The emergence of collective knowledge and cumulative culture in animals, humans and machines.

Abstract

Open AccessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Whiten Andrew, Biro Dora, Bredeche Nicolas, Garland Ellen C. and Kirby Simon 2022The emergence of collective knowledge and cumulative culture in animals, humans and machinesPhil. Trans. R. Soc. B3772020030620200306http://doi.org/10.1098/rstb.2020.0306SectionOpen AccessIntroductionThe emergence of collective knowledge and cumulative culture in animals, humans and machines Andrew Whiten Andrew Whiten http://orcid.org/0000-0003-2426-5890 Centre for Social Learning and Cognitive Evolution, School of Psychology and Neuroscience, Scottish Oceans Institute, School of Biology, University of St Andrews, St Andrews, UK [email protected] Google Scholar Find this author on PubMed Search for more papers by this author , Dora Biro Dora Biro http://orcid.org/0000-0002-3408-6274 Department of Zoology, University of Oxford, Oxford, UK Department of Brain and Cognitive Sciences, University of Rochester, Rochester, NY, USA Google Scholar Find this author on PubMed Search for more papers by this author , Nicolas Bredeche Nicolas Bredeche http://orcid.org/0000-0002-8241-7461 Sorbonne Université, CNRS, Institut des Systèmes Intelligents et de Robotique, ISIR, 75005 Paris, France Google Scholar Find this author on PubMed Search for more papers by this author , Ellen C. Garland Ellen C. Garland http://orcid.org/0000-0002-8240-1267 Centre for Social Learning and Cognitive Evolution, and Sea Mammal Research Unit, Scottish Oceans Institute, School of Biology, University of St Andrews, St Andrews, UK Google Scholar Find this author on PubMed Search for more papers by this author and Simon Kirby Simon Kirby http://orcid.org/0000-0002-6496-1340 Centre for Language Evolution, University of Edinburgh, Edinburgh, UK Google Scholar Find this author on PubMed Search for more papers by this author Andrew Whiten Andrew Whiten http://orcid.org/0000-0003-2426-5890 Centre for Social Learning and Cognitive Evolution, School of Psychology and Neuroscience, Scottish Oceans Institute, School of Biology, University of St Andrews, St Andrews, UK [email protected] Google Scholar Find this author on PubMed Search for more papers by this author , Dora Biro Dora Biro http://orcid.org/0000-0002-3408-6274 Department of Zoology, University of Oxford, Oxford, UK Department of Brain and Cognitive Sciences, University of Rochester, Rochester, NY, USA Google Scholar Find this author on PubMed Search for more papers by this author , Nicolas Bredeche Nicolas Bredeche http://orcid.org/0000-0002-8241-7461 Sorbonne Université, CNRS, Institut des Systèmes Intelligents et de Robotique, ISIR, 75005 Paris, France Google Scholar Find this author on PubMed Search for more papers by this author , Ellen C. Garland Ellen C. Garland http://orcid.org/0000-0002-8240-1267 Centre for Social Learning and Cognitive Evolution, and Sea Mammal Research Unit, Scottish Oceans Institute, School of Biology, University of St Andrews, St Andrews, UK Google Scholar Find this author on PubMed Search for more papers by this author and Simon Kirby Simon Kirby http://orcid.org/0000-0002-6496-1340 Centre for Language Evolution, University of Edinburgh, Edinburgh, UK Google Scholar Find this author on PubMed Search for more papers by this author Published:13 December 2021https://doi.org/10.1098/rstb.2020.0306This article has a CorrectionCorrectionCorrection to ‘The emergence of collective knowledge and cumulative culture in animals, humans and machines’https://doi.org/10.1098/rstb.2022.0020 Andrew Whiten, Dora Biro, Nicolas Bredeche, Ellen C. Garland and Simon Kirby volume 377issue 1850Philosophical Transactions of the Royal Society B: Biological Sciences21 March 20221. IntroductionThe goal of this themed issue and the associated Royal Society and British Academy joint Discussion Meeting is to advance, and bridge between, two topics and their respective research fields that have burgeoned in recent years, although to date they have often done so quite separately. One field is concerned with collective action, collective intelligence and collective knowledge among groupings of individuals; phenomena in which significantly more is achieved by the collective than is possible for any one individual alone. Their manifestations and mechanisms have been studied across populations of the kinds of non-human animals (henceforth ‘animals’), humans and machines that are the subject matter of this issue. These have been flagged by a variety of expressions across animal and human studies including, for example, ‘consensus decision-making’ [1], ‘the wisdom of the hive’ [2], ‘quorum decision-making’ [3], ‘emergent sensing’ [4], ‘collective intelligence’ [5], ‘the wisdom of the crowd’ [6], ‘collective brain’ [7], ‘group cognition’ and ‘extended mind’ [8,9], ‘group-mindedness’ and ‘collective intentionality’ [10]. In artificial