The proximate regulation of prosocial behaviour: towards a conceptual framework for comparative research.

Humans and many other animal species act in ways that benefit others. Such prosocial behaviour has been studied extensively across a range of disciplines over the last decades, but findings to date have led to conflicting conclusions about prosociality across and even within species. Here, we present a conceptual framework to study the proximate regulation of prosocial behaviour in humans, non-human primates and potentially other animals. We build on psychological definitions of prosociality and spell out three key features that need to be in place for behaviour to count as prosocial: benefitting others, intentionality, and voluntariness. We then apply this framework to review observational and experimental studies on sharing behaviour and targeted helping in human children and non-human primates. We show that behaviours that are usually subsumed under the same terminology (e.g. helping) can differ substantially across and within species and that some of them do not fulfil our criteria for prosociality. Our framework allows for precise mapping of prosocial behaviours when retrospectively evaluating studies and offers guidelines for future comparative work.

Wild and captive immature orangutans differ in their non-vocal communication with others, but not with their mothers.

Abstract: In many group-living species, individuals are required to flexibly modify their communicative behaviour in response to current social challenges. To unravel whether sociality and communication systems co-evolve, research efforts have often targeted the links between social organisation and communicative repertoires. However, it is still unclear which social or interactional factors directly predict communicative complexity. To address this issue, we studied wild and zoo-housed immature orangutans of two species to assess the impact of the socio-ecological setting on the production of non-vocal signal repertoires. Specifically, we compared repertoire size, dyadic repertoire similarity, and number of social goals (i.e. observer's estimate of the signaller's intended interaction outcome) for communicative interactions with mothers versus other conspecifics, controlling for critical individual and environmental factors. In this small sample of immature orangutans, wild-captive contrasts were statistically significant only for other-directed repertoires, but not for mother-directed repertoires, and not for the number of social goals that immatures communicated towards. While the repertoires of individuals living in the same research setting were more similar than those living in contrasting settings, this difference was most pronounced for other-directed repertoires of the less socially tolerant orangutan species. These results suggest that the boosted interactional opportunities in captivity rather than mere differences in environmental affordances or communicative needs drive the wild-captive contrast in orangutan communicative repertoires. Overall, this fine-grained analysis of repertoires further underscores that not only a species' social organisation but also the targeted audience may have a profound impact on communicative behaviour. Significance statement: Navigating a dynamic social environment often requires flexible signal use. While it has repeatedly been shown that the social organisation and structure of species predict the complexity of their communication systems, the mechanisms underlying these relationships are largely unknown. Because targeted studies to assess this issue in great apes are difficult, we take an alternative approach here: we compare the same species living in the wild and in artificial habitats in captivity. This contrast allows a direct test of how repertoires respond to the relevant difference in socio-ecological conditions. Our results show that the diversity of interaction partners (i.e. social opportunities), but not the diversity of social goals (i.e. possible interaction outcomes) or the broader physical opportunities (i.e. safe ground use), predict the size and consistency of wild and captive signalling repertoires. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-023-03426-3.

Reproductive success of Bornean orangutan males: scattered in time but clustered in space.

