or perhaps social or sexual) isolation, and the expression of latent physiological or morphological characteristics (e.g., Gottlieb, 2002), all of which provide new selection pressures. Selection favors those individuals with the genetic potential to respond to the new environment with adaptive phenotypes, that is, phenotypes that improve survival or reproductive prospects. Individuals with the adaptive phenotypes increase in frequency and thus the genes that provided the initial potential to create these phenotypes increase in frequency within the population exposed to the new environment. When the environments that initiated behavioral change remain stable over many generations, the behavioral neophenotypes will continue to be well-adapted, perhaps Wlling or constructing new niches and exposing themselves to new selection pressures, prompting further ontogenetic adaptations, and, eventually, phylogenetic changes (Laland, Olding-Smee, & Freldman, 2000; Lewontin, 1982; Odling-Smee, 1988). According to Gottlieb (1987, 1992, 2002), changes in behavior as a result of responses to novel environments are frequently the Wrst step in evolutionary change, preceding genetic change (see also West-Eberhard, 2003). One reason for the appeal of the Baldwin eVect to some people has been the possible inclusion of mind (or at least self-initiated behavior) as an engine of evolutionary change. Learning, and presumably cognition, could aVect the direction of evolution, all within the broader paradigm of Darwinian evolution by natural selection. Perhaps the contemporary theorist to best articulate this position with respect to human cognitive evolution is Terrance Deacon (1997, 2003). Deacon argues that the advent of symbolic representation 3

Although controversy persists about the role that Baldwinian-type changes may play in evolution, many evolutionary biologists agree that the Baldwin eVect is not inconsistent with the fundamental principles of the Modern Synthesis (see Weber & Depew, 2003). In fact, Dawkins (2004) of SelWsh Gene fame refers favorably to the Baldwin eVect in his recent book The Ancestor’s Tale.

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brought about new selection pressures that aVected hominid brain evolution. As Baldwin and more contemporary advocates of epigenetic evolution (see Weber & Depew, 2003), Deacon proposed that behaviorally Xexible animals were able to move into new niches that provided novel selection pressure for them and succeeding generations. With respect to human evolution, Deacon proposed that “Stone and symbolic abilities, which were initially acquired with the aid of Xexible ape-learning abilities, ultimately turned the table on their users and forced them to adapt to a new niche opened by these technologies. Rather than being just useful tricks, these behavioral prostheses for obtaining food and organizing social behaviors became indispensable elements in a new adaptive complex” (1997, p. 345). The central premise of the Baldwin eVect is that behavioral plasticity leads to adaptive behavior that, over generations in a stable environment, becomes inXexibly expressed in all members of the population. Somewhat ironically, the end result is a loss of plasticity. Presumably, the adaptation was of suYcient import that making its expression a species default provided greater beneWts than maintaining the initial level of plasticity. One can easily imagine how the canalization of some aspects of language, for example, would beneWt an individual, being acquired in all normal members of the species under species-typical conditions, rather than being dependent upon a highly speciWc environment for its expression. But rather than aVording less plasticity, Deacon notes that the genetic assimilation (to use Waddington’s term) of human symbolization and language actually provided greater plasticity. This is because what evolved were not adaptations aimed at solving speciWc problems, but adaptations that enhanced representation and learning—that permitted new means of understanding and acquiring information about the physical and social world. According to Deacon (1997), “Once symbolic communication became even slightly elaborated in early hominid societies, its unique representational functions and openended Xexibility would have led to its use for innumerable purposes with equally powerful reproductive consequences” (p. 349). Although not explicitly invoking a Baldwinian interpretation, Jesse Bering and his colleagues (Bering, in press; Bering & Bjorklund, in press; Bering & Shackelford, 2004) recently proposed that the advent of self-awareness (i.e., metarepresentational abilities as reXected in language and theory of mind) aVorded new selection pressures resulting in a suite of novel adaptations. In particular, Bering proposed that the abilities to represent the behavior and minds of others and to communicate via language made ancient adaptive heuristics for selWsh behavior often in need of censoring because of the necessity to avoid detection and to protect one’s reputation (cf. Geary, 2005a). More speciWcally, behavior that may have beneWted our simian ancestors, such as stealing resources from a weaker conspeciWc, sexual coercion, or even killing a competitor, becomes maladaptive if one has the chance of becoming “found out.” For example, a chimpanzee that forcibly takes food from another, weaker chimpanzee, has no fear that his transgression will be reported or that he will suVer for his “crime,” because the aggrieved party does not have the representational or communicative abilities to inform allies about what transpired. With symbolic representation and language, the victim can relate his tale of woe to friends and family and make the wrongdoer pay, or at least impinge the reputation of the thief. In a social species such as humans, such a soiling of one’s reputation could have negative Wtness consequences. To deal with the problems that symbolic representation wrought, new adaptations were needed associated with (1) the inhibition of previously adaptive behavior, such as sexual coercion, (2) “social” emotions, such as shame and guilt, (3) morality, (4) confession, and (5) spirituality/religion, among others. Bering’s ideas are