intelligence research there is ‘swarm robotics’ and ‘collective robotics’ [11–17]. For Mulgan [18], ‘Big Mind’ includes both the latter two domains, integrated in the collective intelligence generated through large-scale human–machine interactions. Few attempts have been made to integrate the contributions reflected in this diversity of terminologies. In this issue, we address the emergence and evolution of these phenomena, appraising commonalities and differences among them.The second field of interest covers the emergence and evolution of the collective entity we call culture—the creation, transmission and spread of traditions through social learning (learning from others), in humans, animals and machines. Culture has long been presented as a unique defining feature of humans [19,20]. It pervades virtually every aspect of what it is to be human [21,22]. Yet, recent decades have revealed that culture, defined as above, plays a significant role in the lives of numerous vertebrate taxa and perhaps of invertebrates (notably insects) too [23–27]. The study of social learning in robots, reviewed in this issue [28–30] also raises the prospect of cultural evolution in the world of machines.The research literatures focused, respectively, on collective knowledge and culture (including each of the animal, human and machine research streams within them) have been built largely as separate endeavours. In this issue, we seek not only to extend them but also to examine emerging links between them. Exploring such connections, Biro et al. [31] pointed out a largely overlooked aspect of collective animal behaviour: that many of the collective outcomes that have been identified may be contingent on the collective's previous history and collective memory. Collective knowledge may change over time when the same group members solve the same task repeatedly, or across partial turnovers in group membership, amounting to the emergence of a group culture. This may in turn extend to cultural transmission of collective knowledge across generations. Any additional extensions in such collective cultural knowledge may in turn evidence cumulative culture.An example of such processes in action was provided by an experiment with homing pigeons [32]. In this study, two pigeons were first repeatedly tracked as they made homing flights. Then, one of the pair was replaced by a naive bird and the new combination again flew repeated flights, before the most experienced was again replaced by a naive bird. Later pairs of pigeons in these transitions were thus different to those flying earlier in the sequence, yet homing flight paths became increasingly efficient and direct over time. The experiment accordingly demonstrated (i) the transmission, across pairings, of information underlying good flight paths generated up to that point; (ii) a capacity of consecutive pairs not only to share this information, but in interaction, improve it; and thence (iii) create cumulative cultural progress across the whole sequence of repeated replacement pairings.How might such processes play out in nature? Long-term records of wild bighorn sheep suggest one answer [33]. In the United States, groups of these animals were translocated, sometimes as much as two centuries ago, to areas in which the species had been extirpated. Here, in territory unknown to them, they failed to exhibit the annual ‘green wave surfing’ in which these animals normally pursue a series of higher and higher altitude springtime patches of graze. However, this behaviour re-emerged in the translocated populations, and the knowledge and skill underlying the ability to optimize foraging movements in time and space was found to grow progressively over decades and over generations. The authors concluded ‘that ungulates accumulate knowledge of local phenological patterns over time via the ‘ratcheting effect’ wherein each generation augments culturally transmitted information with information gained from their own experience, a process known as cumulative cultural evolution’ ([33, p. 1024], citing [34]).2. Core research questionsSuch emerging links between the topics of collective behaviour, knowledge sharing, collective knowledge generation and culture, and a range of other relevant advances in studies of animals, humans and machines lead us to pursue a set of core questions as follows: — how do collectives, whether of animals, humans, robots or other machines achieve shared levels of knowledge/information, beyond those accessible to constituent individuals acting alone?— in what ways and under what conditions are these processes extended temporally, such that collective contributions are maintained and persist over significant time depths?