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Essay Darwin in : New Opportunities for

Johan J. Bolhuis1*, Gillian R. Brown2, Robert C. Richardson3, Kevin N. Laland4* 1 Behavioural Biology Group and Helmholtz Institute, Utrecht University, Utrecht, The Netherlands, 2 School of Psychology, University of St Andrews, St Andrews, Scotland, United Kingdom, 3 Department of Philosophy, University of Cincinnati, Cincinnati, Ohio, United States of America, 4 School of Biology, University of St Andrews, St Andrews, Scotland, United Kingdom

Abstract: Evolutionary Psychology which rapidly became dominated by a pressures acting in ancestral conditions—in (EP) views the human mind as school of thought stemming from the an environment of evolutionary adapted- organized into many modules, each University of California at Santa Barbara ness (EEA)—and are not necessarily adap- underpinned by psychological ad- (see Box 1). The essence of this brand of tive in a contemporary world that has aptations designed to solve prob- Evolutionary Psychology (EP) is neatly changed radically in recent millennia. lems faced by our Pleistocene summarized in the famous quote that ‘‘Our From this vantage point, genetic ancestors. We argue that the key modern skulls house a Stone Age mind’’ [2]. simply could not keep pace fully with the tenets of the established EP para- However, many evolutionarily minded extraordinary rate at which human tech- digm require modification in the psychologists, evolutionary biologists, and nology transformed environments. Tied up light of recent findings from a philosophers of science disagree with the with this notion of adaptive lag (or number of disciplines, including theoretical proposals put forward by the mismatch between our biology and our human genetics, evolutionary biol- Santa Barbara evolutionary psychologists, environment) is an emphasis on evolution- ogy, cognitive neuroscience, devel- and the discipline has been the subject of ary gradualism: evolutionary change, par- opmental psychology, and paleo- intense debates [1,3–13]. Here, we assess ticularly with respect to complex adapta- . For instance, many human genes have been subject to recent the impact of recent developments in tions in the human mind, is deemed to have selective sweeps; humans play an genetics, evolutionary and developmental occurred slowly; too slowly to have led to active, constructive role in co-di- biology, paleoecology, and cognitive sci- significant genetic change in the few recting their own development and ence on EP and then go on to suggest that hundred generations that have elapsed evolution; and experimental evi- these developments provide new avenues since the end of the Pleistocene, or even dence often favours a general for research. since the spread of modern humans around process, rather than a modular the world over the last 50,000 years. account, of cognition. A redefined Reassessing the Major Tenets of Recent developments in human genetics EP could use the theoretical in- Evolutionary Psychology have challenged the concepts of adaptive sights of modern evolutionary bi- lag and gradualism. EP originated in the ology as a rich source of hypothe- EP is encapsulated by four major tenets early 1980s, when our knowledge of the ses concerning the human mind, (see Box 1) that have generated consider- human genome was limited and gradualism and could exploit novel methods able discussion. Here, we argue that all of dominated evolutionary thinking (although from a variety of adjacent research these basic assumptions need to be reas- biologists’ attempts to estimate rates of fields. sessed in the light of contemporary selection in nature were in full flow in the evidence. 1970s [14], leaving the Santa Barbara school’s gradualism assumption conten- The Environment of Evolutionary tious from the outset). Since then, geneti- In the century and a half since Charles Adaptedness and Gradualism cists have not only mapped the genome, but Darwin’s publication of the Origin of , EP argues that that human cognitive have devised means for detecting which evolutionary theory has become the bedrock processes evolved in response to selection genes have been subject to recent selection of modern biology; yet, its application to the human mind remains steeped in controversy Citation: Bolhuis JJ, Brown GR, Richardson RC, Laland KN (2011) Darwin in Mind: New Opportunities for [1–13]. Darwin himself wrote of cognitive Evolutionary Psychology. PLoS Biol 9(7): e1001109. doi:10.1371/journal.pbio.1001109 evolution, most notably in The Descent of Man, Published July 19, 2011 where he suggested that like any other trait, Copyright: ß 2011 Bolhuis et al. This is an open-access article distributed under the terms of the Creative human ‘‘mental faculties’’ are the outcome of Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, evolution by natural and and provided the original author and source are credited. insisted that they should be understood in Funding: JJB is funded by Utrecht University and by Netherlands Organization for Scientific Research (NWO) lightofwhathecalled‘‘commondescent’’. grants (ALW Open Competition and GW Horizon Programme) (http://www.nwo.nl/). GRB is funded by a This evolutionary interpretation of human Wellcome Trust Career Development Fellowship, UK (http://www.wellcome.ac.uk/). RCR is funded by the University of Cincinnati. KNL is funded by the BBSRC, UK (http://www.bbsrc.ac.uk/) and an ERC Advanced Grant cognition was taken up in the 1980s by http://erc.europa.eu/). The funders had no role in study design, data collection and analysis, decision to publish, contemporary evolutionary psychology, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist.

