Policing and punishment across the domains of social evolution

Several decades of research in humans, other vertebrates, and social insects have offered fascinating insights into the dynamics of punishment (and its subset, policing), but authors have only rarely addressed whether there are fundamental joint principles underlying the maintenance of these behaviors. Here we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punishing roles in animal societies. We apply our scheme to societies of eusocial Hymenoptera and nonhuman vertebrate social breeders, and we outline potential extensions for understanding conflict regulation among cells in metazoan bodies and unrelated individuals in human societies. We highlight that: 1) no social unit is expected to express punishment behavior unless it collects positive inclusive fitness benefits that surpass alternative benefits of bystanding; 2) punishment with public good benefits can be maintained through either direct fitness benefits (coercion) or indirect fitness benefits (correction) or both; 3) differences across social systems in the distributions of power, relatedness, and reproductive options drive variation in the extent to which individuals actively punish; and 4) inclusive fitness logic captures many punishment‐relevant evolutionary and ecological variables in a single framework that appears to apply across very different types of social arrangements. Synthesis Researchers have long observed that individuals in animal societies punish (and by extension, police) each other, but they have rarely investigated whether general principles underlie this behavior across social arrangements. In this paper, we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punisher roles in animal societies. We apply the approach to eusocial insects and cooperatively breeding vertebrates and outline extensions towards the control of cancer cell lineages and punishment in human groups. We highlight how variation in specific social variables may drive differences in punishing/policing across the social domains.     

Evo-devo and the evolution of social behavior

The integration of evolutionary biology with developmental genetics into the hybrid field of 'evo-devo' resulted in major advances in understanding multicellular development and morphological evolution. Here we show how insights from evo-devo can be applied to study the evolution of social behavior. We develop this idea by reviewing studies that suggest that molecular pathways controlling feeding behavior and reproduction in solitary insects are part of a 'genetic toolkit' underlying the evolution of a particularly complex form of social behavior, division of labor among workers in honeybee colonies. The evo-devo approach, coupled with advances in genomics for non-model genetic organisms, including the recent sequencing of the honeybee genome, promises to advance our understanding of the evolution of social behavior.     

Kinship shapes affiliative social networks but not aggression in ring-tailed coatis

Animal groups typically contain individuals with varying degrees of genetic relatedness, and this variation in kinship has a major influence on patterns of aggression and affiliative behaviors. This link between kinship and social behavior underlies socioecological models which have been developed to explain how and why different types of animal societies evolve. We tested if kinship and age-sex class homophily in two groups of ring-tailed coatis (Nasua nasua) predicted the network structure of three different social behaviors: 1) association, 2) grooming, and 3) aggression. Each group was studied during two consecutive years, resulting in four group-years available for analysis (total of 65 individuals). Association patterns were heavily influenced by agonistic interactions which typically occurred during feeding competition. Grooming networks were shaped by mother-offspring bonds, female-female social relationships, and a strong social attraction to adult males. Mother-offspring pairs were more likely to associate and groom each other, but relatedness had no effect on patterns of aggressive behavior. Additionally, kinship had little to no effect on coalitionary support during agonistic interactions. Adult females commonly came to the aid of juveniles during fights with other group members, but females often supported juveniles who were not their offspring (57% of coalitionary interactions). These patterns did not conform to predictions from socioecological models.     

Social insects and social amoebae

The evolution of social groupings in insects, especially wasps, is compared to that of social amoebae (cellular slime moulds). They both show a gamut of colony sizes, from solitary forms to complex colonies with a division of labour. The various ideas as to how there might have been an evolution of complexity within insect societies, such as the role of genetic relatedness, the role of mutualism, the origin of sterility, the manipulation and exploitation of some individuals by others within a colony, are discussed, and then applied to social amoebae. The result is both interesting and instructive: despite some differences, there are many striking parallels, which suggests that there are some common denominators in the formation and evolution of a social existence among organisms.     