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consistent with those of Deacon and the position that self-generated cognition served as a spur to intellectual evolution in the line that led to Homo sapiens. Along similar lines, Richardson and Boyd (1976; 2005; see also Flinn, 1997) have argued that humans have two evolving systems of inheritance: genetic and cultural. Natural selection operates on culture as surely as it operates on genes to produce human behavior. They propose that genetic evolution favored the emergence of social learning, particularly imitation, in human ancestors, which permitted the development of cumulative cultural evolution, which they deWne as “behaviors or artifacts that are transmitted and modiWed over many generations, leading to complex artifacts and behaviors” (Richardson & Boyd, 2005, p. 107). Cumulative cultural evolution can result in increasingly complex adaptations more rapidly than natural selection working on genetic variability, yielding to increasingly complex social and technological societies. Such adaptations, they propose, were particularly important in adjusting to the variable environments of the late Pleistocene, and were responsible for humans becoming the most successful large mammal during this time and their eventual ecological domination of the Earth (cf. Alexander, 1989). Humans are not the only animals to pass information from one generation to the next. Comparative biologists and psychologists have labeled the nongenetic transmission of behavior across generations as traditions (see Fragaszy & Perry, 2003). Examples include stripping pine cones for seeds in black rats (Terkel, 1995, see below) and potato washing in Japanese macaques (Kawai, 1965), among many others. Other species, such as dolphins (Rendell & Whitehead, 2001), orangutans (van Schaik et al., 2003), and especially chimpanzees (Whiten et al., 1999) have been shown to transmit a variety of diVerent behaviors across generations, causing some to claim that these species possess “culture.” Although these observations are impressive and make it clear that humans are not the only animal on the planet to pass along its wisdom from one generation to the next, no other animal transmits culture across generations to the extent that humans do, causing Richardson and Boyd to suggest that cumulative cultural evolution may be found only in H. sapiens and attributable to our species’ unique social-learning abilities. (I’ll have more to say about social learning in chimpanzees versus humans below). Maternal eVects There are many paths that epigenetic inheritance can take, of course, but one of them, especially in species with extended infancies or juvenile periods, is via maternal eVects.4 Most mammals and birds, in particular, are highly dependent upon their mothers for care early in life, when plasticity is most pronounced. Mothers act as a buVer or Wlter (for food in mammals quite literally) by which their oVspring experience the external environment. Mothers’ interactions with their oVspring can be viewed as an important part of the developmental system, inXuencing and being inXuenced by their oVspring. In fact, because mothers of some species provide so much of the early environment for their oVspring, their 4

I focus here on mothers because in most mammal females provide the bulk of care to infants, with fathers interacting little, if at all, with their oVspring. Human males are one of a handful of exceptions, and it is likely that they have contributed substantially to nongenetic inheritance via social learning, cf. Richardson and Boyd, 2005, see discussion above. However, even in humans, females have traditionally provided the greatest amount of care to oVspring (Hrdy, 1999), and it is likely that maternal eVects have had greater consequences on epigenetic inheritance in mammals than paternal eVects.

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Maternal Behavior 1

Maternal Behavior 2

Maternal Behvior 3

Phenotype1

Phenotype 2

Phenotype 3

Genetic Expression 1

Genetic Expression 2

Genetic Expression 3

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Fig. 3. Maternal eVects on inheritance.

contribution to heritable variance exceeds 50% (Moore, 2003), and correlations between maternal and oVspring phenotypes are typically greater than between paternal and oVspring phenotypes (Moore, 1995). Fig. 3 is a slightly modiWed version of the earlier Fig. 2 and illustrates how maternal eVects can be viewed from a probabilistic epigenetic perspective, especially early in life. There is a bidirectional relation between the oVspring (represented as the phenotype) and both its genotype (genetic expression) and its mother (maternal eVects). Maternal contribution to oVspring phenotype It hardly seems worth saying that “mothers matter.” Research and various theoretical traditions within developmental psychology have emphasized the role of mothers in psychological development, and natural experiments have demonstrated the deleterious eVects on children when they are deprived of mothers (e.g., Hrdy, 1999; Rutter, 1999; Spitz, 1945). Experimental work by Harlow and Zimmerman (1959) with rhesus monkeys illustrated the devastating eVects that being reared without a mother can have. Within the child development literature, maternal diVerences in style of attachment, discipline, and intellectual stimulation, among others, have been shown to be related to subsequent social, emotional, and cognitive functioning (e.g., Baumrind, 1993; Bradley, 1989; Fagot, 1997; Kochanska, 2001; SameroV, Seifer, Baldwin, & Baldwin, 1993), although environmental eVects can rarely be interpreted independently of potential genetic eVects (see Harris, 2005). Maternal eVects begin prenatally. Mammalian fetuses are exposed to a host of agents including hormones, toxins, immune factors, and nutrients, all of which can aVect their development. For example, the postnatal gustatory preferences of a rat are inXuenced by the diet of its mother when she is pregnant (e.g., Terry & Johanson, 1996), as is a pup’s initial attraction to its mother’s nipples (e.g., Teicher & Blass, 1977). Prenatal hormone exposure inXuences morphology, physiology, and behavior. For example, female rodents that are downstream or next to male rodents are exposed to greater amounts of testosterone than female rodents downstream or next to other females, and as a result show more masculine morphological and behavioral characteristics (e.g., Clark & Galef, 1998; Clemens, Glaude, & Coniglio, 1978). Perhaps of greater interest for most psychologists are postnatal maternal eVects. Some sex diVerences in rats have been traced to diVerences in maternal behavior toward their pups (see Moore, 1995, 2003). For example, mothers engage in anogenital licking more