Essays articulate a specific perspective on a topic of Abbreviations: AI, artificial intelligence; EEA, environment of evolutionary adaptedness; EP, Evolutionary broad interest to scientists. Psychology * E-mail: [email protected] (JJB); [email protected] (KNL)

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Box 1. The Major Tenets of Evolutionary Psychology populations during the Pleistocene epoch (approximately 1.7 million to 10,000 years According to the Santa Barbara school of Evolutionary Psychology (EP), human ago), the abstract concept of stable selec- are organized into a large number of evolved psychological mechanisms— tion pressures in the EEA is challenged by psychological designed to solve recurrent problems faced by our recent evidence from paleoecology and hunter-gatherer ancestors [30]. These evolutionary psychologists attempt to paleoanthropology. The Pleistocene was provide criteria for ‘‘carving the mind at its natural joints’’ [104], generally by apparently far from stable, not only being reverse-engineering from an observable phenomenon to its proposed function. variable, but progressively changing in the pattern of variation [25,26]. The world In the 1980s, four major tenets of EP crystallized, and these ideas became experienced by members of the genus widespread. While not all evolutionary psychologists endorse the Santa Barbara Homo in the early Pleistocene was very perspective, these ideas have nonetheless shaped the broader field, and remain different from that experienced in the late extremely prevalent. Pleistocene, and even early anatomical 1. The environment of evolutionary adaptedness (EEA). This concept refers to the modern Homo sapiens that lived around notion that our psychological mechanisms have evolved in response to stable 150,000 years ago led very different features of ancestral environments [87]. While the EEA has frequently been from Upper Paleolithic people (40,000 equated with an African Pleistocene savanna, this version of the concept has years ago) [27–29]. been strongly critiqued [66], and the more recent formulation of the EEA concept presents a broader, less specific theoretical landscape of our past lives, based on Universalism an abstract statistical composite of all relevant past selective environments [105]. EP has also placed emphasis on the concept of human nature, comprising a 2. Gradualism. Evolutionary psychologists argue that minds are built from co- species-specific repertoire of universal, adapted gene complexes that are unable to respond quickly to selection evolved psychological mechanisms, from [105,106]. When combined with the concept of the EEA, gradualism suggests that a childhood fear of strangers, to a cheater- human beings experience an adaptive lag [88], such that evolved psychological mechanisms may not produce adaptive responses in modern human environ- detection mechanism, to a preference for ments that have undergone dramatic recent changes [105]. specific mate characteristics. This putative universal cognition can be rendered com- 3. Massive . Given that different sets of adaptive problems will have patible with the observed diversity in required different computational solutions, the mind is argued to consist human behaviour by recourse to context- predominantly of domain-specific, modular programmes [105]. Whether the mind dependent strategies. From this perspec- also contains evolved general-purpose processes remains debated within EP tive, the mind shifts between pre-specified [104]. behavioural outputs in response to differ- ential environmental influences [30,31]. 4. Universal human nature. The evolved computational programmes in the human This explanation of human behavioral mind are assumed to be responsible for producing a universal (that is, species- variation is also contentious [3,32–34]. typical) human nature [105]. At the same time, different outcomes of these The notion of universalism has led to the programmes are suggested to be triggered by different environmental or social view that undergraduates at Western conditions, leading to the prediction of both universal behavioural outcomes and universities constitute a representative locally specified adaptive solutions [105]. sample of human nature, a view that has been subject to criticism from anthropol- ogists and psychologists [33–35]. More- [15–19]. There have been substantial wide variety of animals [14,24], finding over, by EP’s formulation, all epigenetic human genetic changes in the last 50,000 that evolutionary change typically occurs and developmental effects simply evoke years, with possibly as much as 10% of much faster than hitherto thought. A alternative genetically pre-specified strate- human genes affected [19]. Events in the recent meta-analysis of 63 studies that gies. Recent trends in developmental Holocene (the last 