Marmosets mutually compensate for differences in rhythms when coordinating vigilance.

Synchronization is widespread in animals, and studies have often emphasized how this seemingly complex phenomenon can emerge from very simple rules. However, the amount of flexibility and control that animals might have over synchronization properties, such as the strength of coupling, remains underexplored. Here, we studied how pairs of marmoset monkeys coordinated vigilance while feeding. By modeling them as coupled oscillators, we noted that (1) individual marmosets do not show perfect periodicity in vigilance behaviors, (2) nevertheless, marmoset pairs started to take turns being vigilant over time, a case of anti-phase synchrony, (3) marmosets could couple flexibly; the coupling strength varied with every new joint feeding bout, and (4) marmosets could control the coupling strength; dyads showed increased coupling if they began in a more desynchronized state. Such flexibility and control over synchronization require more than simple interaction rules. Minimally, animals must estimate the current degree of asynchrony and adjust their behavior accordingly. Moreover, the fact that each marmoset is inherently non-periodic adds to the cognitive demand. Overall, our study provides a mathematical framework to investigate the cognitive demands involved in coordinating behaviors in animals, regardless of whether individual behaviors are rhythmic or not.

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.

Is there a human fear paradox? A more thorough use of comparative data to test the fearful ape hypothesis.

Grossmann's intriguing proposal can benefit from a more thorough integration of the primate literature, particularly on neophobia. Moreover, it directly leads to strong predictions in callitrichids, the only other cooperatively breeding primates beyond humans, which may indeed be met: Being more likely to signal distress than independently breeding monkeys, and responding to such signals with approach and affiliation.

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.

Individual differences in co-representation in three monkey species (Callithrix jacchus, Sapajus apella and Macaca tonkeana) in the joint Simon task: the role of social factors and inhibitory control.

Behavioral coordination is involved in many forms of primate interactions. Co-representation is the simultaneous mental representation of one's own and the partner's task and actions. It often underlies behavioral coordination and cooperation success. In humans, the dyadic social context can modulate co-representation. Here, we first investigated whether individual differences in co-representation in the joint Simon task in capuchin monkeys and Tonkean macaques can be explained by social factors, namely dyadic grooming and sociality index, rank difference and eigenvector centrality. These factors did not predict variation in co-representation. However, in this specific task, co-representation reduces rather than facilitates joint performance. Automatic co-representation therefore needs to be inhibited or suppressed to maximize cooperation success. We therefore also investigated whether general inhibitory control (detour-reaching) would predict co-representation in the joint Simon task in Tonkean macaques, brown capuchin and marmoset monkeys. Inhibitory control did neither explain individual differences nor species differences, since marmosets were most successful in their joint performance despite scoring lowest on inhibitory control. These results suggest that the animals' ability to resolve conflicts between self and other representation to increase cooperation success in this task is gradually learned due to frequent exposure during shared infant care, rather than determined by strong general inhibitory control. Further, we conclude that the joint Simon task, while useful to detect co-representation non-invasively, is less suitable for identifying the factors explaining individual differences and thus a more fruitful approach to identify these factors is to design tasks in which co-representation favors, rather than hinders cooperation success.

Marmoset prosociality is intentional.

Marmoset monkeys show high levels of proactive prosociality, a trait shared with humans, presumably because both species rely on allomaternal care. However, it is not clear whether the proximate regulation of this convergent trait is also similar, in particular with regard to intentionality, which is a defining characteristic of prosocial behavior in the human literature. The aim of this paper was to investigate whether marmoset monkeys' prosociality fulfils the criteria of intentionality developed in primate communication research. The results show that marmoset prosocial behavior (i) has some degree of flexibility, since individuals can use multiple means to reach their goal and adjust them to specific conditions, (ii) depends on the presence of an audience, i.e. potential recipients (social use), and (iii) is goal-directed, because (a) it continues exactly until the putative goal is reached, and (b) individuals check back and look at/for their partner when their prosocial actions do not achieve the putative goal (i.e. if their actions don't lead to the expected outcome, this elicits distinct reactions in the actor). These results suggest that marmoset prosociality is under some degree of voluntary, intentional control. They are in line with other findings that marmosets perceive each other as intentional agents, and only learn socially from actions that are perceived as intentional. The most parsimonious conclusion is, therefore, that prosocial behavior is fundamentally under voluntary control in marmosets, just as it is in humans, even though our more sophisticated cognitive abilities allow for a far more complex integration of prosociality into a broader variety of contexts and of behavioral goals.