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with their male pups than with their female pups (Moore & Morelli, 1979). There seems to be a number of reasons for this diVerence, including the fact that the dam is more attracted to the odor of male urine than female urine; male pups produce more urine than female pups; and male pups assume a posture that promotes licking. When experiments are conducted to reduce maternal licking, as adults, males are less likely to perform intromissions and the penile reXexes observed in sperm competition (Moore, 1995). Transmission of novel feeding behavior from mothers to oVspring has been observed in a population of black rats (Rattus rattus). Aisner and Terkel (1992) observed rats in an Israel forest stripping pine cones to get the nutritious seeds, an activity that had never been previously observed in rats. In the laboratory, they noted that 31 of 32 pups of mothers who stripped pine cones also learned to strip pine cones. They then performed a cross-fostering study, placing rat pups born to mothers who did not strip pine cones with mothers who did, and vice versa. They reported that the pups displayed the feeding behavior of their foster mothers, independent of which mothers had given them birth, conclusive evidence of the transmission of a novel feeding behavior via nongenetic maternal inheritance (see also Terkel, 1995). In rats, licking/grooming (LG) is highly associated with arched-back nursing (ABN), in which the dam arches her back and splays her legs outward during nursing. Researchers have demonstrated that individual diVerences in levels of LG–ABN by dams are associated with a host of behavioral and physiological characteristics in their oVspring as adults, especially those related to responses to stress (e.g., Caldji et al., 1998). OVspring of dams displaying high levels of LG–ABN show less fear of novelty compared to oVspring of dams displaying low levels of LG–ABN. The behavioral diVerences are accompanied by diVerences in HPA responses, including gene expression associated with corticotropin-releasing hormone receptors (Caldji et al., 1998; Francis, Diorio, Liu, & Meaney, 1999; Weaver et al., 2004; see Ellis et al., this issue; Meaney, 2001 for reviews). Cross-fostering studies have shown that placing rat pups whose genetic mothers showed low levels of LG–ABN with dams who showed high levels of LG–ABN produced animals low in stress, consistent with their foster mothers’ phenotype (e.g., Francis et al., 1999; Francis, Szegda, Campbell, Martin, & Insel, 2003; Liu, Diorio, Day, Francis, & Meany, 2000). Such Wndings suggest that maternal behavior can alter the temperamental characteristics of rat pups, perhaps buVering a potentially maladaptive genetic disposition, or even fostering a novel adaptive phenotype that may persist over several generations.5 Nongenetic maternal inheritance Nongenetic maternal inheritance starts with the egg. In mammals, a father contributes his sperm with the haploid number of chromosomes that will be matched by the mother. This nuclear DNA is what is typically referred to as “genetic inheritance.” Whereas this is 5

I do not see the present position as being contradictory with the views of theorists who propose that parents play a relatively minor role in individual diVerences in children, compared with peers or their own genome-inXuenced activities (e.g., Harris, 1995; Scarr, 1992). Mothers are but one of many inXuences on ontogeny, and it is possible that individual diVerences in mothers, or parenting, may not account for as much variance in some individual diVerences in personality or intelligence as other factors. However, the near-species-universal experiences associated with having a mother have a profound impact on development (compared with not having a mother), and it is likely maternal-related experiences outside the typical species range (i.e., those that are not just “good enough”) impact development in a way that may produce novel phenotypes.

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the extent of the father’s contribution, the mother contributes the considerable cytoplasm of her egg, including organelles, such as mitochondria, that constitute the chemical machinery that is required for DNA–RNA–protein transcription to occur. The mitochondria, the “power generator” of cells, have their own DNA that is passed from generation to generation from mothers to oVspring. Experiences of a female animal can aVect the cytoplasm of her ova and can potentially be transmitted to subsequent generations, constituting a form of nongenetic inheritance. For example, the water Xea Daphnia cucullata grows a protective helmet when in the presence of the larva of predators. The oVspring and grandoVspring of these asexually reproducing animals also grow the helmet even when they are not exposed to a predator-spiked environment (Agrawal, Laforsch, & Tollrian, 1999; for other examples of epigenetic inheritance in asexually reproducing species, see Jablonka & Lamb, 1995). In research with fruit Xies, females aVected by a stressor (exposure to ether producing two sets of wings) passed the novel phenotype to their oVspring, whereas aVected males did not (Ho, Tucker, Keeley, & Saunder, 1983). The most parsimonious interpretation of these Wndings is that chemicals in the cytoplasm of the females were responsible for the observed transgenerational eVect. In a recent study with rats, pregnant females were given a toxin that interfered with normal sex determination in their male fetuses. AVected male rats showed sperm cell defects and reduced sperm number and motility. These maternal eVects were observed through four generations, and did not decrease over subsequent generations. The eVects were attributed not to modiWcation of nuclear DNA, but to alterations in the chemical machinery (DNA methylation, in which molecules bind selectively to segments of DNA and thereby silence it), an example of epigenetic transgenerational inheritance (Anway, Cupp, Uzumcu, & Skinner, 2005). Nongenetic maternal inheritance in mammals based on postnatal behavior has also been demonstrated, with initial reports dating back to the 1960s. For instance, handled rats had more active and lighter grandoVspring than nonhandled rats when the second generation (i.e., the oVspring of the handled rats) was given the opportunity to explore their environment (Denenberg & Rosenberg, 1967). In a cross-fostering study, learning performance was greater for rats of either the C57BL or BALD strain when they were raised by BALD dams, and this eVect persisted over subsequent generations (Ressler, 1966). Ressler was not able to identify the mechanism responsible for the transgenerational eVect (possibilities included unobserved inXuences on behavior, physiology, or milk content), but suggested that “a nongenetic system of inheritance based upon transmission of parental inXuences is potentially available to all mammals” (p. 267). Perhaps the best experimental evidence for epigenetic transgenerational eVects based on maternal behavior in mammals comes from a cross-fostering study by Francis et al. (1999). As I noted earlier, maternal licking and grooming and arched-back nursing (LG–ABN) varies among dams and is associated with individual diVerences in behavioral and HPA-stress responses in their oVspring. OVspring of dams who engage in high levels of LG–ABN are less stressful than oVspring of dams who engage in low levels of LG–ABN, and this is mediated by changes in gene expression (see Meaney, 2001). Francis et al. (1999) cross-fostered oVspring born of low-LG–ABN mothers to high-LG–ABN mothers, and vice versa. The oVsprings’ reactions to stress were similar to that of their foster mothers, not of their biological mothers. The second generation of females then served as foster mothers. These mothers displayed levels of LG–ABN characteristic of their own foster mothers, regardless of their genotype, and their oVsprings’ responses to stress varied depending on the level of LG–ABN