Developmental evolution in social insects: regulatory networks from genes to societies

The evolution and development of complex phenotypes in social insect colonies, such as queen-worker dimorphism or division of labor, can, in our opinion, only be fully understood within an expanded mechanistic framework of Developmental Evolution. Conversely, social insects offer a fertile research area in which fundamental questions of Developmental Evolution can be addressed empirically. We review the concept of gene regulatory networks (GRNs) that aims to fully describe the battery of interacting genomic modules that are differentially expressed during the development of individual organisms. We discuss how distinct types of network models have been used to study different levels of biological organization in social insects, from GRNs to social networks. We propose that these hierarchical networks spanning different organizational levels from genes to societies should be integrated and incorporated into full GRN models to elucidate the evolutionary and developmental mechanisms underlying social insect phenotypes. Finally, we discuss prospects and approaches to achieve such an integration.     

Kin recognition in social bees

Kin recognition in social insects has become a central issue in sociobiology because studies of the recognition abilities of social insects provide a test of kin selection theory. W.D. Hamilton(1) formalized kin selection theory by showing how individuals can gain fitness by increasing the reproductive output of relatives (kin). The social interactions of individuals, or groups, should be influenced by the genetic structure of the population. The ability to recognize kin can increase the adaptive value of social behavior by modulating it according to genetic relationship. From this, the specific prediction emerges: if individuals can distinguish among others with which they interact on the basis of the degree to which they are related, then behavior should be biased preferentially toward more closely related reproductive individuals.     

A framework for conceptualizing dimensions of social organization in mammals

Mammalian societies represent many different types of social systems. While some aspects of social systems have been extensively studied, there is little consensus on how to conceptualize social organization across species. Here, we present a framework describing eight dimensions of social organization to capture its diversity across mammalian societies. The framework uses simple information that is clearly separated from the three other aspects of social systems: social structure, care system, and mating system. By applying our framework across 208 species of all mammalian taxa, we find a rich multidimensional landscape of social organization. Correlation analysis reveals that the dimensions have relatively high independence, suggesting that social systems are able to evolve different aspects of social behavior without being tied to particular traits. Applying a clustering algorithm allows us to identify the relative importance of key dimensions on patterns of social organization. Finally, mapping mating system onto these clusters shows that social organization represents a distinct aspect of social systems. In the future, this framework will aid reporting on important aspects of natural history in species and facilitate comparative analyses, which ultimately will provide the ability to generate new insights into the primary drivers of social patterns and evolution of sociality.     

A simple mechanism for complex social behavior

The evolution of cooperation is a paradox because natural selection should favor exploitative individuals that avoid paying their fair share of any costs. Such conflict between the self-interests of cooperating individuals often results in the evolution of complex, opponent-specific, social strategies and counterstrategies. However, the genetic and biological mechanisms underlying complex social strategies, and therefore the evolution of cooperative behavior, are largely unknown. To address this dearth of empirical data, we combine mathematical modeling, molecular genetic, and developmental approaches to test whether variation in the production of and response to social signals is sufficient to generate the complex partner-specific social success seen in the social amoeba Dictyostelium discoideum. Firstly, we find that the simple model of production of and response to social signals can generate the sort of apparent complex changes in social behavior seen in this system, without the need for partner recognition. Secondly, measurements of signal production and response in a mutant with a change in a single gene that leads to a shift in social behavior provide support for this model. Finally, these simple measurements of social signaling can also explain complex patterns of variation in social behavior generated by the natural genetic diversity found in isolates collected from the wild. Our studies therefore demonstrate a novel and elegantly simple underlying mechanistic basis for natural variation in complex social strategies in D. discoideum. More generally, they suggest that simple rules governing interactions between individuals can be sufficient to generate a diverse array of outcomes that appear complex and unpredictable when those rules are unknown.     