10,000 years), particu- measured the strength of psychology and neuroscience have instead larly the adoption of agriculture, domesti- in 62 species, including more than 2,500 stressed the malleability of the human cation of animals, and the increases in estimates of selection, concluded that the , emphasizing how experience tunes human densities that these practices afford- median selection gradient (a measure of and regulates synaptic connectivity, neural ed, were a major source of selection on our the rate of change of with trait circuitry and gene expression in the brain, species [17–22], and possibly accelerated value) was 0.16, which would cause a leading to remarkable plasticity in the [20,22]. Evidence from quantitative trait to change by one stan- brain’s structural and functional organiza- the human genome strongly suggests that dard deviation in just 25 generations [24]. tion [36]. Neuroscientists have been aware has been affected If humans exhibit equivalent rates, then since the 1980s that the human brain has by responses to features of the environment significant genetic evolution would occur too much architectural complexity for it to that were constructed by humans, from over the course of a few hundred years. be plausible that genes specify its wiring in culturally facilitated changes in diet, to While fast evolution is far from inevitable, detail [37]; therefore, developmental pro- aspects of modern living that inadvertently there is nonetheless strong evidence that it cesses carry much of the burden of promoted the spread of diseases [22,23]. has frequently occurred in humans. EP has establishing neural connections. Genes expressed in the human brain are yet to come to terms with the possibility of In parallel, emerging trends in evolu- well-represented in this recent selection recent, rapid genetic changes with their tionary theory, particularly the growth of [11,12]. potential for associated neural rewiring. developmental systems theory, epigenetic Evolutionary biologists have also mea- Even if we consider the selection inheritance, and niche-construction theo- sured the rate of response to selection in a pressures that acted on ancestral human ry, have placed emphasis on organisms as

PLoS Biology | www.plosbiology.org 2 July 2011 | Volume 9 | Issue 7 | e1001109 . active constructors of their environments about behavioural variation within and because the Fodorian executive part of [38–40]. The development of an organ- between populations in traits commonly the brain can directly monitor the fingers ism, including the characteristics of its studied by evolutionary psychologists. For and the feet [71]. The same projections brain, involves a complex interaction example, sex differences in mate prefer- allow exhibit fine control of the tongue, between genetically inherited information, ences constitute a large proportion of EP vocal chords, and breathing, without epigenetic influences, and learning in research and are generally assumed to which humans probably could not have response to constructed features of the exhibit universal patterns (e.g., [59,60]); learned to speak [71]. After evaluating the physical and social environment [5,40– however, sexual selection theory suggests evidence and consistent with Fodor’s 45]. From this viewpoint, the human mind that a number of factors, such as sex- original proposals, Bolhuis and Macphail does not consist of pre-specified pro- biased mortality, population density, and [64] suggested that there is no evidence for grammes, but is built via a constant variation in mate quality, will affect sex modularity in central systems such as those interplay between the individual and its roles (see Box 3). A modern EP would involved in learning and memory. With environment [45,46], a point made by make greater use of the theoretical insights regard to cognitive mechanisms, more developmental psychologist Daniel Lehr- of modern as a often than not, data from animal experi- man [47] many years ago. By constructing source of testable hypotheses [3,6]. ments is consistent with a general-process their worlds (for example, by building account rather than an interpretation homes, planting crops, and setting up Massive Modularity involving adaptively specialized cognitive social institutions), humans co-direct their EP has proposed that the mind consists modules [64,65,67,72]. own development and evolution [22,39, of evolved cognitive modules, a perspec- A large part of EP’s emphasis on massive 48,49]. tive referred to as the massive modularity modularity drew from artificial intelligence The view that a universal genetic hypothesis [61,62]. Massive modularity is (AI) research. While the great lesson from AI programme underpins human cognition a somewhat idiosyncratic interpretation of research of the 1970s was that domain is also not fully