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their foster mothers displayed. In other words, genetic diVerences associated with LG–ABN behavior and responses to stress were moderated by the activities of foster mothers, and this eVect persisted over at least two generations (a third generation was not assessed). Francis and her colleagues (1999) concluded that, “Individual diVerences in the expression of genes in brain regions that regulate stress reactivity can be transmitted from one generation to the next through behaviorƒ The resultsƒ suggest that the mechanism for this pattern involves diVerences in maternal care during the Wrst week of life” (p. 1158). This led Meaney (2001) to suggest that “Individual diVerences in behavioral and neuroendocrine responses to stress in rats are, in part, derived from naturally occurring variations in maternal care. Such eVects might serve as a possible mechanism by which selected traits are transmitted from one generation to another” (p. 1170–1171). Optimal stress reactions vary in diVerent environments (see Boyce & Ellis, 2005), and variations in maternal behavior, as well as genetically related diVerences in neuroendocrine responsivity to stress, may help mediate the development of adaptive behavior, which may then become the target for natural selection. Epigenetic inheritance and the emergence of human social cognition The Wndings that maternal care may contribute to nongenetic transgenerational inheritance with respect to stress response provide some of the most compelling evidence for epigenetic inheritance in mammals. However, such eVects seem distant to the Baldwin eVect, in which changes in learning, not temperament, bring about adaptive change to novel environments, potentially contributing to phylogenetic change. What about cognition? Might developmental plasticity and maternal behavior have inXuenced the evolution of learning and complex cognition, particularly in the line that led to humans? Big brains and evolution Some proponents of epigenetic inheritance have suggested that evolution should be more rapid in big-brained than smaller-brained animals (e.g., Dennett, 1991; Gottlieb, 1992). Large brains relative to body size are associated with increased learning ability and plasticity. Such animals are more readily able to adapt to new environments, may construct new niches, experience novel selection pressures, and display faster evolution. Dennett (1991) suggested that “species with plasticity will tend to evolve faster (and more ‘clearsightedly’) than those without it” (p. 186). Empirical evidence for this position comes from research relating phylogenetic changes from the fossil record with average relative brain size in seven groups of animals (Homo, hominoids, songbirds, other mammals, other birds, lizards, frogs and salamanders; Wyles et al., 1983). The correlation between relative brain size and rate of anatomical change for these seven taxonomic groups was .97; groups of animals with larger relative brain sizes (Homo, hominoids, and songbirds) showed a higher rate of anatomical change than groups of animals with smaller relative brain sizes (salamanders, frogs, and lizards). According to Wyles et al. (1983), animals that acquire new skills will use them “to exploit the environment in a new wayƒ [The] nongenetic propagation of new skills and mobility in large populations will accelerate anatomical evolution by increasing the rate at which anatomical mutants of potentially high Wtness are exposed to selection in new contexts” (p. 4396). My colleagues and I have made the argument that human intelligence evolved as a result of the conXuence of three factors: a large brain, an extended juvenile period, and life

