DETERMINANTS OF PRIMATE SOCIAL ORGANIZATION: COMPARATIVE EVIDENCE AND NEW INSIGHTS FROM MALAGASY LEMURS

The aim of this review is to summarize newly available information on lemur social systems, to contrast it with the social organization of other primates and to relate it to existing models of primate social evolution. Because of their evolutionary history, the primates of Madagascar constitute a natural experiment in social evolution. During millions of years of isolation, they converged with other primates only in the most fundamental way in the evolution of solitary, pair-living and group-living species, but deviate in several respects within these basic categories of social organization. Solitary lemurs remain poorly studied, but their social organization appears to be broadly similar to that of other solitary primates, even though the unexpected lack of sexual dimorphism may indicate that similar types of social organization can give rise to different mating systems. The determinants of a solitary lifestyle remain elusive. Pair-living lemurs show striking convergences with other monogamous primates in several behavioural traits, but also deviate in that the majority of species are at least partly nocturnal and do not exhibit direct paternal care of dependent young. Group-living lemurs have not evolved single-male groups, male-bonded and multi-level societies, and polyandrous groups may also be lacking. Female philopatry is common, but female bonds are generally weakly developed and eviction of females from natal groups is not unusual. Group-living lemurs also differ from anthropoids in that their groups have even adult sex ratios, smaller average size and may split up on a seasonal basis. Feeding competition, predation risk and reproductive competition can not fully explain these unusual aspects of lemur social organization. It has therefore been suggested that the social consequences of the risk of infanticide and of recent changes in activity may be ultimately responsible for these idiosyncracies of group-living lemurs, an explanation largely supported by the available evidence. Thus, social factors and fundamental life-history traits, in addition to ecological factors, contribute importantly to variation in social systems among lemurs, and possibly other primates. However, neither the diversity of lemur social systems, nor the evolutionary forces and mechanisms operating in these and other primates are yet fully understood.     

Self-Organization in Primates: Understanding the Rules Underlying Collective Movements

Patterns of collective movements, such as the distribution of leadership and the organization of individuals, may be either homogeneously (no leader, no specific order), or heterogeneously (1 or several leaders, and a highly stable order) distributed. Members of a group need to synchronize their activities and coordinate their movements, despite the fact that they differ in physiological or morphological traits. The degree of difference in these traits may affect their decision-making strategy. We demonstrate how a theoretical model based on a variation of a simple mimetic rule, i.e., an amplification process, can result in each of the various collective movement patterns and decision-making strategies observed in primates and other species. We consider cases in which 1) the needs of different individuals are identical and social relationships are equivalent between group members, 2) the needs of individuals are different and social relationships are equivalent, and 3) the needs of individuals are different and social relationships are different. Finally, 4) we assess how the synergy between 2 mimetism rules, specifically the probability of joining a movement and that of canceling an initiation, allows group members to stay synchronized and cohesive. Our models suggest that similar self-organized processes have been selected as reliable and well-adapted means for optimal collective decisions across species, despite differences in their biological and social characteristics.     

Food competition in a semi-free-ranging Cebus apella group

The competitive regime faced by individuals is fundamental to modelling the evolution of social organization. In this paper, we assess the relative importance of contest and scramble food competition on the social dynamics of a provisioned semi-free-ranging Cebus apella group (n = 18). Individuals competed directly for provisioned and clumped foods. Effects of indirect competition were apparent with individuals foraging in different areas and with increased group dispersion during periods of low food abundance. We suggest that both forms of competition can act simultaneously and to some extent synergistically in their influence on social dynamics; the combination of social and ecological opportunities for competition and how those opportunities are exploited both influence the nature of the relationships within social groups of primates and underlie the evolved social structure.     