The co‐evolution of social institutions,demography, and large‐scale human cooperation

Human cooperation is typically coordinated by institutions, which determine the outcome structure of the social interactions individuals engage in. Explaining the Neolithic transition from small‐ to large‐scale societies involves understanding how these institutions co‐evolve with demography. We study this using a demographically explicit model of institution formation in a patch‐structured population. Each patch supports both social and asocial niches. Social individuals create an institution, at a cost to themselves, by negotiating how much of the costly public good provided by cooperators is invested into sanctioning defectors. The remainder of their public good is invested in technology that increases carrying capacity, such as irrigation systems. We show that social individuals can invade a population of asocials, and form institutions that support high levels of cooperation. We then demonstrate conditions where the co‐evolution of cooperation, institutions, and demographic carrying capacity creates a transition from small‐ to large‐scale social groups.     

Learned social preference in zebrafish

How social aggregations arise and persist is central to our understanding of evolution, behavior, and psychology. When social groups arise within a species, evolutionary divergence and speciation can result. To understand this diversifying role of social behavior, we must examine the internal and external influences that lead to nonrandom assortment of phenotypes. Many fishes form aggregations called shoals that reduce predation risk while enhancing foraging and reproductive success. Thus, shoaling is adaptive, and signals that maintain shoals are likely to evolve under selection. Given the diversity of pigment patterns among Danio fishes, visual signals might be especially important in mediating social behaviors in this group. Our understanding of pigment pattern development in the zebrafish D. rerio allows integrative analyses of how molecular variation leads to morphological variation among individuals and how morphological variation influences social interactions. Here, we use the zebrafish pigment mutant nacre/mitfa to test roles for genetic and environmental determinants in the development of shoaling preference. We demonstrate that individuals discriminate between shoals having different pigment pattern phenotypes and that early experience determines shoaling preference. These results suggest a role for social learning in pigment pattern diversification in danios.     

Violating social norms when choosing friends: how rule-breakers affect social networks

Social networks rely on basic rules of conduct to yield functioning societies in both human and animal populations. As individuals follow established rules, their behavioral decisions shape the social network and give it structure. Using dynamic, self-organizing social network models we demonstrate that defying conventions in a social system can affect multiple levels of social and organizational success independently. Such actions primarily affect actors' own positions within the network, but individuals can also affect the overall structure of a network even without immediately affecting themselves or others. These results indicate that defying the established social norms can help individuals to change the properties of a social system via seemingly neutral behaviors, highlighting the power of rule-breaking behavior to transform convention-based societies, even before direct impacts on individuals can be measured.     

Insect societies and the molecular biology of social behavior

This article outlines the rationale for a molecular genetic study of social behavior, and explains why social insects are good models. Summaries of research on brain and behavior in two species, honey bees and fire ants, are presented to illustrate the richness of the behavioral phenomena that can be addressed with social insects and to show how they are beginning to be used to study genes that influence social behavior. We conclude by considering the problems and potential of this emerging field.     

Evaluating the role of reproductive constraints in ant social evolution

The reproductive division of labour is a key feature of eusociality in ants, where queen and worker castes show dramatic differences in the development of their reproductive organs. To understand the developmental and genetic basis underlying this division of labour, we performed a molecular analysis of ovary function and germ cell development in queens and workers. We show that the processes of ovarian development in queens have been highly conserved relative to the fruitfly Drosophila melanogaster. We also identify specific steps during oogenesis and embryogenesis in which ovarian and germ cell development have been evolutionarily modified in the workers. These modifications, which we call ‘reproductive constraints’, are often assumed to represent neutral degenerations that are a consequence of social evolutionary forces. Based on our developmental and functional analysis of these constraints, however, we propose and discuss the alternative hypothesis that reproductive constraints represent adaptive proximate mechanisms or traits for maintaining social harmony in ants. We apply a multi-level selection framework to help understand the role of these constraints in ant social evolution. A complete understanding of how cooperation, conflict and developmental systems evolve in social groups requires a ‘socio-evo-devo’ approach that integrates social evolutionary and developmental biology.     

