PAPER Evolutionary neuroscience of cumulative culture COLLOQUIUM Dietrich Stouta,1 and Erin E. Hechtb,c aDepartment of Anthropology, Emory University, Atlanta, GA 30322; bCenter for Behavioral Neuroscience, Georgia State University, Atlanta, GA 30303; and cYerkes National Primate Research Center, Emory University, Atlanta, GA 30302-5090 Edited by Marcus W. Feldman, Stanford University, Stanford, CA, and approved May 1, 2017 (received for review January 12, 2017) Culture suffuses all aspects of human life. It shapes our minds and clear why this exceptional capacity for culture has evolved in hu- bodies and has provided a cumulative inheritance of knowledge, mans and humans alone. skills, institutions, and artifacts that allows us to truly stand on the If there is one thing on which IC and CE agree, it is that shoulders of giants. No other species approaches the extent, cultural capacity is a good thing: It has “undeniable practical diversity, and complexity of human culture, but we remain unsure advantages” (8) that have allowed our species to have “expanded how this came to be. The very uniqueness of human culture is both across the globe and...occupy a wider range than any other ter- a puzzle and a problem. It is puzzling as to why more species have restrial species” (2). Indeed, the benefits are so substantial that not adopted this manifestly beneficial strategy and problematic even small “initial increments” (8) in this direction are expected to because the comparative methods of evolutionary biology are generate powerful biocultural feedback leading to further brain ill suited to explain unique events. Here, we develop a more and cognitive evolution (2, 8). Proponents of a highly modular view particularistic and mechanistic evolutionary neuroscience approach of IC nevertheless argue that this feedback will lead to coordinated to cumulative culture, taking into account experimental, develop- enhancement across multiple domains (8). CE advocates similarly mental, comparative, and archaeological evidence. This approach suggest that evolved cognitive mechanisms (i.e., modules in a loose reconciles currently competing accounts of the origins of human sense) for social learning will lead to more general brain size and culture and develops the concept of a uniquely human technolog- intelligence increases to deal with increased amounts of “valuable ical niche rooted in a shared primate heritage of visuomotor cultural information” (2). So why are humans the only species to coordination and dexterous manipulation. have fallen into this virtuous cycle? Arguing from a CE perspective, Boyd and Richerson (11) brain evolution | cultural evolution | archaeology | imitation suggest that cumulative culture is rare because of the evolu- tionary costs of requisite social-learning mechanisms. According odern humans live in a culturally constructed niche of to this argument, accumulation must begin with simple skills that Martificial landscapes, structures, artifacts, skills, practices, are within the inventive potential of individuals. Insofar as such and beliefs accumulated over generations and beyond the ability simple skills could be socially learned using existing “low-fidelity” of any one individual to recreate in a lifetime (1, 2). Like the air mechanisms, any small increases in learning efficiency provided by we breathe, this cumulative cultural matrix is so immersive that it new high-fidelity social-learning mechanisms would be unlikely to is easy to forget it is there. However, this is the medium through pay for the (presumably high) metabolic and developmental costs which we grow, act, and think, and it exerts profound influences of those mechanisms. In this case, it would only be after accu- on human life across a range of behavioral (2), developmental mulation had already generated a sufficient body of complex, (3), and evolutionary (4) scales. How did our species find itself in difficult-to-learn, and useful cultural content that these expen- this remarkable situation? sive mechanisms would begin to pay for themselves. Boyd and Niche construction is not unique to humans (5), and many Richerson (11) thus suggest that high-fidelity social-learning animals reliably transmit behavioral traditions across generations capacities initially arose as a side effect (exaptation) of some other adaptation, such as behavior prediction for Machiavellian (1). In contrast, it is controversial whether any examples of social strategizing (12, 13). Although reasonable, this hypothesis nonhuman cumulative culture exist and all can agree that no is weakened by its reliance on assumptions regarding the cost of other species approaches the extent, diversity, and complexity of social-learning mechanisms