Abstract: The social and mating systems of orangutans, one of our closest relatives, remain poorly understood. Orangutans (Pongo spp.) are highly sexually dimorphic and females are philopatric and maintain individual, but overlapping home ranges, whereas males disperse, are non-territorial and wide-ranging, and show bimaturism, with many years between reaching sexual maturity and attaining full secondary sexual characteristics (including cheek pads (flanges) and emitting long calls). We report on 21 assigned paternities, among 35 flanged and 15 unflanged, genotyped male Bornean orangutans (Pongo pygmaeus wurmbii), studied from 2003 to 2018 in Tuanan (Central Kalimantan, Indonesia). All 10 infants born since mid-2003 with an already identified sire were sired by flanged males. All adult males ranged well beyond the study area (c. 1000 ha), and their dominance relations fluctuated even within short periods. However, 5 of the 10 identified sires had multiple offspring within the monitored area. Several sired over a period of c. 10 years, which overlapped with siring periods of other males. The long-calling behavior of sires indicated they were not consistently dominant over other males in the area around the time of known conceptions. Instead, when they were seen in the area, the known sires spent most of their time within the home ranges of the females whose offspring they sired. Overall, successful sires were older and more often resident than others. Significance statement: It is difficult to assess reproductive success for individuals of long-lived species, especially for dispersing males, who cannot be monitored throughout their lives. Due to extremely long interbirth intervals, orangutans have highly male-skewed operational sex ratios and thus intensive male-male competition for every conception. Paternity analyses matched 21 immature Bornean orangutans with their most likely sire (only 10 of 50 genotyped males) in a natural population. Half of these identified sires had multiple offspring in the study area spread over periods of at least 10 years, despite frequently ranging outside this area. Dominance was a poor predictor of success, but, consistent with female mating tactics to reduce the risk of infanticide, known "sires" tended to have relatively high local presence, which seems to contribute to the males' siring success. The results highlight the importance of large protected areas to enable a natural pattern of dispersal and ranging. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-023-03407-6.

Does the expensive brain hypothesis apply to amphibians and reptiles?

Vertebrate brains show extensive variation in relative size. The expensive brain hypothesis argues that one important source of this variation is linked to a species' ability to generate the energy required to sustain the brain, especially during periods of unavoidable food scarcity. Here we ask whether this hypothesis, tested so far in endothermic vertebrates, also applies to ectotherms, where ambient temperature is an additional major aspect of energy balance. Phylogenetic comparative analyses of reptiles and amphibians support the hypothesis. First, relative brain size increases with higher body temperature in those species active during the day that can gain free energy by basking. Second, relative brain size is smaller among nocturnal species, which generally face less favorable energy budgets, especially when maintaining high body temperature. However, we do not find an effect of seasonal variation in ambient temperature or food on brain size, unlike in endotherms. We conclude that the factors affecting energy balance in ectotherms and endotherms are overlapping but not identical. We therefore discuss the idea that when body temperatures are seasonally very low, cognitive benefits may be thwarted and selection on larger brain size may be rare. Indeed, mammalian hibernators may show similarities to ectotherms.

Alternative reproductive tactics of unflanged and flanged male orangutans revisited.

In many slowly developing mammal species, males reach sexual maturity well before they develop secondary sexual characteristics. Sexually mature male orangutans have exceptionally long periods of developmental arrest. The two male morphs have been associated with behavioral alternative reproductive tactics, but this interpretation is based on cross-sectional analyses predominantly of Northwest Sumatran populations. Here we present the first longitudinal analyses of behavioral changes of 10 adult males that have been observed in both unflanged and flanged morph. We also analyzed long-term behavioral data on an additional 143 individually identified males from two study sites, Suaq (Sumatra, Pongo abelii) and Tuanan (Borneo, Pongo pygmaeus wurmbii), to assess male mating tactics cross-sectionally in relation to population, male morph (unflanged and flanged), and other socio-ecological factors. Both our longitudinal and cross-sectional results confirm and refine previous cross-sectional accounts of the differences in mating tactics between the unflanged and the flanged male morphs. In the unflanged morph, males exhibit higher sociability, particularly with females, and higher rates of both copulation and sexual coercion than in the flanged morph. Based on our results and those of previous studies showing that females prefer flanged males, and that flanged males have higher reproductive success, we conclude that unflanged males face a trade-off between avoiding male-male contest competition and gaining mating access to females, and thus follow a "best-of-a-bad-job" mating strategy.

Putting the cart before the horse? The origin of information donation.

Heintz & Scott-Phillips propose that the partner choice ecology of our ancestors required Gricean cognitive pragmatics for reputation management, which caused a tendency toward showing and expecting prosociality that subsequently scaffolded language evolution. Here, we suggest a cognitively leaner explanation that is more consistent with comparative data and posits that prosociality and eventually language evolved along with cooperative breeding.

Extended parental provisioning and variation in vertebrate brain sizes.