— to what extent and in what ways do these kinds of collectives create new behaviours or artefacts when they combine and integrate different contributions from different individuals, and do these spread via social learning? and— in what ways may these phenomena recur across multiple generations of cultural transmission, creating the potential for extended cumulative cultural transmission?Of course, many more specific but related questions are addressed in the articles assembled in this issue. We do not provide extended summaries of these articles here. Prospective readers can consult the abstracts. Instead, we outline the key background literature and briefly indicate how the articles in the issue relate to and advance these.3. Collective behaviour, knowledge and culture among non-human animalsMuch of the animal literature to date focuses either on collective phenomena per se, or on culture-related phenomena, and accordingly we introduce these separately here.(a) Collective behaviour and knowledge in animalsAn extensive literature has accumulated, particularly this century, analysing collective actions in animals. Contexts studied include the collective movements of large aggregates (bird flocks, fish schools, insect swarms and ungulate herds [35–37]), collective construction (foraging trail networks, social insect nests and even structures composed of the bodies of the animals themselves, such as ant-bridges [38–40]), the timing and coordination of collective activities (the emergence of synchrony in firefly flashing and in predator evasion [41,42]) and collective decision-making in the group's choice of when, where and what actions to implement [43]. Key principles identified emphasize that much of collective animal behaviour is ‘self-organized’ [44], relying on relatively simple local interactions of individuals with their neighbours and with the environment, in the absence of any ‘global’ overseer or leader. Complex, robust and scalable group-level phenomena emerge that are not necessarily predictable from observing any single individual by itself.In this issue, we are additionally focused on contexts in which information is linked collectively in ways that evoke such terms as ‘collective memory’ [45], ‘collective decision making’ and ‘collective minds’ [46]. The justification for such references to concepts of cognition and knowledge, even where the cognitive powers of individual animals or robots may be relatively elementary, can be illustrated in an analysis of chemical communication among ants [47]. Ants mark trails with pheromones of both low and high volatility, allowing collective route maps to be accumulated and refined over time. This provides both long-term memories of potentially useful foraging routes, and short-term memories coding currently valuable routes to resources. The latter ‘working memory’ facilitates the ‘attention’ of the colony as a whole, adaptively guiding the workforce's learning and exploitation as resource distributions change.Collective decision-making has been extensively studied in the context of negotiated route choices, in situations where component individuals initially express different preferences based on their personal knowledge to date. For example, despite living in societies heavily structured by dominance relationships, at a fine spatio-temporal scale baboons are more likely to follow routes suggested by multiple individuals than to follow the most dominant [48]. When directions suggested in the actions of initiators differ by only relatively small angles, the group typically follows a compromise direction between them, but if the angle is large, just one is chosen. The latter choice tends to occur as a majority of the group progressively express a preference for it. The pattern of ‘compromise’ decisions being made when the angle of disagreement is small, and a ‘winner takes all’ decision emerging when it is large, has been found in a variety of analogous contexts and species, including the choice of homing paths in pigeons [49] and of travel directions in wild vulturine guineafowl [50]. Similarly, the principle of the numerical majority dictating the group consensus is a well-known effect characterizing the selection of new nest sites by colonies of honeybees and ants [51,52], and has also been shown in human crowds instructed to follow a set of simple behavioural rules simulating those underlying collective animal movement [53].In these cases, individuals often vary in their knowledge of a single factor, such as the location of a resource like fruiting trees or nest-sites. However, knowledge concerning different factors might be in play even in contexts like those outlined above: for example, some baboons may try to initiate movement towards a food resource they know of, while others initiate alternative routes to avoid an area they know has recently been frequented by a significant predator. Some individuals may know about only one of these, yet the group as a whole may be able to generate an adaptive overall response that weights both factors. Indeed, the specific weighting that different individuals' inputs receive may vary according to their current physiological