A comparative study of litter size and sex composition in a large dataset of callitrichine monkeys.

In many birds and mammals, the size and sex composition of litters can have important downstream effects for individual offspring. Primates are model organisms for questions of cooperation and conflict, but the factors shaping interactions among same-age siblings have been less-studied in primates because most species bear single young. However, callitrichines (marmosets, tamarins, and lion tamarins) frequently bear litters of two or more, thereby providing the opportunity to ask whether variation in the size and sex composition of litters affects development, survival, and reproduction. To investigate these questions, we compiled a large dataset of nine species of callitrichines (n = 27,080 individuals; Callithrix geoffroyi, Callithrix jacchus, Cebuella pygmaea, Saguinus imperator, Saguinus oedipus, Leontopithecus chrysomelas, Leontopithecus chrysopygus, Leontopithecus rosalia, and Callimico goeldii) from zoo and laboratory populations spanning 80 years (1938-2018). Through this comparative approach, we found several lines of evidence that litter size and sex composition may impact fitness. Singletons have higher survivorship than litter-born peers and they significantly outperform litter-born individuals on two measures of reproductive performance. Further, for some species, individuals born in a mixed-sex litter outperform isosexually-born individuals (i.e., those born in all-male or all-female litters), suggesting that same-sex competition may limit reproductive performance. We also document several interesting demographic trends. All but one species (C. pygmaea) has a male-biased birth sex ratio with higher survivorship from birth to sexual maturity among females (although this was significant in only two species). Isosexual litters occurred at the expected frequency (with one exception: C. pygmaea), unlike other animals, where isosexual litters are typically overrepresented. Taken together, our results indicate a modest negative effect of same-age sibling competition on reproductive output in captive callitrichines. This study also serves to illustrate the value of zoo and laboratory records for biological inquiry.

Corepresentation During Joint Action in Marmoset Monkeys ( Callithrix jacchus).

Behavioral coordination is a fundamental element of human cooperation. It is facilitated when individuals represent not only their own actions but also those of their partner. Identifying whether action corepresentation is unique to humans or also present in other species is therefore necessary to fully understand the evolution of human cooperation. We used the auditory joint Simon task to assess whether action corepresentation occurs in common marmosets, a monkey species that engages extensively in coordinated action during cooperative infant care. We found that marmosets indeed show a joint Simon effect. Furthermore, when coordinating their behavior in the joint task, they were more likely to look at their partner than in a joint control condition. Corepresentation is thus not unique to humans but also present in the cooperatively breeding marmosets. Since marmosets are small-brained monkeys, our results suggest that routine coordination in space and time, rather than complex cognitive abilities, plays a role in the evolution of corepresentation.

Looking for unity in diversity: human cooperative childcare in comparative perspective.

Humans engage in cooperative childcare, which includes some elements not found in other animals, such as the presence of post-reproductive helpers, extensive food sharing among adults and a pervasive sexual division of labour. In animals, cooperative offspring care has typically been studied in two different contexts. The first mainly involves helpers contributing care in cooperatively breeding family groups; the second context is allomaternal care in species usually not categorized as cooperative breeders (e.g. plural and communal breeders, often without male care). Comparative analyses suggest that cooperative breeding and allomaternal care in plural and communal breeders have distinct evolutionary origins, with humans fitting neither pathway entirely. Nevertheless, some critical proximate mechanisms of helping, including hormonal regulators, are likely to be shared across species. Other mechanisms may vary among species, such as social tolerance, proactive prosociality or conditional mother-infant bonding. These are presumably associated with specific details of the care system, such as whether all group members contribute, or whether mothers can potentially raise offspring alone. Thus, cooperative offspring care is seen in different contexts across animal lineages, but may nonetheless share several important psychological characteristics. We end by discussing how work on humans may play a unifying role in studying cooperative offspring care.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

The evolution of general intelligence.