Large brains provide adaptive cognitive benefits but require unusually high, near-constant energy inputs and become fully functional well after their growth is completed. Consequently, young of most larger-brained endotherms should not be able to independently support the growth and development of their own brains. This paradox is solved if the evolution of extended parental provisioning facilitated brain size evolution. Comparative studies indeed show that extended parental provisioning coevolved with brain size and that it may improve immature survival. The major role of extended parental provisioning supports the idea that the ability to sustain the costs of brains limited brain size evolution.

Parental provisioning drives brain size in birds.

Large brains support numerous cognitive adaptations and therefore may appear to be highly beneficial. Nonetheless, the high energetic costs of brain tissue may have prevented the evolution of large brains in many species. This problem may also have a developmental dimension: juveniles, with their immature and therefore poorly performing brains, would face a major energetic hurdle if they were to pay for the construction of their own brain, especially in larger-brained species. Here, we explore the possible role of parental provisioning for the development and evolution of adult brain size in birds. A comparative analysis of 1,176 bird species shows that various measures of parental provisioning (precocial vs. altricial state at hatching, relative egg mass, time spent provisioning the young) strongly predict relative brain size across species. The parental provisioning hypothesis also provides an explanation for the well-documented but so far unexplained pattern that altricial birds have larger brains than precocial ones. We therefore conclude that the evolution of parental provisioning allowed species to overcome the seemingly insurmountable energetic constraint on growing large brains, which in turn enabled bird species to increase survival and population stability. Because including adult eco- and socio-cognitive predictors only marginally improved the explanatory value of our models, these findings also suggest that the traditionally assessed cognitive abilities largely support successful parental provisioning. Our results therefore indicate that the cognitive adaptations underlying successful parental provisioning also provide the behavioral flexibility facilitating reproductive success and survival.

Social tolerance and interactional opportunities as drivers of gestural redoings in orang-utans.

Communicative repair is a fundamental and universal element of interactive language use. It has been suggested that the persistence and elaboration after communicative breakdown in nonhuman primates constitute two evolutionary building blocks of this capacity, but the conditions favouring it are poorly understood. Because zoo-housed individuals of some species are more social and more terrestrial than in the wild, they should be more likely to show gestural redoings (i.e. both repetition and elaboration) after communicative failure in the coordination of their joint activities. Using a large comparative sample of wild and zoo-housed orang-utans of two different species, we could confirm this prediction for elaboration, the more flexible form of redoings. Specifically, results showed that gestural redoings in general were best predicted by the specific social action context (i.e. social play) and interaction dyad (i.e. beyond mother-offspring), although they were least frequent in captive Bornean orang-utans. For gestural elaboration, we found the expected differences between captive and wild research settings in Borneans, but not in Sumatrans (the more socially tolerant species). Moreover, we found that the effectiveness of elaboration in eliciting responses was higher in Sumatrans, especially the captive ones, whereas effectiveness of mere repetition was influenced by neither species nor setting. We conclude that the socio-ecological environment plays a central role in the emergence of communicative repair strategies in great apes. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

The economics of brain size evolution in vertebrates.

Across the animal kingdom, we see remarkable variation in brain size. This variation has even increased over evolutionary time. Traditionally, studies aiming to explain brain size evolution have looked at the fitness benefits of increased brain size in relation to its increased cognitive performance in the social and/or ecological domain. However, brains are among the most energetically expensive tissues in the body and also require an uninterrupted energy supply. If not compensated, these energetic demands inevitably lead to a reduction in energy allocation to other vital functions. In this review, we summarize how an increasing number of studies show that to fully comprehend brain size evolution and the large variation in brain size across lineages, it is important to look at the economics of brains, including the different pathways through which the high energetic costs of brains can be offset. We further show how numerous studies converge on the conclusion that cognitive abilities can only drive brain size evolution in vertebrate lineages where they result in an improved energy balance through favourable ecological preconditions. Cognitive benefits that do not directly improve the organism's energy balance can only be selectively favoured when they produce such large improvements in reproduction or survival that they outweigh the negative energetic effects of the large brain.