社会性昆虫级型和行为分化机制研究进展

社会性的出现是生物演化过程中的重要革新, 理解社会性的演化和调控机制具有重要的理论和实际意义。社会性昆虫的个体间有着明显的级型分化和劳动分工, 这有利于它们适应复杂的环境变化。理解社会性昆虫如何产生不同的形态、行为和生活史特性, 一直是进化和发育生物学的重要目标。随着测序技术的不断更新及生物信息学的快速发展, 已经有众多关于社会性昆虫级型和行为分化机制的研究报道。本文通过整理社会性昆虫研究的已有成果, 从环境因素、生理调控和分子机制等方面对社会性昆虫级型和行为分化机制相关研究进展进行了综述, 并对未来的研究方向做出了展望。根据现有证据, 社会性昆虫所生活的生物环境(食物营养、信息素、表皮碳氢化合物)和非生物环境(温度、气候等)均能直接或间接影响社会性昆虫级型和行为的分化; 保幼激素、蜕皮激素、类胰岛素及生物胺等内分泌激素和神经激素对社会性昆虫的级型和行为分化也有重要的调控作用; 此外, 遗传因素、新基因等DNA序列或基因组结构上的变化以及表观遗传修饰、基因的差异表达等基因调控机制均能不同程度地影响社会性昆虫的行为分化。本文建议加强昆虫纲其他社会性类群如半翅目蚜虫和缨翅目蓟马等的社会性行为及其演化机制的研究, 以加深对社会性昆虫起源及其行为演化的理解和认识。     

The combined role of the main olfactory and vomeronasal systems in social communication in mammals

The main olfactory and the vomeronasal systems are the two systems by which most vertebrates detect chemosensory cues that mediate social behavior. Much research has focused on how one system or the other is critical for particular behaviors. This has lead to a vision of two distinct and complexly autonomous olfactory systems. A closer look at research over the past 30 years reveals a different picture however. These two seemingly distinct systems are much more integrated than previously thought. One novel set of chemosensory cues in particular (MHC Class I peptide ligands) can show us how both systems are capable of detecting the same chemosensory cues, through different mechanisms yet provide the same general information (genetic individuality). Future research will need to now focus on how two seemingly distinct chemosensory systems together detect pheromones and mediate social behaviors. Do these systems work independently, synergistically or competitively in communicating between individuals of the same species?     

The complex structure of hunter-gatherer social networks

In nature, many different types of complex system form hierarchical, self-similar or fractal-like structures that have evolved to maximize internal efficiency. In this paper, we ask whether hunter-gatherer societies show similar structural properties. We use fractal network theory to analyse the statistical structure of 1189 social groups in 339 hunter-gatherer societies from a published compilation of ethnographies. We show that population structure is indeed self-similar or fractal-like with the number of individuals or groups belonging to each successively higher level of organization exhibiting a constant ratio close to 4. Further, despite the wide ecological, cultural and historical diversity of hunter-gatherer societies, this remarkable self-similarity holds both within and across cultures and continents. We show that the branching ratio is related to density-dependent reproduction in complex environments and hypothesize that the general pattern of hierarchical organization reflects the self-similar properties of the networks and the underlying cohesive and disruptive forces that govern the flow of material resources, genes and non-genetic information within and between social groups. Our results offer insight into the energetics of human sociality and suggest that human social networks self-organize in response to similar optimization principles found behind the formation of many complex systems in nature.     

The evolution of social interactions changes predictions about interacting phenotypes

In many traits involved in social interactions, such as courtship and aggression, the phenotype is an outcome of interactions between individuals. Such traits whose expression in an individual is partly determined by the phenotype of its social partner are called "interacting phenotypes." Quantitative genetic models suggested that interacting phenotypes can evolve much faster than nonsocial traits. Current models, however, consider the interaction between phenotypes of social partners as a fixed phenotypic response rule, represented by an interaction coefficient (ψ). Here, we extend existing theoretical models and incorporate the interaction coefficient as a trait that can evolve. We find that the evolution of the interaction coefficient can change qualitatively the predictions about the rate and direction of evolution of interacting phenotypes. We argue that it is crucial to determine whether and how the phenotypic response of an individual to its social partner can evolve to make accurate predictions about the evolution of traits involved in social interactions.     