consistent with current Fodor’s [63] original concept of modular- specificity was critical to intelligent behav- genetic evidence. Humans are less genet- ity. Essentially, Fodor suggested that what iour, the lesson of the new millennium is that ically diverse than many species, including he called input systems (such as those intelligent agents (such as driverless robotic other apes [50], largely because human involved in auditory and visual perception, cars) require integration and decision-mak- effective population sizes were small until but also in language) were modular, i.e., ing across domains, regularly utilize general- around 70,000 years ago [51,52]. None- operating in relative isolation from each process tools such as Bayesian analysis, theless, there is enough to other. Information from these modular stochastic modelling, and optimization, and have supported considerable adaptive systems would be passed on to central are responsive to a variety of environmental change in the intervening time, and recent systems (involved in problem solving or cues [73]. However, while AI research has thinking amongst geneticists is that our thought) that themselves were thought not shifted away from an emphasis on domain species’ unique reliance on learned behav- to be modular. EP has extended modular- specificity, some evolutionary psychologists iour and culture may have relaxed allow- ity to involve the whole mind/brain. continue to argue that selection would have able thresholds for large-scale genomic The thesis of massive modularity is not favoured predominantly domain-specific diversity [21,53]. Human behavioral ge- supported by the neuroscientific evidence mechanisms (e.g., [74]). In contrast, others netics has also identified genetic variation [64–67]. Firstly, comparative psychology have started to present the case for domain- underlying an extensive list of cognitive presents an unassailable case for the general evolved psychological mechanisms and behavioural characteristics [54]. existence of domain-general mechanisms. (e.g., [75,76]), and evidence from develop- While variation within populations ac- The processes of associative learning are mental psychology suggests that domain- counts for the bulk of human genetic widespread in animals and have general general learning mechanisms frequently variation, around 5%–7% of genetic properties that allow animals to learn build on knowledge acquired through do- differences can be attributed to variation about the causal relationships among a main-specific perceptual processes and core between populations [55]. Some of the wide variety of events [68,69]. For in- cognition [44]. Both domain-specific and significant genetic differences between stance, a simple learning theory rule, domain-general mechanisms are compatible human populations have arisen from known as the Rescorla–Wagner rule with evolutionary theory, and their relative recent selective events [56,57]. Gene- [70], has proved extraordinarily useful in importance in human information process- culture may well turn out to explaining the results of hundreds of ing will only be revealed through careful be the characteristic pattern of evolution- experiments in diverse animals, including experimentation, leading to a greater un- ary change in humans over recent time foraging in honeybees, avoidance condi- derstanding of how the brain works [44]. spans [22,58] (see Box 2). From this tioning in goldfish, and inferential reason- perspective, cultural practices are likely ing in humans. to have influenced selection pressures on Secondly, there is broad involvement of Towards a New Science of the the human brain, raising the possibility diverse neural structures in many psycho- Evolution of the Mind that genetic variation could lead to biases logical processes, and there is feedback in the human cognitive processing be- even to the most basic perceptual process- We have reviewed how developments in tween, as well as within, populations. In ing. For instance, the hominid brain has a number of scientific fields have called summary, there is no uniform human not only witnessed a proportional expan- into question the key tenets of EP. genetic program. sion of the neocortex, but the neocortex Fortunately, these developments do not EP’s emphasis on a universal human has become intricately interconnected and just create problems for EP, but also nature has hindered its exploitation of new has evolved projections into the medulla suggest potential solutions. We argue that opportunities to examine human diversity and spinal cord [71]. This has allowed the key factor will be the methodological utilizing evolutionary biology. Contempo- humans to learn intricate routines of and conceptual integration of EP with rary evolution theory makes predictions movement and complex manual tasks, adjacent fields.

