The origins of human cumulative culture: from the foraging niche to collective intelligence

Various studies have investigated cognitive mechanisms underlying culture in humans and other great apes. However, the adaptive reasons for the evolution of uniquely sophisticated cumulative culture in our species remain unclear. We propose that the cultural capabilities of humans are the evolutionary result of a stepwise transition from the ape-like lifestyle of earlier hominins to the foraging niche still observed in extant hunter–gatherers. Recent ethnographic, archaeological and genetic studies have provided compelling evidence that the components of the foraging niche (social egalitarianism, sexual and social division of labour, extensive co-residence and cooperation with unrelated individuals, multilocality, fluid sociality and high between-camp mobility) engendered a unique multilevel social structure where the cognitive mechanisms underlying cultural evolution (high-fidelity transmission, innovation, teaching, recombination, ratcheting) evolved as adaptations. Therefore, multilevel sociality underlies a ‘social ratchet’ or irreversible task specialization splitting the burden of cultural knowledge across individuals, which may explain why human collective intelligence is uniquely able to produce sophisticated cumulative culture. The foraging niche perspective may explain why a complex gene-culture dual inheritance system evolved uniquely in humans and interprets the cultural, morphological and genetic origins of Homo sapiens as a process of recombination of innovations appearing in differentiated but interconnected populations. This article is part of a discussion meeting issue ‘The emergence of collective knowledge and cumulative culture in animals, humans and machines’.

Differential time allocation of foraging workers in the subterranean termite

Background Foraging in group living animals such as social insects, is collectively performed by individuals. However, our understanding on foraging behavior of subterranean termites is extremely limited, as the process of foraging in the field is mostly concealed. Because of this limitation, foraging behaviors of subterranean termites were indirectly investigated in the laboratory through tunnel geometry analysis and observations on tunneling behaviors. In this study, we tracked subsets of foraging workers from juvenile colonies of Coptotermes formosanus (2-yr-old) to describe general foraging behavioral sequences and to find how foraging workers allocate time between the foraging site (food acquisition or processing) and non-foraging site (food transportation). Results Once workers entered into the foraging site, they spent, on average, a significantly longer time at the foraging site than the non-foraging site. Our clustering analysis revealed two different types of foraging workers in the subterranean termite based on the duration of time they spent at the foraging site and their foraging frequency. After entering the foraging site, some workers (cluster 1) immediately initiated masticating wood fragments, which they transferred as food boluses to recipient workers at the foraging site. Conversely, the recipient workers (cluster 2) moved around after entering the foraging site and received food from donating workers. Conclusions This study provides evidence of task specialization within foraging cohorts in subterranean termites.

Biomarkers in a socially exchanged fluid reflect colony maturity, behavior and distributed metabolism

In cooperative systems exhibiting division of labor, such as microbial communities, multicellular organisms, and social insect colonies, individual units share costs and benefits through both task specialization and exchanged materials. Socially exchanged fluids, like seminal fluid and milk, allow individuals to molecularly influence conspecifics. Many social insects have a social circulatory system, where food and endogenously produced molecules are transferred mouth-to-mouth (stomodeal trophallaxis), connecting all the individuals in the society. To understand how these endogenous molecules relate to colony life, we used quantitative proteomics to investigate the trophallactic fluid within colonies of the carpenter ant Camponotus floridanus. We show that different stages of the colony life cycle circulate different types of proteins: young colonies prioritize direct carbohydrate processing; mature colonies prioritize accumulation and transmission of stored resources. Further, colonies circulate proteins implicated in oxidative stress, ageing, and social insect caste determination, potentially acting as superorganismal hormones. Brood-caring individuals that are also closer to the queen in the social network (nurses) showed higher abundance of oxidative stress-related proteins. Thus, trophallaxis behavior could provide a mechanism for distributed metabolism in social insect societies. The ability to thoroughly analyze the materials exchanged between cooperative units makes social insect colonies useful models to understand the evolution and consequences of metabolic division of labor at other scales.