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in a socially complex group (Bjorklund & Bering, 2003a; Bjorklund, Cormier, & Rosenberg, 2004; Bjorklund & Pellegrini, 2002; Bjorklund & Rosenberg, 2005). Because this theme has been presented elsewhere, I will not elaborate on it here, but only brieXy state the argument. Large brains are associated with greater learning ability, but such brains take time to develop. Human brains continue to grow and remain plastic well into the second decade of life, and this extended neural plasticity is responsible for the behavioral and cognitive Xexibility characteristic of our species. Although there have been numerous theories about the “causes” for the evolution of human cognition, many contemporary theorists have focused on the need to deal with conspeciWcs as the primary impetus (e.g., Alexander, 1979; Bjorklund & Harnishfeger, 1995; Byrne & Whiten, 1988; Dunbar, 1995; Geary, 2005a; Geary & Flinn, 2001; Humphrey, 1976). Having to cooperate and compete with others who could communicate about the past, present, and future and who understood that people’s behavior was governed by what they knew and what they wanted, served as a potent selection pressure for enhanced social cognition. Consistent with this position, in a review of approximately 1000 published articles, Reader and Laland (2002) reported a relation between executive brain ratio (ratio of neocortex to brain stem) and social learning/tool use/innovation among primates. Species with greater executive brain ratios displayed higher levels of social learning, tool use, and innovation (discovering novel solutions to environmental or social problems) than species with smaller ratios. More directly related to the relation among brain size, length of the juvenile period, and social complexity is research by JoVe (1997), who reported a relationship between size of the nonvisual cortex, length of the juvenile period, and social complexity (i.e., size of typical social group) among 27 primate species. JoVe found that larger brains, longer juvenile periods, and larger social groups co-occurred, and likely co-evolved. With respect to human evolution, we last shared a common ancestor with chimpanzees (Pan troglodytes) between 6 and 8 million years ago. H. sapiens is the only member of the hominid clan alive today, which may have included as many as two dozen diVerent species, many living contemporaneously with one another, over the past 6 million years. Although we have fossil records of what some of these animals looked like, we can only infer their minds and behavior from the artifacts they left behind and by comparisons with modern species (Mithen, 1996). However, we can also gain valuable insight about human psychological origins from studying our closest genetic relative, the chimpanzee. Although humans did not evolve from chimpanzees, it is likely our common ancestor with chimps possessed many of the characteristics of these modern animals. Like humans, chimpanzees have large brains for their body size (the second largest of all land mammals after humans), have an extended juvenile period, and live in socially complex groups. Chimpanzees display evidence of culture, passing information such as styles of grooming, greeting, termite Wshing, or nut cracking across generations (Whiten, 2005; Whiten et al., 1999). These are precisely the conditions that have been proposed to be conducive to the evolution of human intelligence, particularly epigenetic evolution as proposed by Baldwin and some of his modern advocates (e.g., Deacon, 1997; Dennett, 1991; see Weber & Depew, 2003). The enculturation hypothesis Consistent with the argument that maternal behavior may contribute to important behavioral or cognitive changes that can serve as grist for natural selection, there is evidence that chimpanzees reared by humans, much as human children are reared, display

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patterns of social cognition that diVer from mother or wild-reared chimpanzees. The enculturation hypothesis (Call & Tomasello, 1996) refers to the idea that the cognition of chimpanzees and other great apes is appreciably changed, in the direction of human cognition, as a result of a species-atypical rearing environment. These animals are “mothered” by humans (both male and female), and experience early life much as human children would. Adult humans speak to and explicitly teach chimpanzees (teaching is rarely done by mother chimpanzees either in the wild or in laboratories, but see discussion below). They also engage in shared-joint, or triadic, attention, with humans, pointing to objects that both they and the ape can see and looking back and forth between the participants and objects, with one “knowing” that the other one sees (i.e., has knowledge of) the object. Such triadic interaction is not observed in nonenculturated great apes (e.g., Tomonaga et al., 2004). The importance of such treatment is that enculturated apes are treated as intentional agents—as having wishes and desires that motivate their behavior and realizing that others’ behavior is similarly motivated. Call and Tomasello (1996) proposed that such treatment facilitates the development of certain species-atypical sociocognitive abilities, particularly the ability to understand others as intentional agents. This implies the acquisition of metarepresentational skills not typically attributed to great apes, speciWcally the ability to take the perspective of others as indicated in theory-of-mind tasks, in which participants understand peoples’ behavior is motivated by their beliefs and desires (Wellman, 1990) and that others can have false beliefs (e.g., Wimmer & Perner, 1983). There is research evidence to suggest that aspects of enculturated great apes’ social cognition is diVerent from that of mother-reared apes and more like that of human children, although this position remains controversial (see Bering, 2001, 2004; Povinelli, Bering, & Giambrone, 2001). One reason for the controversy is that such research often lacks the experimental controls psychologists like. Sample sizes are small, proper control participants are often hard to come by, and to date, there have been no systematic studies specifying precisely what experiences diVerentiate enculturated from nonenculturated animals. Nonetheless, the arguments and observations associated with the enculturation hypothesis are provocative and have substantial theoretical import about the role of experience in shaping great-ape cognition and the possible role of rearing experiences on human cognitive evolution, and I will brieXy review this literature. First, there is no experimental evidence that enculturated great apes can pass false-belief tasks (Call & Tomasello, 1999). These tasks involve a participant and a confederate observing where an object is hidden, the confederate leaving the room, at which time the object is moved to a new location. The question is, will the participant realize that the confederate, who was not privy to the moving of the object, know where the object is now hidden? Most children under 4-years of age fail this task, stating that the confederate will know the correct location of the object, whereas most children over 4-years of age correctly say that the confederate will have a false belief, believing that the object is still in its original location. Call and Tomasello (1999) developed a well-controlled nonverbal form of the false-belief task, which children passed around 5-years of age, but none of the apes tested (both enculturated and nonenculturated) did. The two areas in which enculturated apes’ cognition have been shown to be diVerent than that of nonenculturated apes is in referential communication and social learning. Referential communication in apes is assessed via referential pointing—pointing to indicate objects at a distance. Apes in the wild do use gestures in short-range social interactions