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Box 2. Gene-Culture Coevolution [6,81]. For example, the numerous studies supporting the hypothesis that human Gene-culture coevolutionary theory explores how genetic and cultural processes beings are predisposed to detect cheaters interact over evolutionary time [22,58]. Changes in diet afforded by cultural in social situations [74,82] are consistent practices, such as agriculture and the of and animals, with several evolutionary explanations. provide compelling examples of gene-culture coevolution, demonstrating how While the original researchers reasoned cultural practices have transformed the selection pressures acting on humans and that cheater detection has resulted from a given rise to some of the genetic differences between human populations. For selective history of instance, there is now little doubt that dairy farming created the selective [82], alternative evolutionary explana- environment that favoured the spread of alleles for adult lactose tolerance tions, for instance that a history of cultural [85,107,108]. Another example concerns the evolution of the human amylase has selected for this trait gene: Perry et al. [109] found that copy number of the salivary amylase gene [83], and non-evolutionary explanations, (AMY1) is positively correlated with salivary amylase protein level and that are also plausible. individuals from human populations with high-starch diets have, on average, more AMY1 copies than those with traditionally low-starch diets. Indeed, the The recent trend within the behavioural transition to novel sources with the advent of agriculture and the sciences has been away from confirmation colonization of new habitats would appear to have been a major source of or rejection of a single hypothesis towards selection on humans [17,110], and several genes related to the metabolism of the far more powerful simultaneous eval- carbohydrates, lipids, and phosphates show signals of recent selection [17–19]. uation of multiple competing statistical models through model selection proce- More generally, human dispersal and subsequent exposure to novel climates, dures [84]. A modern EP would, as aggregation and exposure to new pathogens, and farming and exposure to new standard practice, conduct empirical stud- diets are now widely thought to be the source of selection for the spread of many ies designed specifically to test between human alleles [22]. Amongst the overrepresented categories in genome-wide multiple competing adaptive and non- scans of recent selection are numerous alleles expressed in the human nervous adaptive explanations [13], and would test system and brain [17–19]. This raises the possibility that complex cognition on the evolutionary historical, as well as the which culture is reliant (social intelligence, language, and challenges associated proximate, aspects of its hypotheses. In the with constructing and adapting to new environmental conditions) have driven following sections, we examine how EP human brain evolution. Mathematical models exploring how genetic and cultural could expand to cover all four of Tinber- processes interact provide strong support for the role of gene-culture coevolution gen’s questions. in human evolution [92,111–115]. Analyses of these models has often revealed patterns and rates of change that are uncharacteristic of more traditional i) A modern EP would evaluate the population genetic theory [92,114–116]. Gene-culture dynamics are typically evolution of a character by constructing and faster and stronger and operate over a broader range of conditions than testing population genetic models, estimat- conventional evolutionary dynamics [22,83,117,118]. ing and measuring responses to selection, exploring the covariation of phenotypic traits or genetic variation with putative selective agents, making comparisons Traditionally, EP has tested hypotheses rejected [1]. Here, we ask which of across species and seeking correlates to using the conventional tools of psychology Tinbergen’s questions is currently ad- selected traits in the selective environment, (questionnaires, computer-based experi- dressed in the field of EP and describe and so forth, as do contemporary evolu- ments, etc.). Generally these hypotheses how EP could expand its focus to provide tionary biologists. In addition to these have a functional perspective—that is, EP a broader and richer understanding of established tools, researchers can also proposes that a particular mechanism human behaviour. exploit modern comparative statistical functioned to enhance reproductive suc- Evolutionary psychologists commonly methods applied to cultural and behav- cess in our ancestors. However, Nobel seek to study how the human mind works ioural variation [85] and gene-culture laureate Niko Tinbergen [77] famously by using knowledge of evolution to coevolutionary theory [22,58,83,86] to proposed that understanding behavior formulate, and sometimes test, hypotheses reconstruct human evolutionary histories. requires comprehension not only of its concerning the function of cognitive ar- The function of reliable aspects of human function and evolution, but also of its causation chitecture. While functional or evolution- cognition, and of consistent behavioural and development [78], and he argued that a ary considerations cannot be used to test patterns, can be explored utilizing the complete understanding of behavior in- hypotheses about mechanisms, consider- same methods. An important point here is volves addressing all four of these ques- ations in one domain can generate hy- that researchers are not restricted to tions. These distinctions are relevant potheses concerning problems in the other considerations of the current function of because accounts of the evolution of brain domain. For instance, a theory of the evolved traits, and well-established meth- and cognition cannot in themselves ex- evolution of a certain cognitive trait may ods are available to reconstruct the plain the brain’s underlying working generate hypotheses as to the mechanisms