Geographic patterns in the distribution of social systems in terrestrial arthropods

The role of ecology in the evolution and maintenance of arthropod sociality has received increasing research attention in recent years. In some organisms, such as halictine bees, polistine wasps, and social spiders, researchers are investigating the environmental factors that may contribute to high levels of variation in the degree of sociality exhibited both among and within species. Within lineages that include only eusocial members, such as ants and termites, studies focus more on identifying extrinsic factors that may contribute to the dramatic variation in colony size, number of queens, and division of labour that is evident across these species. In this review, I propose a comparative approach that seeks to identify environmental factors that may have a common influence across such divergent social arthropod groups. I suggest that seeking common biogeographic patterns in the distribution of social systems or key social traits may help us to identify ecological factors that play a common role in shaping the evolution of sociality across different organisms. I first review previous studies of social gradients that form along latitudinal and altitudinal axes. Within families and within species, many organisms show an increasing degree of sociality at lower latitudes and altitudes. In a smaller number of cases, organisms form larger groups or found nests cooperatively at higher latitudes and altitudes. I then describe several environmental factors that vary consistently along such gradients, including climate variables and abundance of predators, and outline their proposed role in the social systems of terrestrial arthropods. Finally, I map distributions of a social trait against several climatic factors in five case studies to demonstrate how future comparative studies could inform empirical research.     

Sociality in theridiid spiders: repeated origins of an evolutionary dead end

Evolutionary "dead ends" result from traits that are selectively advantageous in the short term but ultimately result in lowered diversification rates of lineages. In spiders, 23 species scattered across eight families share a social system in which individuals live in colonies and cooperate in nest maintenance, prey capture, and brood care. Most of these species are inbred and have highly female-biased sex ratios. Here we show that in Theridiidae this social system originated eight to nine times independently among 11 to 12 species for a remarkable 18 to 19 origins across spiders. In Theridiidae, the origins cluster significantly in one clade marked by a possible preadaptation: extended maternal care. In most derivations, sociality is limited to isolated species: social species are sister to social species only thrice. To examine whether sociality in spiders represents an evolutionary dead end, we develop a test that compares the observed phylogenetic isolation of social species to the simulated evolution of social and non-social clades under equal diversification rates, and find that sociality in Theridiidae is significantly isolated. Because social clades are not in general smaller than their nonsocial sister clades, the "spindly" phylogenetic pattern-many tiny replicate social clades-may be explained by extinction rapid enough that a nonsocial sister group does not have time to diversify while the social lineage remains extant. In this case, this repeated origin and extinction of sociality suggests a conflict between the short-term benefits and long-term costs of inbred sociality. Although benefits of group living may initially outweigh costs of inbreeding (hence the replicate origins), in the long run the subdivision of the populations in relatively small and highly inbred colony lineages may result in higher extinction, thus an evolutionary dead end.     

The thermal environment as a moderator of social evolution

Animal sociality plays a crucial organisational role in evolution. As a result, understanding the factors that promote the emergence, maintenance, and diversification of animal societies is of great interest to biologists. Climate is among the foremost ecological factors implicated in evolutionary transitions in social organisation, but we are only beginning to unravel the possible mechanisms and specific climatic variables that underlie these associations. Ambient temperature is a key abiotic factor shaping the spatio-temporal distribution of individuals and has a particularly strong influence on behaviour. Whether such effects play a broader role in social evolution remains to be seen. In this review, we develop a conceptual framework for understanding how thermal effects integrate into pathways that mediate the opportunities, nature, and context of social interactions. We then implement this framework to discuss the capacity for temperature to initiate organisational changes across three broad categories of social evolution: group formation, group maintenance, and group elaboration. For each category, we focus on pivotal traits likely to have underpinned key social transitions and explore the potential for temperature to affect changes in these traits by leveraging empirical examples from the literature on thermal and behavioural ecology. Finally, we discuss research directions that should be prioritised to understand the potentially constructive and/or destructive effects of future warming on the origins, maintenance, and diversification of animal societies.     