Taking sociality seriously: the structure of multi-dimensional social networks as a source of information for individuals

Understanding human cognitive evolution, and that of the other primates, means taking sociality very seriously. For humans, this requires the recognition of the sociocultural and historical means by which human minds and selves are constructed, and how this gives rise to the reflexivity and ability to respond to novelty that characterize our species. For other, non-linguistic, primates we can answer some interesting questions by viewing social life as a feedback process, drawing on cybernetics and systems approaches and using social network neo-theory to test these ideas. Specifically, we show how social networks can be formalized as multi-dimensional objects, and use entropy measures to assess how networks respond to perturbation. We use simulations and natural 'knock-outs' in a free-ranging baboon troop to demonstrate that changes in interactions after social perturbations lead to a more certain social network, in which the outcomes of interactions are easier for members to predict. This new formalization of social networks provides a framework within which to predict network dynamics and evolution, helps us highlight how human and non-human social networks differ and has implications for theories of cognitive evolution.     

From social network (centralized vs. decentralized) to collective decision-making (unshared vs. shared consensus)

Relationships we have with our friends, family, or colleagues influence our personal decisions, as well as decisions we make together with others. As in human beings, despotism and egalitarian societies seem to also exist in animals. While studies have shown that social networks constrain many phenomena from amoebae to primates, we still do not know how consensus emerges from the properties of social networks in many biological systems. We created artificial social networks that represent the continuum from centralized to decentralized organization and used an agent-based model to make predictions about the patterns of consensus and collective movements we observed according to the social network. These theoretical results showed that different social networks and especially contrasted ones--star network vs. equal network--led to totally different patterns. Our model showed that, by moving from a centralized network to a decentralized one, the central individual seemed to lose its leadership in the collective movement's decisions. We, therefore, showed a link between the type of social network and the resulting consensus. By comparing our theoretical data with data on five groups of primates, we confirmed that this relationship between social network and consensus also appears to exist in animal societies.     

Anatomical Network Analysis Shows Decoupling of Modular Lability and Complexity in the Evolution of the Primate Skull

Modularity and complexity go hand in hand in the evolution of the skull of primates. Because analyses of these two parameters often use different approaches, we do not know yet how modularity evolves within, or as a consequence of, an also-evolving complex organization. Here we use a novel network theory-based approach (Anatomical Network Analysis) to assess how the organization of skull bones constrains the co-evolution of modularity and complexity among primates. We used the pattern of bone contacts modeled as networks to identify connectivity modules and quantify morphological complexity. We analyzed whether modularity and complexity evolved coordinately in the skull of primates. Specifically, we tested Herbert Simon’s general theory of near-decomposability, which states that modularity promotes the evolution of complexity. We found that the skulls of extant primates divide into one conserved cranial module and up to three labile facial modules, whose composition varies among primates. Despite changes in modularity, statistical analyses reject a positive feedback between modularity and complexity. Our results suggest a decoupling of complexity and modularity that translates to varying levels of constraint on the morphological evolvability of the primate skull. This study has methodological and conceptual implications for grasping the constraints that underlie the developmental and functional integration of the skull of humans and other primates.     

The functions of societies and the evolution of group living: spider societies as a test case

Many models have been advanced to suggest how different expressions of sociality have evolved and are maintained. However these models ignore the function of groups for the particular species in question. Here we present a new perspective on sociality where the function of the group takes a central role. We argue that sociality may have primarily a reproductive, protective, or foraging function, depending on whether it enhances the reproductive, protective or foraging aspect of the animal's life (sociality may serve a mixture of these functions). Different functions can potentially cause the development of the same social behaviour. By identifying which function influences a particular social behaviour we can determine how that social behaviour will change with changing conditions, and which models are most pertinent. To test our approach we examined spider sociality, which has often been seen as the poor cousin to insect sociality. By using our approach we found that the group characteristics of eusocial insects is largely governed by the reproductive function of their groups, while the group characteristics of social spiders is largely governed by the foraging function of the group. This means that models relevant to insects may not be relevant to spiders. It also explains why eusocial insects have developed a strict caste system while spider societies are more egalitarian. We also used our approach to explain the differences between different types of spider groups. For example, differences in the characteristics of colonial and kleptoparasitic groups can be explained by differences in foraging methods, while differences between colonial and cooperative spiders can be explained by the role of the reproductive function in the formation of cooperative spider groups. Although the interactions within cooperative spider colonies are largely those of a foraging society, demographic traits and colony dynamics are strongly influenced by the reproductive function. We argue that functional explanations help to understand the social structure of spider groups and therefore the evolutionary potential for speciation in social spiders.     