A Structural Model of a Multitasking Salesforce: Incentives, Private Information, and Job Design

This paper broadens the focus of empirical research on salesforce management to include multitasking settings with multidimensional incentives, where salespeople have private information about customers. This allows us to ask novel substantive questions around multidimensional incentive design and job design while managing the costs and benefits of private information. To this end, the paper introduces the first structural model of a multitasking salesforce in response to multidimensional incentives. The model also accommodates (i) dynamic intertemporal tradeoffs in effort choice across the tasks and (ii) salesperson’s private information about customers. We apply our model in a rich empirical setting in microfinance and illustrate how to address various identification and estimation challenges. We extend two-step estimation methods used for unidimensional compensation plans by embedding a flexible machine learning (random forest) model in the first-stage multitasking policy function estimation within an iterative procedure that accounts for salesperson heterogeneity and private information. Estimates reveal two latent segments of salespeople—a hunter segment that is more efficient in loan acquisition and a farmer segment that is more efficient in loan collection. Counterfactuals reveal heterogeneous effects: hunters’ private information hurts the firm as they engage in adverse selection; farmers’ private information helps the firm as they use it to better collect loans. The payoff complementarity induced by multiplicative incentive aggregation softens adverse specialization by hunters relative to additive aggregation but hurts performance among farmers. Overall, task specialization in job design for hunters (acquisition) and farmers (collection) hurts the firm as adverse selection harm overwhelms efficiency gain. This paper was accepted by Duncan Simester, marketing.

Morphological determinants of bite force capacity in insects: a biomechanical analysis of polymorphic leaf-cutter ants

The extraordinary success of social insects is partially based on division of labour, i.e. individuals exclusively or preferentially perform specific tasks. Task preference may correlate with morphological adaptations so implying task specialization, but the extent of such specialization can be difficult to determine. Here, we demonstrate how the physical foundation of some tasks can be leveraged to quantitatively link morphology and performance. We study the allometry of bite force capacity in Atta vollenweideri leaf-cutter ants, polymorphic insects in which the mechanical processing of plant material is a key aspect of the behavioural portfolio. Through a morphometric analysis of tomographic scans, we show that the bite force capacity of the heaviest colony workers is twice as large as predicted by isometry. This disproportionate ‘boost’ is predominantly achieved through increased investment in muscle volume; geometrical parameters such as mechanical advantage, fibre length or pennation angle are likely constrained by the need to maintain a constant mandibular opening range. We analyse this preference for an increase in size-specific muscle volume and the adaptations in internal and external head anatomy required to accommodate it with simple geometric and physical models, so providing a quantitative understanding of the functional anatomy of the musculoskeletal bite apparatus in insects.

Soldier neural architecture is temporarily modality-specialized but poorly predicted by repertoire size in the stingless bee Tetragonisca angustula

Individual heterogeneity within societies provides opportunities to test hypotheses about adaptive neural investment in the context of group cooperation. Here we explore neural investment in defense specialist soldiers of the eusocial stingless bee (Tetragonisca angustula) which are age sub-specialized on distinct defense tasks, and have an overall higher lifetime task repertoire than other sterile workers within the colony. Consistent with predicted behavioral demands, soldiers had higher relative visual (optic lobe) investment than non-soldiers but only during the period when they were performing the most visually demanding defense task (hovering guarding). As soldiers aged into the less visually demanding task of standing guarding this difference disappeared. Neural investment was otherwise similar across all colony members. Despite having larger task repertoires, soldiers had similar absolute brain size and smaller relative brain size compared to other workers, meaning that lifetime task repertoire size was a poor predictor of brain size. Together, our results are consistent with the specialized but flexible defense strategies of this species, broadening our understanding of how neurobiology mediates age and morphological task specialization in highly cooperative societies.

The geometry of domain-general performance monitoring representations in the human medial frontal cortex

Flexibly adapting behavior to achieve a desired goal depends on the ability to monitor one's own performance. A key open question is how performance monitoring can be both highly flexible to support multiple tasks and specialized to support specific tasks. We characterized performance monitoring representations by recording single neurons in the human medial frontal cortex (MFC). Subjects performed two tasks that involve three types of cognitive conflict. Neural population representations of conflict, error and control demand generalized across tasks and time while at the same time also encoding task specialization. This arose from a combination of single neurons whose responses were task-invariant and non-linearly mixed. Neurons encoding conflict ex-post served to iteratively update internal estimates of control demand as predicted by a Bayesian model. These findings reveal how the MFC representation of evaluative signals are both abstract and specific, suggesting a mechanism for computing and maintaining control demand estimates across trials and tasks.