needs, motivational states, or the reliability of their information, leading to more flexible integration of pooled preferences [54]. For example, in plains zebras, lactating females—i.e. those with the highest water and energy needs—are more likely to influence the herd's movements than non-lactating ones [55].Alternatively, collective responses can also be the cumulative output of individual inputs rather than their (weighted) average. The potential complexities of such additive effects are challenging to tease apart in nature, but have been explored in controlled experimental contexts. For example, Webster et al. [56] tested sticklebacks faced with a two-step task in which the first step was navigating through a structured environment to a food patch, and the second step was accessing the food by swimming through a small hole. Some shoals contained only entirely naive fish, whereas others mixed naive fish with fish already experienced in the navigation step only, or experienced in the food access step only. In a fourth combination, the group included equal numbers of naive fish, and others trained in either navigation-only or food access-only. Results clearly showed that these mixtures were superior to the others in the proportion of the group successfully entering the feeder and the speed with which they were able to do so, demonstrating what the authors describe as adaptive ‘experience pooling’.Although not tracked in that study, from what we know of social learning in fishes [57], all the fish whose discovery of this foraging innovation was enhanced by the experience pooling would probably be more successful at the task subsequently, implicating a form of social transmission. Such effects illustrate one potential link between collective knowledge, social learning and culture, when a perspective with some time-depth is taken. Outstanding key questions concern the role of the collective (its size, composition, stability and life history) in generating new information not discoverable by single individuals, the role of individual heterogeneity in where and how much of this information is stored as the group's ‘collective memory’, the time-depth of the latter, and context-dependent effects on the retrieval and execution of appropriate behavioural solutions in collectively learnt tasks.(b) Social learning and culture in animalsCulture was defined above as the creation and spread of traditions through social learning (learning from others). Traditions can in turn be defined as behaviours, artefacts or other entities that are shared within a community and maintained over significant periods, including across generations. Once thought unique to humans, over the last 70 years or so, culture conceptualized in this way has been discovered to play a significant part in the lives of an ever-expanding range of animal taxa including a variety of mammals, birds, reptiles and fishes [23–27]. Such evidence has emerged in some cases through the accumulation of long-term field studies, but also through the refinement of a diverse portfolio of methodologies, from controlled experiments in both laboratory and field, to statistical techniques to identify the signature of cultural transmission in the ways that innovations spread preferentially through social networks [58]. Here it is important to recognize the distinction between evidence for social learning per se, and that required to identify cultural transmission, through the demonstration of repeated episodes of social learning as innovations diffuse within and/or across groups and generations. Much of what animals learn socially may have only transient significance, such as the location of a short-lived resource, and never become the basis for a tradition. The identification of social learning of a preference for particular flowers by bumblebees [59], for example, thus does not in itself establish culture. However, laboratory-based experiments have gone on to demonstrate cultural transmission along chains of learners, including in the foraging behaviour of bumblebees [60] and mate-choice copying of fruit flies [61]. What remains unclear is the reach of culture in insects' lives in the wild.In vertebrates, the diversity of behavioural repertoires found to be shaped by cultural transmission has progressively expanded alongside its taxonomic diversity. Examples include foraging techniques [62,63], tool use [64,65], vocal communication [66,67], social customs [68,69], preferences for particular prey [70] and other dietary items [71], migratory pathways and destinations [72,73] and mate characteristics [61].Cultural transmission spans not only this diversity of functions but may also pervade successive phases of animals’ life history. In species with parental care, much appears to be transmitted during this initial phase of dependence, but in group-living animals ‘horizontal’ transmission between peers and ‘oblique’ transmission from non-parental adults can