The function and mechanism of vocal accommodation in humans and other primates

The study of non‐human animals, in particular primates, can provide essential insights into language evolution. A critical element of language is vocal production learning, i.e. learning how to produce calls. In contrast to other lineages such as songbirds, vocal production learning of completely new signals is strikingly rare in non‐human primates. An increasing body of research, however, suggests that various species of non‐human primates engage in vocal accommodation and adjust the structure of their calls in response to environmental noise or conspecific vocalizations. To date it is unclear what role vocal accommodation may have played in language evolution, in particular because it summarizes a variety of heterogeneous phenomena which are potentially achieved by different mechanisms. In contrast to non‐human primates, accommodation research in humans has a long tradition in psychology and linguistics. Based on theoretical models from these research traditions, we provide a new framework which allows comparing instances of accommodation across species, and studying them according to their underlying mechanism and ultimate biological function. We found that at the mechanistic level, many cases of accommodation can be explained with an automatic perception–production link, but some instances arguably require higher levels of vocal control. Functionally, both human and non‐human primates use social accommodation to signal social closeness or social distance to a partner or social group. Together, this indicates that not only some vocal control, but also the communicative function of vocal accommodation to signal social closeness and distance must have evolved prior to the emergence of language, rather than being the result of it. Vocal accommodation as found in other primates has thus endowed our ancestors with pre‐adaptations that may have paved the way for language evolution.     

The concurrent evolution of cooperation and the population structures that support it

The evolution of cooperation often depends upon population structure, yet nearly all models of cooperation implicitly assume that this structure remains static. This is a simplifying assumption, because most organisms possess genetic traits that affect their population structure to some degree. These traits, such as a group size preference, affect the relatedness of interacting individuals and hence the opportunity for kin or group selection. We argue that models that do not explicitly consider their evolution cannot provide a satisfactory account of the origin of cooperation, because they cannot explain how the prerequisite population structures arise. Here, we consider the concurrent evolution of genetic traits that affect population structure, with those that affect social behavior. We show that not only does population structure drive social evolution, as in previous models, but that the opportunity for cooperation can in turn drive the creation of population structures that support it. This occurs through the generation of linkage disequilibrium between socio-behavioral and population-structuring traits, such that direct kin selection on social behavior creates indirect selection pressure on population structure. We illustrate our argument with a model of the concurrent evolution of group size preference and social behavior.     

Predation risk sensitivity and the spatial organization of primate groups: A case study using GIS in lowland Woolly Monkeys (Lagothrix lagotricha poeppigii)

Predation risk is thought to be a potent force influencing intragroup cohesion, and the level of risk experienced by an individual is expected to vary with both group size and spatial position within a group. Smaller‐bodied and less‐experienced individuals are presumed to be more vulnerable to predators, suggesting that within‐group spatial organization should show size‐ and age‐dependent patterns in predator sensitive positioning. However, such effects have been difficult to evaluate for arboreal primates living in large groups. We conducted a preliminary study using a novel, spatially explicit method of assessing group spatial organization using GIS data in two groups of wild lowland Woolly monkeys, in which one group had a membership roughly twice as large as the second. In the larger group, group spread was more diffuse and large adult males were more frequently on the outskirts of the group than other age/sex classes, while immatures and females with dependents were more often in the center. Leaf cover around an individual—presumed to index an animal's perception of risk—increased significantly with distance from the group center for all immatures, although they were typically under lower leaf cover than adults; the number of groupmates in proximity also had an effect, but nearest neighbor distance did not. These differences were not detectable in the smaller group. This preliminary study suggests that thorough studies of spatial organization and predation risk sensitivity in arboreal primates are possible and could yield valuable information on how gregarious individuals offset ecological risks through social spacing. Am J Phys Anthropol 156:158–165, 2015 © 2014 Wiley Periodicals, Inc.     