The function and evolution of child-directed communication.

Humans communicate with small children in unusual and highly conspicuous ways (child-directed communication (CDC)), which enhance social bonding and facilitate language acquisition. CDC-like inputs are also reported for some vocally learning animals, suggesting similar functions in facilitating communicative competence. However, adult great apes, our closest living relatives, rarely signal to their infants, implicating communication surrounding the infant as the main input for infant great apes and early humans. Given cross-cultural variation in the amount and structure of CDC, we suggest that child-surrounding communication (CSC) provides essential compensatory input when CDC is less prevalent-a paramount topic for future studies.

Individual variation and plasticity in the infant-directed communication of orang-utan mothers.

Between-individual variation in behavioural expression, such as social responsiveness, has been shown to have important eco-evolutionary consequences. However, most comparative research on non-human primate communication has focused on species- or population-level variation, while among- and within-individual variation has been largely ignored or considered as noise. Here, we apply a behavioural reaction norm framework to repeated observations of mother-offspring interactions in wild and zoo-housed orang-utans (Pongo abelii, P. pygmaeus) to tease apart variation on the individual level from population-level and species-level differences. Our results showed that mothers not only differed in the composition of their infant-directed gestural repertoires, but also in communicative tactics, such as gestural redoings (i.e. persistence) and responsiveness to infants' requests. These differences remained after controlling for essential moderators, including species, setting, parity and infant age. Importantly, mothers differed in how they adjusted their behaviour across social contexts, making a strong case for investigating within-individual variation. Our findings highlight that partitioning behavioural variation into its within-individual, between-individual and environmental sources allows us to estimate the extent of plastic responses to the immediate environment in great ape communication.

Four levers of reciprocity across human societies: concepts, analysis and predictions.

This paper surveys five human societal types - mobile foragers, horticulturalists, pre-state agriculturalists, state-based agriculturalists and liberal democracies - from the perspective of three core social problems faced by interacting individuals: coordination problems, social dilemmas and contest problems. We characterise the occurrence of these problems in the different societal types and enquire into the main force keeping societies together given the prevalence of these. To address this, we consider the social problems in light of the theory of repeated games, and delineate the role of intertemporal incentives in sustaining cooperative behaviour through the reciprocity principle. We analyse the population, economic and political structural features of the five societal types, and show that intertemporal incentives have been adapted to the changes in scope and scale of the core social problems as societies have grown in size. In all societies, reciprocity mechanisms appear to solve the social problems by enabling lifetime direct benefits to individuals for cooperation. Our analysis leads us to predict that as societies increase in complexity, they need more of the following four features to enable the scalability and adaptability of the reciprocity principle: nested grouping, decentralised enforcement and local information, centralised enforcement and coercive power, and formal rules.

Problem-solving in groups of common marmosets (Callithrix jacchus): more than the sum of its parts.

Human hypercooperativity and the emergence of division of labor enables us to solve problems not only effectively within a group but also collectively. Collective problem-solving occurs when groups perform better than the additive performance of separate individuals. Currently, it is unknown whether this is unique to humans. To investigate the evolutionary origin of collective problem-solving and potential precursors, we propose a continuum of group effects on problem-solving, from simple to complex ones, eventually culminating in collective problem-solving. We tested captive common marmosets with a series of problem-solving tasks, either alone or in a group. To test whether the performance of a group was more than the sum of its parts, we compared real groups to virtual groups (pooled scores of animals tested alone). Marmosets in real groups were both more likely to solve problems than marmosets within the virtual groups and to do so faster. Although individuals within real groups approached the problem faster, a reduction in neophobia was not sufficient to explain the greater success. Success within real groups arose because animals showed higher perseverance, especially after a fellow group member had found the solution in complex tasks. These results are consistent with the idea that group problem-solving evolved alongside a continuum, with performance improving beyond baseline as societies move from social tolerance to opportunities for diffusion of information to active exchange of information. We suggest that increasing interdependence and the adoption of cooperative breeding pushed our ancestors up this scale.

Relative Brain Size and Cognitive Equivalence in Fishes.