The presence of general intelligence poses a major evolutionary puzzle, which has led to increased interest in its presence in nonhuman animals. The aim of this review is to critically evaluate this question and to explore the implications for current theories about the evolution of cognition. We first review domain-general and domain-specific accounts of human cognition in order to situate attempts to identify general intelligence in nonhuman animals. Recent studies are consistent with the presence of general intelligence in mammals (rodents and primates). However, the interpretation of a psychometric g factor as general intelligence needs to be validated, in particular in primates, and we propose a range of such tests. We then evaluate the implications of general intelligence in nonhuman animals for current theories about its evolution and find support for the cultural intelligence approach, which stresses the critical importance of social inputs during the ontogenetic construction of survival-relevant skills. The presence of general intelligence in nonhumans implies that modular abilities can arise in two ways, primarily through automatic development with fixed content and secondarily through learning and automatization with more variable content. The currently best-supported model, for humans and nonhuman vertebrates alike, thus construes the mind as a mix of skills based on primary and secondary modules. The relative importance of these two components is expected to vary widely among species, and we formulate tests to quantify their strength.

Future directions for studying the evolution of general intelligence.

The goal of our target article was to lay out current evidence relevant to the question of whether general intelligence can be found in nonhuman animals in order to better understand its evolution in humans. The topic is a controversial one, as evident from the broad range of partly incompatible comments it has elicited. The main goal of our response is to translate these issues into testable empirical predictions, which together can provide the basis for a broad research agenda.

Oxytocin is associated with infant-care behavior and motivation in cooperatively breeding marmoset monkeys.

The neurohormone oxytocin (OT) is positively involved in the regulation of parenting and social bonding in mammals, and may thus also be important for the mediation of alloparental care. In cooperatively breeding marmosets, infants are raised in teamwork by parents and adult and sub-adult non-reproductive helpers (usually older siblings). Despite high intrinsic motivation, which may be mediated by hormonal priming, not all individuals are always equally able to contribute to infant-care due to competition among care-takers. Among the various care-taking behaviors, proactive food sharing may reflect motivational levels best, since it can be performed ad libitum by several individuals even if competition among surplus care-takers constrains access to infants. Our aim was to study the link between urinary OT levels and care-taking behaviors in group-living marmosets, while taking affiliation with other adults and infant age into account. Over eight reproductive cycles, 26 individuals were monitored for urinary baseline OT, care-taking behaviors (baby-licking, -grooming, -carrying, and proactive food sharing), and adult-directed affiliation. Mean OT levels were generally highest in female breeders and OT increased significantly in all individuals after birth. During early infancy, high urinary OT levels were associated with increased infant-licking but low levels of adult-affiliation, and during late infancy, with increased proactive food sharing. Our results show that, in marmoset parents and alloparents, OT is positively involved in the regulation of care-taking, thereby reflecting the changing needs during infant development. This particularly included behaviors that are more likely to reflect intrinsic care motivation, suggesting a positive link between OT and motivational regulation of infant-care.

High emotional reactivity toward an experimenter affects participation, but not performance, in cognitive tests with common marmosets (Callithrix jacchus).