Evolution of human growth

The human pattern of growth and development (ontogeny) appears to differ markedly from patterns of ontogeny in other primate species. Humans present complex and sinuous growth curves for both body mass and stature. Many human proportions change dramatically during ontogeny, as we reach sizes that are among the largest of living primates. Perhaps most obviously, humans grow for a long time, with the interval between birth and maturation exceeding that of all other primate species. These ontogenetic traits are as distinctive as other key derived human traits, such as a large brain and language. Ontogenetic adaptations are also linked to human social organization, particularly by necessitating high levels of parental investment during the first several years of life.     

Social traits,social networks and evolutionary biology

The social environment is both an important agent of selection for most organisms, and an emergent property of their interactions. As an aggregation of interactions among members of a population, the social environment is a product of many sets of relationships and so can be represented as a network or matrix. Social network analysis in animals has focused on why these networks possess the structure they do, and whether individuals’ network traits, representing some aspect of their social phenotype, relate to their fitness. Meanwhile, quantitative geneticists have demonstrated that traits expressed in a social context can depend on the phenotypes and genotypes of interacting partners, leading to influences of the social environment on the traits and fitness of individuals and the evolutionary trajectories of populations. Therefore, both fields are investigating similar topics, yet have arrived at these points relatively independently. We review how these approaches are diverged, and yet how they retain clear parallelism and so strong potential for complementarity. This demonstrates that, despite separate bodies of theory, advances in one might inform the other. Techniques in network analysis for quantifying social phenotypes, and for identifying community structure, should be useful for those studying the relationship between individual behaviour and group‐level phenotypes. Entering social association matrices into quantitative genetic models may also reduce bias in heritability estimates, and allow the estimation of the influence of social connectedness on trait expression. Current methods for measuring natural selection in a social context explicitly account for the fact that a trait is not necessarily the property of a single individual, something the network approaches have not yet considered when relating network metrics to individual fitness. Harnessing evolutionary models that consider traits affected by genes in other individuals (i.e. indirect genetic effects) provides the potential to understand how entire networks of social interactions in populations influence phenotypes and predict how these traits may evolve. By theoretical integration of social network analysis and quantitative genetics, we hope to identify areas of compatibility and incompatibility and to direct research efforts towards the most promising areas. Continuing this synthesis could provide important insights into the evolution of traits expressed in a social context and the evolutionary consequences of complex and nuanced social phenotypes.     

Systems approach to studying animal sociality: individual position versus group organization in dynamic social network models

Social networks can be used to represent group structure as a network of interacting components, and also to quantify both the position of each individual and the global properties of a group. In a series of simulation experiments based on dynamic social networks, we test the prediction that social behaviors that help individuals reach prominence within their social group may conflict with their potential to benefit from their social environment. In addition to cases where individuals were able to benefit from improving both their personal relative importance and group organization, using only simple rules of social affiliation we were able to obtain results in which individuals would face a trade-off between these factors. While selection would favor (or work against) social behaviors that concordantly increase (or decrease, respectively) fitness at both individual and group level, when these factors conflict with each other the eventual selective pressure would depend on the relative returns individuals get from their social environment and their position within it. The presented results highlight the importance of a systems approach to studying animal sociality, in which the effects of social behaviors should be viewed not only through the benefits that those provide to individuals, but also in terms of how they affect broader social environment and how in turn this is reflected back on an individual's fitness.     