Is Cooperative Breeding Associated With Bigger Brains? A Comparative Test in the Corvida (Passeriformes)

The cognitive demands of a social existence favour the evolution of relatively large brains and neocortices in primates. Comparable tests of sociality and brain size/structure in birds have not been performed, despite marked similarities in the social systems of birds and mammals. Here, we test whether one aspect of avian sociality, cooperative breeding, is associated with an increase in brain size across 155 species of the passeriform parvorder Corvida. Using conventional and phylogeny‐corrected statistics, we examined the correlated evolution of relative brain size and: the presence/absence of cooperative breeding, percentage of nests that are cooperative and cooperatively breeding group size. Most of the comparisons yielded non‐significant results, which suggests that cooperative breeding is not related to relative brain size in this parvorder. There are a number of potential explanations for our findings. First, changes in brain region size may be correlated with cooperative breeding without affecting overall brain size. Secondly, cooperatively breeding birds might not possess more complex social behaviour than non‐cooperatively breeding birds. Thirdly, relatively large brains might be ancestral in this parvorder. This may predispose them to evolve the range of complex behaviours found in this group, including extreme sociality. Finally, ecological and/or developmental factors might play a more significant role than social behaviour in the diversification of avian brain size. Assessing these alternatives requires more information on the neural and cognitive differences between bird species.     

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.     

Convergent evolution in social swallows (Aves: Hirundinidae)

Behavioral shifts can initiate morphological evolution by pushing lineages into new adaptive zones. This has primarily been examined in ecological behaviors, such as foraging, but social behaviors may also alter morphology. Swallows and martins (Hirundinidae) are aerial insectivores that exhibit a range of social behaviors, from solitary to colonial breeding and foraging. Using a well‐resolved phylogenetic tree, a database of social behaviors, and morphological measurements, we ask how shifts from solitary to social breeding and foraging have affected morphological evolution in the Hirundinidae. Using a threshold model of discrete state evolution, we find that shifts in both breeding and foraging social behavior are common across the phylogeny of swallows. Solitary swallows have highly variable morphology, while social swallows show much less absolute variance in all morphological traits. Metrics of convergence based on both the trajectory of social lineages through morphospace and the overall morphological distance between social species scaled by their phylogenetic distance indicate strong convergence in social swallows, especially socially foraging swallows. Smaller physical traits generally observed in social species suggest that social species benefit from a distinctive flight style, likely increasing maneuverability and foraging success and reducing in‐flight collisions within large flocks. These results highlight the importance of sociality in species evolution, a link that had previously been examined only in eusocial insects and primates.     

Primate sociality in evolutionary context

Much work has been done to further our understanding of the mechanisms that underlie the diversity of primate social organizations, but none has addressed the limits to that diversity or the question of what causes species to either form or not form social networks. The fact that all living primates typically live in social networks makes it highly likely that the last common ancestor of living primates already lived in social networks, and that sociality formed an integral part of the adaptive nature of primate origins. A characterization of primate sociality within the wider mammalian context is therefore essential to further our understanding of the adaptive nature of primate origins. Here we determine correlates of sociality and nonsociality in rodents as a model to infer causes of sociality in primates. We found sociality to be most strongly associated with large-bodied arboreal species that include a significant portion of fruit in their diet. Fruits and other plant products, such as flowers, seeds, and young leaves, are patchily distributed in time and space and are therefore difficult to find. These food resources are, however, predictable and dependable when their location is known. Hence, membership in a social unit can maximize food exploitation if information on feeding sites is shared. Whether sociality evolved in the primate stem lineage or whether it was already present earlier in the evolution of Euarchontoglires remains uncertain, although tentative evidence points to the former scenario. In either case, frugivory is likely to have played an important role in maintaining the presence of a social lifestyle throughout primate evolution.     

The social biology of domiciliary cockroaches: colony structure, kin recognition and collective decisions

A substantial body of research on eusocial insects seen in the last decades has gone hand-in-hand with the development of social evolution theory. In contrast, little attention has been given to the non-eusocial insect species that nevertheless exhibit a rich spectrum of social behaviours, thus effectively skewing our vision of insect sociality. Recent studies on the behaviour, ecology and genetic of “gregarious” cockroaches (Blattodea) have revealed a diversity of social structures and group dynamics unique among insects, providing an important comparative model for the broader understanding of insect social evolution. Here, we present an overview of the social biology of the domiciliary cockroaches (ca. 25 species adapted to human habitats) based on research on two model species, Blattella germanica and Periplaneta americana. We discuss the evolution of these domiciliary cockroaches, considering them in the context of “social herds” within the insect sociality framework.     