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(Goodall, 1986; McGrew & Tutin, 1978), but there is no evidence that such gestures are referential, and there is no experimental research indicating that nonenculturated apes engage in referential pointing. Nonenculturated apes appear not to understand humans’ use of pointing (Call & Tomasello, 1994; Povinelli, Reaux, Bierschwale, Allain, & Simon, 1997) and use the proximity of a person’s hand to a desired treat, rather than the direction in which the hand is pointing, in interpreting human hand gestures (Povinelli et al., 1997). In comparison, enculturated members of each species of great ape have been shown to use referential pointing: chimpanzees (Pan troglodytes, Povinelli, Nelson, & Boysen, 1992; Savage-Rumbaugh, 1986), bonobos (Pan paniscus, Savage-Rumbaugh, McDonald, Sevcik, Hopkins, & Rubert, 1986), gorillas (Gorilla gorilla, Patterson, 1978), and orangutans (Pongo pygmaeus, Call & Tomasello, 1994; Miles, 1990). Referential pointing seems to be the crux of shared-joint attention and the realization that a communication partner’s attention can be directed to an object via a distal cue (i.e., pointing). The inability to engage in referential pointing suggests that one is not able to take the perspective of another, whereas the opposite is inferred when one displays referential pointing (but see Bering, 2004 for alternative interpretations). With respect to social learning, there is no question that chimpanzees acquire information via observation. As I noted above, there is evidence that wild chimpanzees transmit cultural information, such as forms of greetings, grooming, and tool use, from one generation to the next (Whiten et al., 1999). Similar observations have been made for wild orangutans (van Schaik et al., 2003). However, comparative psychologists have long recognized that not all forms of social learning are equivalent (see e.g., Tomasello & Call, 1997; Whiten, Horner, LitchWeld, & Marshall-Pescini, 2004). SpeciWcally, the cognitive requirements underlying diVerent types of social learning may vary considerably. Social facilitation may be the simplest, with the behavior of animals being activated by the presence of others, and the target behavior being “discovered” via trial and error learning. Emulation is an eVective type of social learning and involves achieving the same goal as a model (e.g., getting ants from under a log) but using diVerent behaviors or sequences of actions than the model. In contrast, true imitation, as deWned by Tomasello and his colleagues (Boesch & Tomasello, 1998; Tomasello, 1996, 2000), requires that the observer understand the goal, or intentions, of the model, as well as duplicate important aspects of the model’s behavior in pursuit of that goal. Such social learning requires perspective taking. More complicated yet is deferred imitation, the copying of an observed behavior after some signiWcant delay. Piaget (1962) believed that deferred imitation is a reXection of the symbolic, or semiotic, function and observed in human infants about 18-months of age. More recent research indicates that infants as young as 6-months of age can display deferred imitation for simple actions on objects (Collie & Hayne, 1999), suggesting to some that symbolic representation is within the capacity of infants within the Wrst year of life (e.g., MeltzoV, 1995). Deferred imitation may involve explicit, or declarative, memory (in contrast to implicit, or nondeclarative memory) (e.g., Bauer, 1997, 2004; MeltzoV & Moore, 1997). This is illustrated by the failure of patients with hippocampal brain damage, which has been shown to impede the acquisition of new declarative memories, to perform successfully deferred-imitation tasks, much as those “passed” by toddlers (McDonough, Mandler, McKee, & Squire, 1995). Although there is controversy about whether nonenculturated apes possess true imitation (see Tomasello & Call, 1997; Whiten et al., 2004), there is agreement that they are much more likely to solve social learning tasks via is emulation than are human children,

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who are more likely to engage in imitation. For example, Horner and Whiten (2005) showed chimpanzees and 3- to 4-year-old children ways in which to open a puzzle box in order to get a treat. The children tended to reproduce the exact actions of the model (imitation), even if there was a more eYcient way of opening the box. The chimpanzees instead opted for emulation, using alternative behaviors (and ignoring irrelevant ones displayed by the model) to open the box (see also Call & Carpenter, 2003; Call, Carpenter, & Tomasello, 2004). In many cases, emulation may be a more eYcient approach to achieve a goal. But consistent with the theorizing of Richardson and Boyd (2005) discussed above, and others (e.g., Tomasello, 1999; Tomasello & Carpenter, 2005), human children may be particularly susceptible imitative learning, which is the basis for cumulative cultural evolution. There is also no evidence that nonenculturated chimpanzees display deferred imitation. However, several research projects have demonstrated deferred imitation of actions on objects in enculturated apes. In the Wrst published experiment on this topic, Tomasello, Savage-Rumbaugh, and Kruger (1993) tested three enculturated chimpanzees (one common chimp and two bonobos) and three mother-reared chimpanzees (one common chimp and two bonobos). In a series of trials in which both immediate and deferred imitation was assessed, there was no evidence of above-chance performance for the mother-reared animals, but there was for enculturated chimpanzees. In fact, the enculturated chimpanzees actually out-performed 1.5- and 2.5-year old children on the deferred-imitation tasks. In subsequent research, Bjorklund, Bering, and their colleagues tested three juvenile enculturated chimpanzees and three juvenile enculturated orangutans on deferred imitation tasks (Bering, Bjorklund, & Ragan, 2000; Bjorklund, Bering, & Ragan, 2000; Bjorklund, Yunger, Bering, & Ragan, 2002; Yunger & Bjorklund, 2004; see Bjorklund & Rosenberg (2005) for review). In an initial study, each animal interacted with the target objects for a single task for 4-min, observed a human model display speciWc actions on the objects (e.g., placing a plastic nail in a form board and striking it with a plastic hammer), and after a 10-min delay, was given the objects again (Bering et al., 2000). Both the chimpanzees and orangutans displayed greater-than-chance levels of deferred imitation. The youngest chimpanzee (2 years, 1-month old at initial testing) had the lowest level of deferred imitation (28%), but showed increased levels at later ages, suggesting a developmental component of deferred imitation in enculturated chimpanzees (see Bjorklund & Bering, 2003b).6 Later research used a generalization of imitation task, in which a target behavior was modeled for one set of objects (musical cymbals, for example) and the animals subsequently were given similar but not identical objects (e.g., trowels) to determine if they would generalize the observed actions. Three enculturated chimpanzees displayed abovechance levels of deferred imitation of actions on objects (although at lower levels than for deferred imitation when the same objects were used in the modeling and imitation phases) (Bjorklund et al., 2002); in contrast, there was no evidence of generalization of imitation for two enculturated orangutans (Yunger & Bjorklund, 2004).