Within-group social bonds in white-faced saki monkeys (Pithecia pithecia) display male-female pair preference

White‐faced saki monkeys (Pithecia pithecia) lack most of the behavioral and physical traits typical of primate monogamy [Fuentes, 1999 ]. In order to determine if social bonds in this species reflect patterns displayed by pair‐bonded groups or larger multimale–multifemale groups, we draw on 17 months of data collected on wild white‐faced sakis at Brownsberg Nature Park, Suriname. We analyzed within‐group social bonds for three habituated groups (one two‐adult and two multiadult groups) by measuring grooming, proximity, and approach/leave patterns between adult and subadult group members. We found that both two‐adult and multiadult groups showed significantly stronger social bonds between a single male–female dyad within each group (deemed “primary dyads”). In all three groups, primary dyads were composed of the oldest adult male and a breeding female. These pairs had significantly higher levels of grooming than other within‐group dyads and were also in close proximity (<1 m) more often than nonprimary dyads. Grooming in primary dyads was nonreciprocal, and consistently biased toward female investment. Grooming patterns in nonprimary dyads varied, but were often more reciprocal. Grooming and proximity of the primary dyad also changed in relation to infant development. Our results suggest that while white‐faced sakis do not show behavioral and physical traits typical of monogamy or pair‐bonding, social bonds are strongest between a single male–female pair. Pitheciine social systems range from small group monogamy in Callicebus to large multimale–multifemale groups in Chiropotes and Cacajao. As the middle taxon in this platyrrhine radiation, behavioral strategies of white‐faced sakis provide a model for how social bonds and affiliation could be influenced by and affect the evolution of larger group size in primates. Am. J. Primatol. 73:1051–1061, 2011. © 2011 Wiley‐Liss, Inc.     

A genetic linkage map of the vervet monkey (Chlorocebus aethiops sabaeus)

The spectacular progress in genomics increasingly highlights the importance of comparative biology in biomedical research. In particular, nonhuman primates, as model systems, provide a crucial intermediate between humans and mice. The close similarities between humans and other primates are stimulating primate studies in virtually every area of biomedical research, including development, anatomy, physiology, immunology, and behavior. The vervet monkey (Chlorocebus aethiops sabaeus) is an important model for studying human diseases and complex traits, especially behavior. We have developed a vervet genetic linkage map to enable mapping complex traits in this model organism and facilitate comparative genomic analysis between vervet and other primates. Here we report construction of an initial genetic map built with about 360 human orthologous short tandem repeats (STRs) that were genotyped in 434 members of an extended vervet pedigree. The map includes 226 markers mapped in a unique order with a resolution of 9.8 Kosambi centimorgans (cM) in the vervet monkey genome, and with a total length (including all 360 markers) of 2726 cM. At least one complex and 11 simple rearrangements in marker order distinguish vervet chromosomes from human homologs. While inversions and insertions can explain a similar number of changes in marker order between vervet and rhesus homologs, mostly inversions are observed when vervet chromosome organization is compared to that in human and chimpanzee. Our results support the notion that large inversions played a less prominent role in the evolution within the group of the Old World monkeys compared to the human and chimpanzee lineages. Electronic supplementary material The online version of this article (doi: ) contains supplementary material, which is available to authorized users.     

Human‐aided admixture may fuel ecosystem transformation during biological invasions: theoretical and experimental evidence

Biological invasions can transform our understanding of how the interplay of historical isolation and contemporary (human‐aided) dispersal affects the structure of intraspecific diversity in functional traits, and in turn, how changes in functional traits affect other scales of biological organization such as communities and ecosystems. Because biological invasions frequently involve the admixture of previously isolated lineages as a result of human‐aided dispersal, studies of invasive populations can reveal how admixture results in novel genotypes and shifts in functional trait variation within populations. Further, because invasive species can be ecosystem engineers within invaded ecosystems, admixture‐induced shifts in the functional traits of invaders can affect the composition of native biodiversity and alter the flow of resources through the system. Thus, invasions represent promising yet under‐investigated examples of how the effects of short‐term evolutionary changes can cascade across biological scales of diversity. Here, we propose a conceptual framework that admixture between divergent source populations during biological invasions can reorganize the genetic variation underlying key functional traits, leading to shifts in the mean and variance of functional traits within invasive populations. Changes in the mean or variance of key traits can initiate new ecological feedback mechanisms that result in a critical transition from a native ecosystem to a novel invasive ecosystem. We illustrate the application of this framework with reference to a well‐studied plant model system in invasion biology and show how a combination of quantitative genetic experiments, functional trait studies, whole ecosystem field studies and modeling can be used to explore the dynamics predicted to trigger these critical transitions.     