When testing primates with cognitive tasks, it is usually not considered that subjects differ markedly in terms of emotional reactivity toward the experimenter, which potentially affects a subject's cognitive performance. We addressed this issue in common marmosets (Callithrix jacchus), a monkey species in which males tend to show stronger emotional reactivity in testing situations, whereas females have been reported to outperform males in cognitive tasks. In a two-phase experiment, we first quantified the emotional reactivity of 14 subjects toward four different experimenters performing a standardized behavioral action sequence and then assessed whether and how it affected the subjects' participation and performance in a subsequent object permanence task. A test session was terminated if a subject refused to make a choice in four consecutive trials. Highly emotionally aroused individuals, particularly males, were less likely to participate in the cognitive task and completed fewer trials. However, whenever they did participate and were attentive to the task, their performance was not affected. Our results suggest that differences in emotional reactivity toward an experimenter have no major impact on cognitive performance if strict criteria are applied on when to abandon a test session and if performance is corrected for attention to the test procedure. Furthermore, they suggest that the reported sex differences in cognitive performance in marmosets may be owing to motivational and attentional factors, rather than a difference in cognitive ability per se.

Short-term memory, attentional control and brain size in primates.

Brain size variability in primates has been attributed to various domain-specific socio-ecological factors. A recently published large-scale study of short-term memory abilities in 41 primate species (ManyPrimates 2022 Anim. Behav. Cogn. 9, 428-516. (doi:10.26451/abc.09.04.06.2022)) did not find any correlations with 11 different proxies of external cognitive demands. Here, we found that the interspecific variation in test performance shows correlated evolution with total brain size, with the relationship becoming tighter as species with small sample sizes were successively removed, whereas it was not predicted by the often-used encephalization quotient. In a subsample, we also found that the sizes of brain regions thought to be involved in short-term memory did not predict performance better than overall brain size. The dependence on brain size suggests that domain-general cognitive processes underlie short-term memory as tested by ManyPrimates. These results support the emerging notion that comparative studies of brain size do not generally identify domain-specific cognitive adaptations but rather reveal varying selections on domain-general cognitive abilities. Finally, because attentional processes beyond short-term memory also affect test performance, we suggest that the delayed response test can be refined.

Human Amygdala Volumetric Patterns Convergently Evolved in Cooperatively Breeding and Domesticated Species.

The amygdala is a hub in brain networks that supports social life and fear processing. Compared with other apes, humans have a relatively larger lateral nucleus of the amygdala, which is consistent with both the self-domestication and the cooperative breeding hypotheses of human evolution. Here, we take a comparative approach to the evolutionary origin of the relatively larger lateral amygdala nucleus in humans. We carry out phylogenetic analysis on a sample of 17 mammalian species for which we acquired single amygdala nuclei volumetric data. Our results indicate that there has been convergent evolution toward larger lateral amygdala nuclei in both domesticated and cooperatively breeding mammals. These results suggest that changes in processing fearful stimuli to reduce fear-induced aggression, which are necessary for domesticated and cooperatively breeding species alike, tap into the same neurobiological proximate mechanism. However, humans show changes not only in processing fearful stimuli but also in proactive prosociality. Since cooperative breeding, but not domestication, is also associated with increased proactive prosociality, a prominent role of the former during human evolution is more parsimonious, whereas self-domestication may have been involved as an additional stepping stone.

Who is calling? Optimizing source identification from marmoset vocalizations with hierarchical machine learning classifiers.

With their highly social nature and complex vocal communication system, marmosets are important models for comparative studies of vocal communication and, eventually, language evolution. However, our knowledge about marmoset vocalizations predominantly originates from playback studies or vocal interactions between dyads, and there is a need to move towards studying group-level communication dynamics. Efficient source identification from marmoset vocalizations is essential for this challenge, and machine learning algorithms (MLAs) can aid it. Here we built a pipeline capable of plentiful feature extraction, meaningful feature selection, and supervised classification of vocalizations of up to 18 marmosets. We optimized the classifier by building a hierarchical MLA that first learned to determine the sex of the source, narrowed down the possible source individuals based on their sex and then determined the source identity. We were able to correctly identify the source individual with high precisions (87.21%-94.42%, depending on call type, and up to 97.79% after the removal of twins from the dataset). We also examine the robustness of identification across varying sample sizes. Our pipeline is a promising tool not only for source identification from marmoset vocalizations but also for analysing vocalizations of other species.