6 Although a group of adult nonenculturated apes was not available for this research, Wve nonenculturated chimpanzees housed at Yerkes Field Station were subsequently tested using our procedures by Kristen Bonnie and Franz de Waal. On a series of trials, these animals displayed no evidence of either immediate or deferred imitation of actions on objects. Thus, although these informal data do not prove that mother-reared animals cannot display true imitation, they indicate, at the least, that they are not inclined to do so, even when prompted.

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Coupled with the Wnding from studies of referential communication, the results of the research by Tomasello, Kruger, and Ratner (1993) and Bjorklund, Bering, and their colleagues suggests that the species-atypical rearing aVorded the enculturated chimpanzees produced species-atypical social cognition. We cannot state with certainty that nonenculturated apes are incapable of such social learning. Perhaps they have the abilities but merely lack the proper motivation to display them. The experiences of enculturated apes may involve a socialization of attention (Tomasello, 1999; see also Call & Carpenter, 2003), in which they learn to be attentive to human behavior, which in turn promotes social learning. Similarly, Bering (2004) proposed the apprentice hypothesis, in which enculturated apes learn that humans provide solutions to many problems, and, as a result, they become especially attentive to human actions that, in turn, enhances their social-learning abilities when humans serve as models. Each of these proposals acknowledges that enculturated apes perform diVerently on social-cognitive tasks than nonenculturated apes, but questions whether these reXect “deep” changes in terms of representational ability. Regardless, chimpanzees possess suYcient plasticity to modify their behavior (and perhaps their representational abilities) as a result of experiencing a species-atypical environment. In some sense, this is not news, for such plasticity in behavior has been shown in cross-fostering studies for a wide range of animals (e.g., Francis et al., 1999; Kuo, 1976). What is impressive here is that the animals in question are humans’ closest genetic relatives, the rearing environment is similar to that experienced by human children, and the cognitive/behavioral change is toward a more H. sapiens way of thinking. This, of course, does not forecast a “Planet of the Apes” scenario, in which enculturated apes join forces to take over the Earth. The changes displayed here are modest and do not alter the essential nature of chimpanzees. My point is that these animals have suYcient plasticity to modify their behavior and cognition in response to early “mothering” in a human-like direction. Should our common ancestor with chimpanzees also have had this degree of cognitive Xexibility in response to early environments, such plasticity could have begun a cascade of events that generated novel phenotypes subject to natural selection, that, in combination with other selection pressures over many generations, were precursors to the modern human mind. Plasticity, mothers, and the evolution of human intelligence Given the plasticity displayed by enculturated great apes, which was likely also possessed by our common ancestor, a change in “mothering” (for mothers do the bulk of parenting in all great-ape species) could have prompted a change in the cognitive development of their oVspring. If the environment responsible for the parenting change remained stable and if it aVected multiple members of a population, it could have yielded a selective advantage for those individuals possessing enhanced social-learning skills. It would also have opened new niches for such individuals, perhaps promoting the transmission of social and technical (e.g., tool use) information and fostering new selective pressures that would further accelerate phylogenetic change. Note that the plasticity needed for such a scenario must lie both within the infant and the mother. For mammals, many aspects of early environments are interpreted through mothers, making infant mammals especially sensitive to variations in maternal behavior. It is mothers who are the Wrst responders to environmental change. They must be able to modify their behavior in response to environmental input if they are to have an impact on