Relatedness and genetic structure in a socially polymorphic population of the spider Anelosimus studiosus

The evolution of sociality remains a challenge in evolutionary biology and a central question is whether association between kin is a critical factor favouring the evolution of cooperation. This study examines genetic structure of Anelosimus studiosus, a spider exhibiting polymorphic social behaviour. Two phenotypes have been identified: an ‘asocial’ phenotype with solitary female nests and a ‘social’ phenotype with multi‐female/communal nests. To address the questions of whether these phenotypes are differentiated populations and whether cooperative individuals are closely related, we used microsatellites to analyse individuals from both communal and solitary nests. We found no evidence of differentiation between social and solitary samples, implying high rates of interbreeding. This is consistent with the hypothesis that these phenotypes coexist as a behavioural polymorphism within populations. Pairwise relatedness coefficients were used to test whether cooperating individuals are more closely related than expected by chance. Pairwise relatedness of females sharing communal webs averaged 0.25, the level expected for half‐siblings and significantly more closely related than random pairs from the population. Solitary females collected at similar distances to the communal spider pairs were also more closely related than expected by chance (mean relatedness = 0.18), but less related than social pairs. These results imply that low dispersal contributes to increase likelihood of interaction between kin, but relatedness between social pairs is not explained by spatial structure alone. We propose that these phenotypes represent stages in the evolution of sociality, where viscous population structure creates opportunities for kin selection and cooperation is favoured under certain environmental conditions.     

Social ageing: exploring the drivers of late-life changes in social behaviour in mammals

Social interactions help group-living organisms cope with socio-environmental challenges and are central to survival and reproductive success. Recent research has shown that social behaviour and relationships can change across the lifespan, a phenomenon referred to as ‘social ageing’. Given the importance of social integration for health and well-being, age-dependent changes in social behaviour can modulate how fitness changes with age and may be an important source of unexplained variation in individual patterns of senescence. However, integrating social behaviour into ageing research requires a deeper understanding of the causes and consequences of age-based changes in social behaviour. Here, we provide an overview of the drivers of late-life changes in sociality. We suggest that explanations for social ageing can be categorized into three groups: changes in sociality that (a) occur as a result of senescence; (b) result from adaptations to ameliorate the negative effects of senescence; and/or (c) result from positive effects of age and demographic changes. Quantifying the relative contribution of these processes to late-life changes in sociality will allow us to move towards a more holistic understanding of how and why these patterns emerge and will provide important insights into the potential for social ageing to delay or accelerate other patterns of senescence.     

Is sociality required for the evolution of communicative complexity? Evidence weighed against alternative hypotheses in diverse taxonomic groups

Complex social communication is expected to evolve whenever animals engage in many and varied social interactions; that is, sociality should promote communicative complexity. Yet, informal comparisons among phylogenetically independent taxonomic groups seem to cast doubt on the putative role of social factors in the evolution of complex communication. Here, we provide a formal test of the sociality hypothesis alongside alternative explanations for the evolution of communicative complexity. We compiled data documenting variations in signal complexity among closely related species for several case study groups--ants, frogs, lizards and birds--and used new phylogenetic methods to investigate the factors underlying communication evolution. Social factors were only implicated in the evolution of complex visual signals in lizards. Ecology, and to some degree allometry, were most likely explanations for complexity in the vocal signals of frogs (ecology) and birds (ecology and allometry). There was some evidence for adaptive evolution in the pheromone complexity of ants, although no compelling selection pressure was identified. For most taxa, phylogenetic null models were consistently ranked above adaptive models and, for some taxa, signal complexity seems to have accumulated in species via incremental or random changes over long periods of evolutionary time. Becoming social presumably leads to the origin of social communication in animals, but its subsequent influence on the trajectory of signal evolution has been neither clear-cut nor general among taxonomic groups.     

The other facets of family life and their role in the evolution of animal sociality

Family life forms an integral part of the life history of species across the animal kingdom and plays a crucial role in the evolution of animal sociality. Our current understanding of family life, however, is almost exclusively based on studies that (i) focus on parental care and associated family interactions (such as those arising from sibling rivalry and parent‐offspring conflict), and (ii) investigate these phenomena in the advanced family systems of mammals, birds, and eusocial insects. Here, we argue that these historical biases have fostered the neglect of key processes shaping social life in ancestral family systems, and thus profoundly hamper our understanding of the (early) evolution of family life. Based on a comprehensive survey of the literature, we first illustrate that the strong focus on parental care in advanced social systems has deflected scrutiny of other important social processes such as sibling cooperation, parent–offspring competition and offspring assistance. We then show that accounting for these neglected processes – and their changing role over time – could profoundly alter our understanding of the origin and subsequent evolution of family life. Finally, we outline how this ‘diachronic’ perspective on the evolution of family living provides novel insights into general processes driving the evolution of animal sociality. Overall, we infer that the explicit consideration of thus‐far neglected facets of family life, together with their study across the whole diversity of family systems, are crucial to advance our understanding of the processes that shape the evolution of social life.     