Effects of social disruption in elephants persist decades after culling

Background

Multi-level fission-fusion societies, characteristic of a number of large brained mammal species including some primates, cetaceans and elephants, are among the most complex and cognitively demanding animal social systems. Many free-ranging populations of these highly social mammals already face severe human disturbance, which is set to accelerate with projected anthropogenic environmental change. Despite this, our understanding of how such disruption affects core aspects of social functioning is still very limited.

Results

We now use novel playback experiments to assess decision-making abilities integral to operating successfully within complex societies, and provide the first systematic evidence that fundamental social skills may be significantly impaired by anthropogenic disruption. African elephants (Loxodonta africana) that had experienced separation from family members and translocation during culling operations decades previously performed poorly on systematic tests of their social knowledge, failing to distinguish between callers on the basis of social familiarity. Moreover, elephants from the disrupted population showed no evidence of discriminating between callers when age-related cues simulated individuals on an increasing scale of social dominance, in sharp contrast to the undisturbed population where this core social ability was well developed.

Conclusions

Key decision-making abilities that are fundamental to living in complex societies could be significantly altered in the long-term through exposure to severely disruptive events (e.g. culling and translocation). There is an assumption that wildlife responds to increasing pressure from human societies only in terms of demography, however our study demonstrates that the effects may be considerably more pervasive. These findings highlight the potential long-term negative consequences of acute social disruption in cognitively advanced species that live in close-knit kin-based societies, and alter our perspective on the health and functioning of populations that have been subjected to anthropogenic disturbance.

     

Detecting instability in animal social networks: genetic fragmentation is associated with social instability in rhesus macaques

The persistence of biological systems requires evolved mechanisms which promote stability. Cohesive primate social groups are one example of stable biological systems, which persist in spite of regular conflict. We suggest that genetic relatedness and its associated kinship structure are a potential source of stability in primate social groups as kinship structure is an important organizing principle in many animal societies. We investigated the effect of average genetic relatedness per matrilineal family on the stability of matrilineal grooming and agonistic interactions in 48 matrilines from seven captive groups of rhesus macaques. Matrilines with low average genetic relatedness show increased family-level instability such as: more sub-grouping in their matrilineal groom network, more frequent fighting with kin, and higher rates of wounding. Family-level instability in multiple matrilines within a group is further associated with group-level instability such as increased wounding. Stability appears to arise from the presence of clear matrilineal structure in the rhesus macaque group hierarchy, which is derived from cohesion among kin in their affiliative and agonistic interactions with each other. We conclude that genetic relatedness and kinship structure are an important source of group stability in animal societies, particularly when dominance and/or affilative interactions are typically governed by kinship.     

Hormone response to bidirectional selection on social behavior

Behavior is a quantitative trait determined by multiple genes. Some of these genes may have effects from early development and onward by influencing hormonal systems that are active during different life-stages leading to complex associations, or suites, of traits. Honey bees (Apis mellifera) have been used extensively in experiments on the genetic and hormonal control of complex social behavior, but the relationships between their early developmental processes and adult behavioral variation are not well understood. Bidirectional selective breeding on social food-storage behavior produced two honey bee strains, each with several sublines, that differ in an associated suite of anatomical, physiological, and behavioral traits found in unselected wild type bees. Using these genotypes, we document strain-specific changes during larval, pupal, and early adult life-stages for the central insect hormones juvenile hormone (JH) and ecdysteroids. Strain differences correlate with variation in female reproductive anatomy (ovary size), which can be influenced by JH during development, and with secretion rates of ecdysteroid from the ovaries of adults. Ovary size was previously assigned to the suite of traits of honey bee food-storage behavior. Our findings support that bidirectional selection on honey bee social behavior acted on pleiotropic gene networks. These networks may bias a bee's adult phenotype by endocrine effects on early developmental processes that regulate variation in reproductive traits.