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their more pliable oVspring. Is there any evidence that our ancestral mothers had this plasticity? We must again turn to chimpanzees. As I noted above, although chimpanzees are impressive social learners, it seems that most of their observational learning does not involve the perspective taking necessary for true imitation or the representational ability needed for deferred imitation. But there is some evidence for explicit teaching in chimpanzees. Teaching requires that the teacher understand what the learner knows and his or her goals, and that the student appreciate the teacher’s goal (Tomasello et al., 1993). That is, teachers must view their students as intentional agents, and vice versa. Mother chimpanzees have been observed to systematically modify their tool-use behavior (e.g., cracking nuts with stones, Wshing for termites with sticks) in the presence of their oVspring in such a way as to promote the acquisition of the behavior in their oVspring (Boesch, 1991, 1993; GreenWeld, Maynard, Boehm, & Schmidtling, 2000). Such observations are rare and their status as “true” incidents of teaching have been questioned (e.g., Bering, 2001, 2004), but they have been observed enough times for them to be credible. [There is also some evidence of teaching by mother dolphins to their calves of tool use (sponging, Krützen et al., 2005) and of foraging (Bortot, Herzing, & Bjorklund, 2006).] It seems clear that most complicated social behavior in chimpanzee societies are not transmitted via teaching, but by other less-sophisticated means, such as social facilitation or emulation. But some chimpanzee mothers and their oVspring do appear to engage in teaching-learning bouts, for nut cracking and termite Wshing. (It seems that female infants are more attentive than males to their mothers’ tool use during termite Wshing, Lonsdorf, Pusey, & Eberly, 2004, and acquire termite Wshing proWciency earlier than males, Lonsdorf, 2005.) I am aware of no evidence indicating that these few “teaching mothers” and their oVspring diVer from other chimpanzees in terms of genetics or rearing experience (although I predict that they do). However, the very existence of such “teaching mothers,” coupled with the species-wide chimpanzee pattern of big brains, slow development, and socially complex lifestyles, suggests that the conditions for a Baldwin-like evolutionary change, at the hands of mothers, were present in our ancestors. One can only speculate at the environmental change that may have been the impetus for the proposed social-cognitive modiWcation. When teaching is observed in chimpanzees, it usually involves tool use. Perhaps ecological conditions made tool use more important for survival, and those mothers who could pass along this skill more eVectively to their oVspring had greater inclusive Wtness than other mothers. For example, Kaplan, Hill, Lancaster, and Hurtado (2000) note that the hunting and food-gathering skills of traditional people, relative to the technologies used by chimpanzees, require an extended apprenticeship. Acquiring these survival skills would have been enhanced by more sophisticated social-learning abilities. Once these greater social-cognitive skills became established within a population, they could be applied to almost any problem—technical, social, or political—in which viewing other individuals as intentional agents was involved. There would have been great selection pressure for individuals to develop such skills, and mothers who did not promote these abilities in their oVspring would Wnd their progeny at a decided disadvantage. Conclusion Counter to the canonical view through most of the last century, modern evolutionary theory is beginning to recognize the role of ontogeny in phylogeny. Although much

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emphasis in Evo-Devo has been at the molecular level, behavior has also come to be seen as a possible motivator of evolutionary change, harking back to the ideas of James Mark Baldwin. Epigenetic evolution has been documented in many species, and contemporary research with mammals indicates that changes in early rearing experience can have transgenerational eVects and can produce variation that is subject to natural selection. In mammals in particular, mothers are the most inXuential “environment” of a young animal, and changes in maternal behavior, brought about by changes in the environment, can have signiWcant impact on oVspring, and possibly on evolution. Such maternal eVects may be greatest in big-brained animals, which show greater cognitive and behavioral plasticity. These include our closest-living relatives the great apes, particularly chimpanzees. Although one cannot turn back the clock and either observe our ancient ancestors change over the millennia or perform experiments on them, a knowledge of the process of current ontogeny in humans, great apes, and animals in general, can provide insight into how our species’ perhaps most distinguishing ability evolved over the past 6–8 million years, and perhaps the direction that cognitive evolution may take in the future. Acknowledgments I thank Jesse Bering, Carlos Hernández Blasi, David Lewkowitz, and Annemie Ploeger, for comments on earlier drafts of this manuscript. References Agrawal, A. A., Laforsch, C., & Tollrian, R. (1999). Transgenerational induction of defences in animals and plants. Nature, 40, 60–63. Aisner, R., & Terkel, J. (1992). Ontogeny of pine cone opening behavior in the black rats, Rattus rattus. Animal Behaviour, 44, 327–336. Alexander, R. D. (1979). Darwinism and human aVairs. Seattle: University of Washington Press. Alexander, R. D. (1989). Evolution of the human psyche. In P. Mellers & C. Stringer (Eds.), The human revolution: behavioural and biological perspectives on the origins of modern humans (pp. 455–513). Princeton, NJ: Princeton University Press. Anway, M. D., Cupp, A. S., Uzumcu, M., & Skinner, M. K. (2005). Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science, 308(3), 1466–1469. Avital, E., & Jablonka, E. (2001). Animal traditions: Behavioural inheritance in evolution. Cambridge: Cambridge University Press. Baldwin, J. M. (1896). A new factor in evolution. American Naturalist, 30, 441–451 pp. 536–553. Baldwin, J. M. (1902). Development and evolution. New York: McMillan. Barr, C. S., Newman, T. K., Shannon, C., Parker, C., Dvoskin, R. L., Becker, M. L., et al. (2004). Rearing condition and rh5-HTTLPR interact to inXuence limbic–hypothalamic–pituitary–adrenal axis response to stress in infant macaques. Biological Psychiatry, 55, 733–738. Bateson, P. P. G. (1988). The active role of behaviour in evolution. In M.-W. Ho & S. Fox (Eds.), Process and metaphors in evolution (pp. 191–207). Chichester: Wiley. Bauer, P. J. (1997). Development of memory in early childhood. In N. Cowan (Ed.), The development of memory in childhood (pp. 83–111). Hove East Essex, England: Psychology Press. Bauer, P. J. (2004). Getting declarative memory oV the ground: steps toward construction of a neuro-developmental account of changes in the Wrst two years of life. Developmental Review, 24, 347–373. Baumrind, D. (1993). The average expectable environment is not good enough: a response to Scarr. Child Development, 64, 1299–1317. Bennett, A. J., Lesch, K. P., Heils, A., Long, J., Lorenz, J., Shoaf, S. E., et al. (2002). Early experience and serotonin transporter gene variation interact to inXuence primate CNS function. Molecular Psychiatry, 17, 118–122. Bering, J. M. (in press). The folk psychology of souls. Behavioral and Brain Sciences.

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