evolutionary history of human cognition. mechanisms [1], since these are logically of that trait. Evolutionary psychologists ii) With regard to functional questions, distinct questions. While evolutionary have conducted hundreds of empirical while EP has stressed the idea that human analyses may generate clues as to the studies to test the predictions generated beings are adapted to past worlds [87], a mechanisms of human cognition, these are by consideration of evolutionary argu- niche-construction perspective argues that best regarded as hypotheses, not estab- ments [80]. However, we should be clear human beings are predicted to build lished explanations, that need to be tested that such studies do not test the evolution- environments to suit their adaptations, empirically [1,64,79], and there are in- ary hypotheses themselves, but rather test and to construct solutions to self-imposed stances where such evolutionary hypothe- whether the predictions about the psycho- challenges, aided and abetted by the ses about mechanisms have had to be logical mechanisms have been upheld extraordinary level of adaptive plasticity

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Box 3. Reconsidering the Evolution of Sex Roles use of optimality models proves unpro- ductive, and gene-cul- Based on the classic work of Bateman [119] and Trivers [120], EP has predicted sex ture coevolutionary models could be differences in the relative competiveness and choosiness of men and women developed to investigate whether the data when seeking mating partners. Men are generally assumed to have been selected conform to equilibria that are not globally to favour more sexual partners than women and to base their choices on the age, optimal (e.g., [92]). Researchers could go health, and physical attractiveness of prospective partners; in contrast, women on to explore which factors explain this are assumed to be more choosy than men and to base their judgements on the variation, for instance by measuring, willingness of males to invest resources in their offspring [59]. However, among diverse traits and across a broad contemporary sexual selection theory [121,122] suggests that a number of range of populations, what percentage of factors, such as sex-biased mortality, population density, and variation in mate the variance in behaviour is explained by quality, will affect how competitive and choosy males and females are, with sex local ecology and what percentage is better roles expected to vary considerably within and between societies. For example, predicted by cultural history (e.g., [93]). this theory predicts that, in human beings, both sexes will be choosy when encounter rates with potential mates are high, particularly where the parental iii) In order to study the causal mechanisms investment levels of both sexes are large and not too different, and/or where underlying the character, researchers can variation in mate quality of both sexes is high, and males are likely to be choosy in employ methodologies that are available populations with a female-biased adult sex ratio and considerable paternal to modern cognitive psychologists and investment. neuroscientists, such as fMRI and related technology, and take advantage of ad- The prediction that sex roles will vary between populations is borne out in data vances in genetics. While much EP on variance in mating and reproductive success in current and historic human research describes human behaviour in populations, which does not support the notion of a single universal pattern terms of information processing, decision [123]. In addition, evolutionary psychologists have themselves begun to record rules and cognition, the psychological cross-cultural variation in mate preferences and to examine whether variables adaptations can also be described at the such as adult sex ratios and local pathogen loads can explain within- and level of the nervous system. Cognitive and between-population variation in mating behaviour (e.g., [31]). However, the EP behavioural neuroscientists have amassed perspective generally assumes that context-specific strategies are pre-pro- a huge amount of research on the grammed within our evolved psychological mechanisms, such that individuals functioning of the nervous system, includ- possess multiple strategies that are differentially elicited by certain external ing the influence of genes on brain factors or that individuals develop a particular strategy as a result of environmental inputs acting on evolved developmental systems during early development. However, evolutionary psy- (e.g., [30,60]. Arguably, the more flexible and variable the exhibited behaviour, the chologists rarely examine whether their less explanatory power can be attributed to evolved structure in the mind. hypotheses regarding evolved psychologi- cal mechanisms are supported by what is An alternative perspective, supported by developmental systems and niche known about how the brain works. Here construction theorists (e.g., [38,39]), posits that the human mind does not consist the role of evolutionary knowledge is less solely of pre-specified programmes and that brain development is strongly direct, and again relegated to the gener- influenced by transmitted culture. One of the key contrasts between this ation of novel hypotheses that can be perspective and traditional EP is therefore the role that socially transmitted tested using established protocols. culture has to play in the development of the brain and behaviour [32]. For Variation in experimental procedures, illustration, consider how the relatively recent developments of agriculture (niche patterns of connectivity, differences be- construction), high-density populations, and the evolution of social stratification tween individuals, and comparisons across (transmitted culture), have dramatically changed the ecological context of human species potentially allows researchers to mating decisions from what would have occurred in hunter-gatherer societies. explore to what extent the circuitry According to the aforementioned theory, the increasing