Economic behaviours among non-human primates

Do we have any valid reasons to affirm that non-human primates display economic behaviour in a sufficiently rich and precise sense of the phrase? To address this question, we have to develop a set of criteria to assess the vast array of experimental studies and field observations on individual cognitive and behavioural competences as well as the collective organization of non-human primates. We review a sample of these studies and assess how they answer to the following four main challenges. (i) Do we see any economic organization or institutions emerge among groups of non-human primates? (ii) Are the cognitive abilities, and often biases, that have been evidenced as underlying typical economic decision-making among humans, also present among non-human primates? (iii) Can we draw positive lessons from performance comparisons among primate species, humans and non-humans but also across non-human primate species, as elicited by canonical game-theoretical experimental paradigms, especially as far as economic cooperation and coordination are concerned? And (iv) in which way should we improve models and paradigms to obtain more ecological data and conclusions? Articles discussed in this paper most often bring about positive answers and promising perspectives to support the existence and prevalence of economic behaviours among non-human primates.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Primate group size and interpreting socioecological models: Do folivores really play by different rules?

Because primates display such remarkable diversity, they are an ideal taxon within which to examine the evolutionary significance of group living and the ecological factors responsible for variation in social organization. However, as with any social vertebrate, the ecological determinants of primate social variability are not easily identified. Interspecific variation in group size and social organization results from the compromises required to accommodate the associative and dissociative forces of many factors, including predation, 1 - 3 conspecific harassment and infanticide, 4 - 6 foraging competition 1 , 7 and cooperation, 8 dominance interactions, 9 reproductive strategies, and socialization. 10 - 12 Causative explanations have emerged primarily through the construction of theoretical models that organize the observed variation in primate social organization and group size relative to measurable ecological variation.     

Plain faces are more expressive: comparative study of facial colour,mobility and musculature in primates

Facial colour patterns and facial expressions are among the most important phenotypic traits that primates use during social interactions. While colour patterns provide information about the sender''s identity, expressions can communicate its behavioural intentions. Extrinsic factors, including social group size, have shaped the evolution of facial coloration and mobility, but intrinsic relationships and trade-offs likely operate in their evolution as well. We hypothesize that complex facial colour patterning could reduce how salient facial expressions appear to a receiver, and thus species with highly expressive faces would have evolved uniformly coloured faces. We test this hypothesis through a phylogenetic comparative study, and explore the underlying morphological factors of facial mobility. Supporting our hypothesis, we find that species with highly expressive faces have plain facial colour patterns. The number of facial muscles does not predict facial mobility; instead, species that are larger and have a larger facial nucleus have more expressive faces. This highlights a potential trade-off between facial mobility and colour patterning in primates and reveals complex relationships between facial features during primate evolution.     

The social nature of primate cognition

The hypothesis that the enlarged brain size of the primates was selected for by social, rather than purely ecological, factors has been strongly influential in studies of primate cognition and behaviour over the past two decades. However, the Machiavellian intelligence hypothesis, also known as the social brain hypothesis, tends to emphasize certain traits and behaviours, like exploitation and deception, at the expense of others, such as tolerance and behavioural coordination, and therefore presents only one view of how social life may shape cognition. This review outlines work from other relevant disciplines, including evolutionary economics, cognitive science and neurophysiology, to illustrate how these can be used to build a more general theoretical framework, incorporating notions of embodied and distributed cognition, in which to situate questions concerning the evolution of primate social cognition.