be important at later ages, including a renewed role for learning from others as adults disperse to new groups and ranges unfamiliar to them [71,74]. A recent book-length review of the accumulating evidence for cetaceans concluded that culture so permeates whales' lives that ‘culture is a major part of what the whales are’ [23, p. 17]. In similar vein, Schuppli & van Schaik [75] argue that prior approaches to identifying the scope of ape cultures that rested on comparing different communities have much underestimated the role of culture in these animals' lives, neglecting local ecological adaptations and cultural universals. By instead logging all the contexts in which juveniles closely peered at adult behaviour patterns, a measure the authors earlier validated as indexing social learning, studies of two orangutan populations indicated as many as 125 and 190 culturally transmitted behaviours, respectively. The authors concluded ‘that immatures learn virtually all of their skills socially’ [75, p. 5].Culture may pervade many animals' lives, but does it evolve, as human culture so manifestly does? The answer depends in part on what counts as evolution. If, as can be the case in evolutionary biology, we are talking of only cultural change, then there is growing evidence for the occurrence of cultural evolution among animals, as long-term studies accumulate [25,27]. Changes in birdsong logged over periods that have now extended over several decades have provided the greatest number of peer-reviewed publications that index ‘cultural evolution’ in their titles [25]. Long-term changes were also identified in the spread of a ‘lob-tail’ technique of predation in humpback whales over 26 years [63], but some changes can be much faster, as when a new form of sponge-making to aid drinking emerged and spread in chimpanzees over only approximately a single week [76].Human scientific lives are short compared to many of the potential evolutionary changes (whether based on genetic or cultural inheritance) that interest us. Archaeology has begun to change this somewhat for animals, as it has for human cultural change. Archaeological excavations focused on the types of stones used to crack nuts by modern-day bearded capuchins pointed to four different evolutionary phases spanning 3000 years, marked by changes in size, wear, percussive battering and anvil types [77].A more demanding concept of cultural evolution requires it to be cumulative, such that ‘some measure of performance’ is progressively enhanced [78, p. 2]. In our introduction, we already noted two quite different examples of this, an experimental study of pigeon homing [32] and an analysis of long-term records of green wave surfing skill in bighorn sheep [33]. Both of these concern enhancements in movement efficiency, but other examples have begun to extend the diversity of species and behavioural arenas in which such cumulative cultural change has been identified. One such study showed cumulative cultural evolution (CCE) in the capacity of baboons to recognize and transmit visual patterns, in an analogue of similar changes in the cultural evolution of artificial languages in human experiments [79,80]. Another study tracked changes in the songs of humpback whales over 12 years, during which periods of rising complexity alternated with falls occurring when radically new songs (cultural revolutions) emerged [81]. All such cases are suggestive of collective contributions of different animals' innovations to cumulative cultural change, across significant time-depths. That of the humpback whales is pursued in greater depth in this issue [82].4. Collective knowledge and cumulative culture in humansStudying the wisdom of collectives is often traced back to Galton [83], who showed that the sometimes widely differing estimates of the weight of an ox at a county fair, when averaged, came surprisingly to within 1% of the true weight. Since that time, studies of a variety of related collective cognitive phenomena have generated large and growing literatures in fields as varied as economics, psychology, sociology, law, political science and anthropology [84]. However, ‘culture’ was not even indexed in the latter ‘Handbook of collective intelligence’.Similarly, collective knowledge/intelligence was not in the index of the most recent wide-ranging compilation of research findings from the field of human cultural evolution [85]. The study of cultural evolution can be traced at least as far back as works by Schleicher [86] concerning language evolution, well known to Darwin [87]. With time, evolutionary analyses were extended to fields such as weaponry and other technologies [88]. The modern field of cultural evolution is generally traced to foundational systematic analyses by Cavalli-Sforza & Feldman [89] and Boyd & Richerson [90], its maturation marked in 2017 by the first international conference of a ‘Cultural Evolution Society’. A growing number of studies have, however, begun to integrate the topic of collective knowledge with that of culture [91]. Here, we introduce examples that offer foundations for articles in this issue that carry this work forwards.