Scientists have long struggled to establish how larger brains translate into higher cognitive performance across species. While absolute brain size often yields high predictive power of performance, its positive correlation with body size warrants some level of correction. It is expected that larger brains are needed to control larger bodies without any changes in cognitive performance. Potentially, the mean value of intraspecific brain-body slopes provides the best available estimate for an interspecific correction factor. For example, in primates, including humans, an increase in body size translates into an increase in brain size without changes in cognitive performance. Here, we provide the first evaluation of this hypothesis for another clade, teleost fishes. First, we obtained a mean intraspecific brain-body regression slope of 0.46 (albeit with a relatively large range of 0.26-0.79) from a dataset of 51 species, with at least 10 wild adult specimens per species. This mean intraspecific slope value (0.46) is similar to that of the encephalisation quotient reported for teleosts (0.5), which can be used to predict mean cognitive performance in fishes. Importantly, such a mean value (0.46) is much higher than in endothermic vertebrate species (≤0.3). Second, we used wild-caught adult cleaner fish Labroides dimidiatus as a case study to test whether variation in individual cognitive performance can be explained by body size. We first obtained the brain-body regression slope for this species from two different datasets, which gave slope values of 0.58 (MRI scan data) and 0.47 (dissection data). Then, we used another dataset involving 69 adult cleaners different from those tested for their brain-body slope. We found that cognitive performance from four different tasks that estimated their learning, numerical, and inhibitory control abilities was not significantly associated with body size. These results suggest that the intraspecific brain-body slope captures cognitive equivalence for this species. That is, individuals that are on the brain-body regression line are cognitively equal. While rather preliminary, our results suggest that fish and mammalian brain organisations are fundamentally different, resulting in different intra- and interspecific slopes of cognitive equivalence.

The development and maintenance of sex differences in dietary breadth and complexity in Bornean orangutans.

ABSTRACT: Orangutans show a pronounced sexual dimorphism, with flanged males (i.e., males with fully grown secondary sexual characteristics) reaching twice the size of adult females. Furthermore, adult orangutans show sex-specific dispersal and activity patterns. This study investigates sex differences in adult foraging behavior and sheds light on how these differences develop in immatures. We analyzed 11 years of feeding data on ten adult female, seven flanged male, and 14 immature Bornean orangutans (Pongo pygmaeus wurmbii) at Tuanan in Central Kalimantan, Indonesia. We found that the diets of the adult females were significantly broader and required more processing steps before ingestion than the diets of flanged males. We also found evidence for a similar difference in overall diet repertoire sizes. For the immatures, we found that whereas females reached 100% of their mothers' diet spectrum size by the age of weaning, males reached only around 80%. From the age of 4 years on (i.e., years before being weaned) females had significantly broader daily diets than males. We found no difference in daily or overall diet processing intensity of immature males and females but found preliminary evidence that immature males included fewer items of their mother's diet in their own diets that were processing-intensive. Overall, our results suggest that by eating a broader variety and more complex to process food items, female orangutans go to greater lengths to achieve a balanced diet than males do. These behavioral differences are not just apparent in adult foraging behavior but also reflected in immature development from an early age on. SIGNIFICANCE STATEMENT: In many species, males and females have different nutritional needs and are thus expected to show sex-specific foraging behavior. Sex differences in several aspects of foraging behavior have been found in various species, but it remains largely unclear when and how those develop during ontogeny, which is especially relevant for long-lived altricial species that learn foraging skills over many years. In our study, we analyzed a cross-sectional and longitudinal data set containing more than 750,000 feeding events of adult and immature Bornean orangutans (Pongo pygmaeus wurmbii). We found that adult females had significantly broader and more complex diets than males. We also found that these differences started to develop during infancy, suggesting that immature orangutans prepare for their sex-specific foraging niches long before those become physiologically relevant while they are still in constant association with their mothers and before being frequently exposed to other role models. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00265-021-03014-3.

Orangutans have larger gestural repertoires in captivity than in the wild-A case of weak innovation?