and the rarity of social-cognitive pre- human culture (6, 7). Two kinds of explanations have been “ ” adaptations. In fact, the hypothesis does not so much explain the proposed for this disjunction. Individual cognition accounts rarity of cumulative culture as shift the puzzle to explaining the (IC) propose that humans accumulate more complex cultures rarity of preadaptations, like behavior prediction, which might also primarily because the biological evolution of greater intelligence be assumed to be quite generally beneficial. in human individuals has promoted innovation and allowed An alternative, IC-compatible proposal is that it is large brains mastery of more complex concepts and skills (7, 8). Alternatively, in general that are expensive, rather than social-learning capacities “cultural evolution” accounts (CE) propose that the difference in particular. Thus, Pinker (8) argues that human cognitive ex- arises from uniquely human psychological specializations for ceptionalism arises from the fortuitous fact that “hominid ances- “high-fidelity” social learning [e.g., theory of mind (ToM), imi- tors, more so than any other species, had a collection of traits that tation], which have enabled the lossless “ratchet-effect” of cul- had tilted the payoffs toward further investment in intelligence.” tural accumulation to supplant biology as humanity’s primary Whether such “intelligence” is thought to be composed of discrete mode of adaptation (2, 9). Both views recognize a role for social but tightly coevolving innate modules (8) or a general-purpose learning in reducing the costs of knowledge and skill acquisition, but they differ on the phylogenetic uniqueness (e.g., ref. 7 vs. ref. NEUROSCIENCE 9) and transformative power (e.g., ref. 2 vs. ref. 8) of human This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “The Extension of Biology Through Culture,” held November 16–17, 2016, at the high-fidelity social transmission. This plays out in starkly differ- Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering ent visions of cumulative culture as either a fundamental evo- in Irvine, CA. The complete program and video recordings of most presentations are available lutionary transition (cf. ref. 10) that altered the very medium of on the NAS website at www.nasonline.org/Extension_of_Biology_Through_Culture. human adaption (2), or just another “unique or extreme” bi- Author contributions: D.S. and E.E.H. wrote the paper. ological trait comparable to “the elephant’s trunk, the narwhal’s The authors declare no conflict of interest. ’ ’ This article is a PNAS Direct Submission. tusk, the whale s baleen, the platypus s duckbill, and the arma- ANTHROPOLOGY dillo’sarmor” (8). Neither option, however, makes it immediately 1To whom correspondence should be addressed. Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1620738114 PNAS | July 25, 2017 | vol. 114 | no. 30 | 7861–7868 Downloaded by guest on September 29, 2021 capacity only “secondarily” specialized by experience (14), the on the complexity and difficulty of the production process. premise is that bigger brains are generally advantageous but can Transmission chains building spaghetti towers and paper air- only evolve under a narrow set of conditions. Lifespans must be planes achieve sufficient fidelity for cumulative improvement long enough (i.e., mortality low enough) to reward early invest- even in purely end-state emulative (i.e., reverse engineering) ments in growth and additional energetic costs must be accom- conditions (23), whereas more challenging tasks—such as de- modated through increased intake or reallocation (4). For many signing virtual “fishing nets” (24), building real weight-bearing species, constraints such as small body size, unstable environ- devices (25), and reproducing particular artifact forms (26)— ments, and unavoidable mortality from predation and disease may may require imitative copying of specific actions or processes. simply make large brains impractical. In this framework, high- Interactions between particular tasks demands, required fidelity, fidelity social learning can increase the payoffs of large brains and sufficient mechanisms are critical to the interpretation of (8, 15) but is not associated with its own unique costs, as it is comparative and evolutionary evidence, yet remain underex- thought to rely on cognitive abilities that overlap (15) or evolved in plored and undertheorized. The objective is obviously to move tandem with (8) asocial learning and problem solving. This ap- from particularistic analyses of specific behaviors to identifica- proach actually parallels the suggestion of Boyd and Richerson tion of general principles, yet it is not obvious how to design or (11) that