Can we measure brain efficiency? An empirical test with common marmosets (Callithrix jacchus).

Various measures of brain size correlate with cognitive performance; however, the fit is not perfect, which bears the question of whether brains also vary in efficiency. Such variation could be expected if a species faces constraints on brain enlargement, for example due to the impossibility of slowing down life history as a consequence of predator pressure, while simultaneously experiencing selective benefits from enhanced cognitive ability related to particular ecological or social conditions. Arguably, this applies to callitrichid monkeys and would lead to the prediction that their relatively small brains are particularly efficient in comparison to their sister taxa, Cebus. This study investigated whether callitrichids' cognitive performance is better than would be expected given their brain size rather than comparing absolute performance between the taxa. As a measure of cognitive performance, we used the reversal learning paradigm, which is reliably and closely associated with brain size across primate taxa, and assessed performance in this paradigm (transfer index) in 14 common marmosets (Callithrix jacchus) as representatives of the callitrichids. These marmosets were found to show higher performance than would be expected for their brain size, and this relative performance was also higher than the relative performance in capuchin monkeys. We outline how these effects may be due to the cooperative breeding system of the callitrichids, particularly the enhancement of behavioural and cognitive propensities associated with shared care and provisioning.

Primate origins of corepresentation and cooperative flexibility: A comparative study with common marmosets (Callithrix jacchus), brown capuchins (Sapajus apella), and Tonkean macaques (Macaca tonkeana).

Human joint action is generally facilitated by the tendency to represent not only one's own task and behavior but also the partner's. Yet, under some conditions, such as in the joint Simon task, corepresentation can cause interference and hampers, rather than facilitates, joint performance. A competent cooperator should thus also be able to flexibly inhibit corepresentation if that is conducive to cooperation success. To investigate the evolutionary origin of corepresentation, as well as the cooperative flexibility to inhibit it when necessary, we tested brown capuchins and Tonkean macaques in the joint Simon task and compared them with the previously tested marmosets. Corepresentation was present in all 3 species, but its strength and the cooperation success varied substantially. The cooperatively breeding marmosets showed the weakest corepresentation effect and, therefore, highest cooperation success, and they were the only ones to use mutual gaze when coordination with the partner was necessary. Cooperative flexibility was therefore not correlated with brain size but with the prevalence of cooperation in nature. This conclusion was corroborated by species differences in gazing patterns and suggests that the drivers of cooperative flexibility in humans were not solely cognitive. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

The evolutionary drivers of primate scleral coloration.

The drivers of divergent scleral morphologies in primates are currently unclear, though white sclerae are often assumed to underlie human hyper-cooperative behaviours. Humans are unusual in possessing depigmented sclerae whereas many other extant primates, including the closely-related chimpanzee, possess dark scleral pigment. Here, we use phylogenetic generalized least squares (PGLS) analyses with previously generated species-level scores of proactive prosociality, social tolerance (both n = 15 primate species), and conspecific lethal aggression (n = 108 primate species) to provide the first quantitative, comparative test of three existing hypotheses. The 'self-domestication' and 'cooperative eye' explanations predict white sclerae to be associated with cooperative, rather than competitive, environments. The 'gaze camouflage' hypothesis predicts that dark scleral pigment functions as gaze direction camouflage in competitive social environments. Notably, the experimental evidence that non-human primates draw social information from conspecific eye movements is unclear, with the latter two hypotheses having recently been challenged. Here, we show that white sclerae in primates are associated with increased cooperative behaviours whereas dark sclerae are associated with reduced cooperative behaviours and increased conspecific lethal violence. These results are consistent with all three hypotheses of scleral evolution, suggesting that primate scleral morphologies evolve in relation to variation in social environment.