(a) Inferences about collective information and culture in past and present foraging societiesTwo very different empirical sources, both represented in this issue, focus particularly on reconstructing our evolutionary past. There is an important complementarity between the two given the strengths and weaknesses of each. One is the archaeological record, including fossils, genomic material and particularly artefacts dating from the stone age to the present day [92]. The artefacts provide us with a progressively more detailed record of the evolution of human material culture, but limited inferences can be drawn about social matters such as collective action and knowledge. By contrast, rich data on the latter come from the study of present-day peoples dependent on the hunting and gathering (HG) ways of life that the archaeological material tells us characterized millennia of our species' recent history [93]. However, the cultures of these communities tend to be very stable, revealing little of evolutionary change, whereas change permeates the archaeological record of the last few million years. The two perspectives thus enrich and inform each other in multiple ways.Studies of Hadza HG in Africa and Ache HG in South America suggest that the collective cultural knowledge of these peoples is structured in significant ways by forms of social interaction that differ much from those of great apes [94]. These include intermittent and friendly interactions between bands. Estimates from quantitative studies of these peoples suggest that across their lifetimes, Hadza and Ache men are likely to be able to observe as many as 300 men engaged in tool making across different bands. This contrasts strikingly with the lives of male chimpanzees, whose inter-community relationships are extremely intolerant and typically marked by lethal raiding. Hill et al. [94] suggested that the scale of information exchange observed in HG societies is likely to have been a key factor in facilitating cultural transmission and particularly the scope for CCE to take place.Parallel conclusions have been derived from archaeologically based analyses identifying correlations between reconstructed demographic changes and major transitions in material culture in late Pleistocene times [95]. Population densities and migration patterns inferred from genomic data were shown to attain levels predicted to promote marked acceleration in cumulative cultural change at two significant spatio-temporal junctures. The more recent, at approximately 45 ka in Europe and western Asia, represents the Upper Palaeolithic transition marked by an extensive cluster of cultural advances including fine stone tools and sophisticated weaponry like spear throwers, together with realistic art and body decoration materials. The earlier juncture, around approximately 100 ka, corresponds to what are thought to be the first archeological signatures of such cultural advances in Africa.Of course these scenarios concern a much larger-scale inferred linkage between the promotion of collective knowledge through major demographic shifts and cultural advances, than the recent studies of HG populations. They also rely on a significant number of assumptions and inferential leaps, given the fragmentary nature of archaeological evidence bases. Studies of contemporary HG life, therefore, provide invaluable and complementary concrete observations of the collective and cultural phenomena of interest.For example, a study of the forms of usage of 33 plant species by 219 BaYaka HG individuals in Congo revealed a hierarchical structure in their collective knowledge [96]. Knowledge of medicinal usages are principally shared at the level of the family—between spouses and both biological and affinal kin, whereas collective knowledge concerning social norms such as ritual usage, and foraging requirements, occurs at the level of the camp. The authors proposed that multi-family camps provide a framework facilitating the exchange of social and functional information and ultimately potentials for cumulative cultural change.Wireless sensing technology, in which small ‘mote’ devices worn by individuals provide objective information on social networks across large populations, have now been used to delineate such multiple-level HG social structures in detail [97]. For the 53 adults in seven Agta camps in forests in the Philippines, 59% of all the possible close dyadic interactions were recorded as occurring within a band in a single month, plus an additional 28% of the possible dyadic interactions between camps. For 37 adults in three coastal camps, the equivalent figures were 85% and 56%.A number of studies converge to suggest that such hierarchical structuring may facilitate CCE because