Evaluating Population Receptive Field Estimation Frameworks in Terms of Robustness and Reproducibility

Within vision research retinotopic mapping and the more general receptive field estimation approach constitute not only an active field of research in itself but also underlie a plethora of interesting applications. This necessitates not only good estimation of population receptive fields (pRFs) but also that these receptive fields are consistent across time rather than dynamically changing. It is therefore of interest to maximize the accuracy with which population receptive fields can be estimated in a functional magnetic resonance imaging (fMRI) setting. This, in turn, requires an adequate estimation framework providing the data for population receptive field mapping. More specifically, adequate decisions with regard to stimulus choice and mode of presentation need to be made. Additionally, it needs to be evaluated whether the stimulation protocol should entail mean luminance periods and whether it is advantageous to average the blood oxygenation level dependent (BOLD) signal across stimulus cycles or not. By systematically studying the effects of these decisions on pRF estimates in an empirical as well as simulation setting we come to the conclusion that a bar stimulus presented at random positions and interspersed with mean luminance periods is generally most favorable. Finally, using this optimal estimation framework we furthermore tested the assumption of temporal consistency of population receptive fields. We show that the estimation of pRFs from two temporally separated sessions leads to highly similar pRF parameters.     

Ecological constraints drive social evolution in the African mole-rats.

The African mole-rats (family Bathyergidae) are subterranean hystricomorph rodents occurring in a variety of habitats and displaying levels of sociality which range from solitary to eusocial, making them a unique mammalian taxonomic group to test ecological influences on sociality. Here, we use an extensive DNA-based phylogeny and comparative analysis to investigate the relationship between ecology, sociality and evolution within the family. Mitochondrial cytochrome-b and 12s rRNA trees reveal that the solitary species are monophyletic when compared to the social species. The naked mole-rat (Heterocephalus glaber) is ancestral and divergent from the Damaraland mole-rat (Cryptomys damarensis), supporting previous findings that have suggested the multiple evolution of eusociality within the family. The Cryptomys genus is species-rich and contains taxa exhibiting different levels of sociality, which can be divided into two distinct clades. A total of seven independent comparisons were generated within the phylogeny, and three ecological variables were significantly correlated with social group size: geophyte density (p < 0.05), mean months per year of rainfall greater than 25 mm (p < 0.001), and the coefficient of rainfall variation (p = 0.001). These results support the food-aridity hypothesis for the evolution of highly social cooperative behaviour in the Bathyergidae, and are consistent with the current theoretical framework for skew theory.     

Comparative analyses suggest that information transfer promoted sociality in male bats in the temperate zone

The evolution of sociality is a central theme in evolutionary biology. The vast majority of bats are social, which has been explained in terms of the benefits of communal breeding. However, the causes for segregated male groups remain unknown. In a comparative study, we tested whether diet and morphological adaptations to specific foraging styles, two factors known to influence the occurrence of information transfer, can predict male sociality. Our results suggest that the species most likely to benefit from information transfer--namely, those preying on ephemeral insects and with morphological adaptations to feeding in open habitat--are more likely to form male groups. Our findings also indicate that solitary life was the ancestral state of males and sociality evolved in several lineages. Beyond their significance for explaining the existence of male groups in bats, our findings highlight the importance of information transfer in the evolution of animal sociality.     