Whether nonhuman species can change their communicative repertoire in response to socio-ecological environments has critical implications for communicative innovativeness prior to the emergence of human language, with its unparalleled productivity. Here, we use a comparative sample of wild and zoo-housed orangutans of two species (Pongo abelii, Pongo pygmaeus) to assess the effect of the wild-captive contrast on repertoires of gestures and facial expressions. We find that repertoires on both the individual and population levels are larger in captive than in wild settings, regardless of species, age class, or sampling effort. In the more sociable Sumatran species, dominant use of signals toward single outcomes was also higher in captive settings. We thus conclude that orangutans exposed to more sociable and terrestrial conditions evince behavioral plasticity, in that they produce additional innate or innovated signals that are highly functionally specific. These findings suggest a latent capacity for innovativeness in these apes' communicative repertoires.

A Farewell to the Encephalization Quotient: A New Brain Size Measure for Comparative Primate Cognition.

Both absolute and relative brain sizes vary greatly among and within the major vertebrate lineages. Scientists have long debated how larger brains in primates and hominins translate into greater cognitive performance, and in particular how to control for the relationship between the noncognitive functions of the brain and body size. One solution to this problem is to establish the slope of cognitive equivalence, i.e., the line connecting organisms with an identical bauplan but different body sizes. The original approach to estimate this slope through intraspecific regressions was abandoned after it became clear that it generated slopes that were too low by an unknown margin due to estimation error. Here, we revisit this method. We control for the error problem by focusing on highly dimorphic primate species with large sample sizes and fitting a line through the mean values for adult females and males. We obtain the best estimate for the slope of circa 0.27, a value much lower than those constructed using all mammal species and close to the value expected based on the genetic correlation between brain size and body size. We also find that the estimate of cognitive brain size based on cognitive equivalence fits empirical cognitive studies better than the encephalization quotient, which should therefore be avoided in future studies on primates and presumably mammals and birds in general. The use of residuals from the line of cognitive equivalence may change conclusions concerning the cognitive abilities of extant and extinct primate species, including hominins.

Multicomponent and multisensory communicative acts in orang-utans may serve different functions.

From early infancy, human face-to-face communication is multimodal, comprising a plethora of interlinked communicative and sensory modalities. Although there is also growing evidence for this in nonhuman primates, previous research rarely disentangled production from perception of signals. Consequently, the functions of integrating articulators (i.e. production organs involved in multicomponent acts) and sensory channels (i.e. modalities involved in multisensory acts) remain poorly understood. Here, we studied close-range social interactions within and beyond mother-infant pairs of Bornean and Sumatran orang-utans living in wild and captive settings, to examine use of and responses to multicomponent and multisensory communication. From the perspective of production, results showed that multicomponent acts were used more than the respective unicomponent acts when the presumed goal did not match the dominant outcome for a specific communicative act, and were more common among non-mother-infant dyads and Sumatran orang-utans. From the perception perspective, we found that multisensory acts were more effective than the respective unisensory acts, and were used more in wild compared to captive populations. We argue that multisensory acts primarily facilitate effectiveness, whereas multicomponent acts become relevant when interaction outcomes are less predictable. These different functions underscore the importance of distinguishing between production and perception in studies of communication.

Cooperation in large-scale human societies-What, if anything, makes it unique, and how did it evolve?

To resolve the major controversy about why prosocial behaviors persist in large-scale human societies, we propose that two questions need to be answered. First, how do social interactions in small-scale and large-scale societies differ? By reviewing the exchange and collective-action dilemmas in both small-scale and large-scale societies, we show they are not different. Second, are individual decision-making mechanisms driven by self-interest? We extract from the literature three types of individual decision-making mechanism, which differ in their social influence and sensitivity to self-interest, to conclude that humans interacting with non-relatives are largely driven by self-interest. We then ask: what was the key mechanism that allowed prosocial behaviors to continue as societies grew? We show the key role played by new social interaction mechanisms-change in the rules of exchange and collective-action dilemmas-devised by the interacting individuals, which allow for self-interested individuals to remain prosocial as societies grow.