encounter rates that associated with the focal mechanism is such practices likely afforded should have led to much greater choosiness in both human specific, and to identify both the modern men and women compared to their Pleistocene ancestors. Modern evolutionary theory has much to offer evolutionary psychologists who are willing major genes involved and the environ- to eschew a focus on universality. mental conditions that regulate their expression. There is evidence that modern neuroscience technologies are starting to be used to test hypotheses generated from afforded by our capacities for learning and in the Holocene whilst exposed to modern, evolutionary theory [94–97], and some culture [88]. While adaptiveness is far culturally constructed environmental con- evolutionary psychologists are beginning from guaranteed, from this theoretical ditions [60]. However, rather than simply to present evolutionary accounts of genetic perspective humans are expected to expe- pronouncing that human behaviour is, or variation underlying traits such as person- rience far less adaptive lag than anticipat- is not, likely to be adaptive, a modern EP ality [98–100]. The aforementioned de- ed by EP [88]. If correct, examining the would carry out quantitative analyses velopments in cognitive neuroscience and relationship between evolved psychologi- across a multitude of behavioural and genetics open up further opportunities for cal mechanisms and reproductive success cognitive traits to measure to what extent, a broader EP. in modern environments will not neces- or on what occasions, human behaviour is iv) As discussed earlier, development is an sarily be an unproductive task. currently adaptive (e.g., [89]). We antici- extremely important factor in human Consistent with this hypothesis is the pate that the formal methods of human cognition, and the human mind is built observation that humans have experienced behavioural ecology are likely to be via a constant interplay between the extraordinary levels of population growth, productive even in modern societies, in individual and its environment. Recent indicative of increments in absolute fitness, many instances (e.g., [90,91]). Where the work by developmental psychologists dem-

PLoS Biology | www.plosbiology.org 5 July 2011 | Volume 9 | Issue 7 | e1001109 . onstrates how it is possible to detect the neled in a context specific manner is evolutionary novelty to which social sci- unlearned roots of cognition, such as deep, unclear. Innovation could instead be entists can actively participate. explicit conceptual understanding, reliant on domain-general mechanisms through careful experimentation on young expressed in complex cognition, intelli- Conclusions children [44]. Such experiments also gence and learning; for instance, innova- reveal the manner in which culturally tion could involve learned behaviour None of the aforementioned scientific and individually variable concepts emerge, patterns being adapted to a new domain. developments render evolutionary psy- through domain-general learning akin to Available evidence suggests the latter chology unfeasible; they merely require bootstrapping, in response to a culturally scenario [76,101]. that EP should change its daily practice. constructed, symbolically encoded envi- Similarly, EP has engaged in a long- The key concepts of EP have led to a series ronments [44]. In principle, all posited standing debate with advocates of cultural of widely held assumptions (e.g., that evolved psychological mechanisms, from evolution over whether human social human behaviour is unlikely to be adap- fear of snakes to cheater-detection mech- learning is governed by evolved content tive in modern environments, that cogni- anisms, could be subject to the same kind biases (e.g., choose the sugar-rich food) or tion is domain-specific, that there is a of detailed developmental investigation. by domain-general context biases (e.g., universal human nature), which with the Recent trends in developmental biology conform to the local norm). There is benefit of hindsight we now know to be and cognitive neuroscience recognize that sufficient empirical evidence for the de- questionable. A modern EP would em- the human brain and behaviour are ployment of context biases, such as brace a broader, more open, and multi- shaped to an important extent by individ- conformity or prestige bias, to render the disciplinary theoretical framework, draw- ual and social learning [36]. Hitherto, EP’s casual dismissal of transmitted culture ing on, rather than being isolated from, theoretical stance led it to assume domain counterproductive [102,103]. A broader the full repertoire of knowledge and tools specificity in cognition, resulting in the EP could actively pursue these questions, available in adjacent disciplines. Such a neglect of opportunities to investigate to by testing experimentally whether human field would embrace the challenge of what extent human social and asocial social learning is dominated by content or exploring empirically, for instance, to what learning are reliant upon processes that context biases, and by investigating the extent human cognition is domain-general apply across domains, or the manner in factors that affect reliance on each. The or domain specific, under what circum- which cross-domain general learning pro- finding that innovation, social learning, stances human behaviour is adaptive, how cesses build on domain-specific inputs. For and other aspects of development are best to explain variation in human behav- instance, while behavioural innovation is capable of introducing novelty into phe- iour and cognition. The evidence from critical to the survival of animals living in notype design space, thereby establishing adjacent disciplines suggests that, if EP can changing and unpredictable environ- new selective scenarios [39,41,48], opens reconsider its basic tenets, it will flourish as ments, whether such innovation is chan- up new opportunities for investigating a scientific discipline.

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