Sociality in New World hystricognath rodents is linked to predators and burrow digging

The importance of predation and burrow digging in explainingthe evolution of sociality is generally unclear. We focusedon New World hystricognath rodents to evaluate three key predictionsof the predation hypothesis. First, large-bodied surface-dwellingspecies will be more vulnerable because they are more detectable;thus sociality should be associated with body size. Second,surface-dwelling, diurnal species would be more vulnerable topredators than nocturnal species; thus sociality should be associatedwith the evolution of diurnality. Third, species living in openhabitats will be more vulnerable; thus sociality should evolvein species living in open habitats. Regarding the importanceof burrows, we tested if species that dig burrows can benefitfrom communal labor; thus, sociality should be associated withburrow digging. All traits had significant phylogenetic signal,thus comparative analyses should explicitly address this. Ina comparative analysis on independent contrasts we found thatsociality was correlated with body size (larger species weremore social), diurnality (diurnal species were more social),and burrowing (burrowing species were more social), but we foundno effect of overhead plant cover of habitat on sociality inhystricognath rodents. Somewhat different results were foundwhen we analyzed the raw data. Taken together, our results providesupport for a link between predation risk, burrow digging, andsociality in this group.     

Group living in squamate reptiles: a review of evidence for stable aggregations

How sociality evolves and is maintained remains a key question in evolutionary biology. Most studies to date have focused on insects, birds, and mammals but data from a wider range of taxonomic groups are essential to identify general patterns and processes. The extent of social behaviour among squamate reptiles is under‐appreciated, yet they are a promising group for further studies. Living in aggregations is posited as an important step in the evolution of more complex sociality. We review data on aggregations among squamates and find evidence for some form of aggregations in 94 species across 22 families. Of these, 18 species across 7 families exhibited ‘stable’ aggregations that entail overlapping home ranges and stable membership in long‐term (years) or seasonal aggregations. Phylogenetic analysis suggests that stable aggregations have evolved multiple times in squamates. We: (i) identify significant gaps in our understanding; (ii) outline key traits which should be the focus of future research; and (iii) outline the potential for utilising reproductive skew theory to provide insights into squamate sociality.     

GROUP FORMATION AND THE EVOLUTION OF SOCIALITY

In spite of its intrinsic evolutionary instability, altruistic behavior in social groups is widespread in nature, spanning from organisms endowed with complex cognitive abilities to microbial populations. In this study, we show that if social individuals have an enhanced tendency to form groups and fitness increases with group cohesion, sociality can evolve and be maintained in the absence of actively assortative mechanisms such as kin recognition or nepotism toward other carriers of the social gene. When explicitly taken into account in a game‐theoretical framework, the process of group formation qualitatively changes the evolutionary dynamics with respect to games played in groups of constant size and equal grouping tendencies. The evolutionary consequences of the rules underpinning the group size distribution are discussed for a simple model of microbial aggregation by differential attachment, indicating a way to the evolution of sociality bereft of peer recognition.     

Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies

This paper introduces a theme issue presenting the latest developments in research on the impacts of sociality on health and fitness. The articles that follow cover research on societies ranging from insects to humans. Variation in measures of fitness (i.e. survival and reproduction) has been linked to various aspects of sociality in humans and animals alike, and variability in individual health and condition has been recognized as a key mediator of these relationships. Viewed from a broad evolutionary perspective, the evolutionary transitions from a solitary lifestyle to group living have resulted in several new health-related costs and benefits of sociality. Social transmission of parasites within groups represents a major cost of group living, but some behavioural mechanisms, such as grooming, have evolved repeatedly to reduce this cost. Group living also has created novel costs in terms of altered susceptibility to infectious and non-infectious disease as a result of the unavoidable physiological consequences of social competition and integration, which are partly alleviated by social buffering in some vertebrates. Here, we define the relevant aspects of sociality, summarize their health-related costs and benefits, and discuss possible fitness measures in different study systems. Given the pervasive effects of social factors on health and fitness, we propose a synthesis of existing conceptual approaches in disease ecology, ecological immunology and behavioural neurosciences by adding sociality as a key factor, with the goal to generate a broader framework for organismal integration of health-related research.     

Higher disease prevalence can induce greater sociality: a game theoretic coevolutionary model

There is growing evidence that communicable diseases constitute a strong selective force on the evolution of social systems. It has been suggested that infectious diseases may determine upper limits of host sociality by, for example, inducing territoriality or early juvenile dispersal. Here we use game theory to model the evolution of host sociality in the context of communicable diseases. Our model is then augmented with the evolution of virulence to determine coevolutionarily stable strategies of host sociality and pathogen virulence. In contrast to a controversial hypothesis by Ewald (1994), our analysis indicates that pathogens may become more virulent when contact rates are low, and their prevalence can ultimately induce greater sociality.