Evidence for coevolution of sociality and relative brain size in three orders of mammals

As the brain is responsible for managing an individual's behavioral response to its environment, we should expect that large relative brain size is an evolutionary response to cognitively challenging behaviors. The "social brain hypothesis" argues that maintaining group cohesion is cognitively demanding as individuals living in groups need to be able to resolve conflicts that impact on their ability to meet resource requirements. If sociality does impose cognitive demands, we expect changes in relative brain size and sociality to be coupled over evolutionary time. In this study, we analyze data on sociality and relative brain size for 206 species of ungulates, carnivores, and primates and provide, for the first time, evidence that changes in sociality and relative brain size are closely correlated over evolutionary time for all three mammalian orders. This suggests a process of coevolution and provides support for the social brain theory. However, differences between taxonomic orders in the stability of the transition between small-brained/nonsocial and large-brained/social imply that, although sociality is cognitively demanding, sociality and relative brain size can become decoupled in some cases. Carnivores seem to have been especially prone to this.     

Differential Adhesion between Moving Particles as a Mechanism for the Evolution of Social Groups

The evolutionary stability of cooperative traits, that are beneficial to other individuals but costly to their carrier, is considered possible only through the establishment of a sufficient degree of assortment between cooperators. Chimeric microbial populations, characterized by simple interactions between unrelated individuals, restrain the applicability of standard mechanisms generating such assortment, in particular when cells disperse between successive reproductive events such as happens in Dicyostelids and Myxobacteria. In this paper, we address the evolutionary dynamics of a costly trait that enhances attachment to others as well as group cohesion. By modeling cells as self-propelled particles moving on a plane according to local interaction forces and undergoing cycles of aggregation, reproduction and dispersal, we show that blind differential adhesion provides a basis for assortment in the process of group formation. When reproductive performance depends on the social context of players, evolution by natural selection can lead to the success of the social trait, and to the concomitant emergence of sizeable groups. We point out the conditions on the microscopic properties of motion and interaction that make such evolutionary outcome possible, stressing that the advent of sociality by differential adhesion is restricted to specific ecological contexts. Moreover, we show that the aggregation process naturally implies the existence of non-aggregated particles, and highlight their crucial evolutionary role despite being largely neglected in theoretical models for the evolution of sociality.     

Third Presentation of the Niko Tinbergen-Förderpreis

Cooperative social life originated independently at least 3 times in the eresid spider genus Stegodyphus. The ultimate and proximate factors for sociogenesis have been analyzed in two African social species, S. dumicola and S. mimosarum.

• 1 More profitable hunting as the ultimate benefit of sociality can explain group sizes up to 30 individuals. Most groups are much larger, reducing average female fecundity. They benefit mainly from the shelter against predators provided by the compact silk nest as a heritable resource.
• 2 Sociogenesis is not based on extended maternal care but on interattraction and tolerance of juvenile spiders, retained throughout life in females. Their neotenic sociality came to overlap with advanced (pedomorphic) sexual maturity. This evolutionary pathway towards sociality is called the “sibling-route”.
• 3 Negative side effects, accumulating with group size, may make sociality in Stegodyphus evolutionarily unstable.

     

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.     

Primordial Enemies: Fungal Pathogens in Thrips Societies

Microbial pathogens are ancient selective agents that have driven many aspects of multicellular evolution, including genetic, behavioural, chemical and immune defence systems. It appears that fungi specialised to attack insects were already present in the environments in which social insects first evolved and we hypothesise that if the early stages of social evolution required antifungal defences, then covariance between levels of sociality and antifungal defences might be evident in extant lineages, the defences becoming stronger with group size and increasing social organisation. Thus, we compared the activity of cuticular antifungal compounds in thrips species (Insecta: Thysanoptera) representing a gradient of increasing group size and sociality: solitary, communal, social and eusocial, against the entomopathogen Cordyceps bassiana. Solitary and communal species showed little or no activity. In contrast, the social and eusocial species killed this fungus, suggesting that the evolution of sociality has been accompanied by sharp increases in the effectiveness of antifungal compounds. The antiquity of fungal entomopathogens, demonstrated by fossil finds, coupled with the unequivocal response of thrips colonies to them shown here, suggests two new insights into the evolution of thrips sociality: First, traits that enabled nascent colonies to defend themselves against microbial pathogens should be added to those considered essential for social evolution. Second, limits to the strength of antimicrobials, through resource constraints or self-antibiosis, may have been overcome by increase in the numbers of individuals secreting them, thus driving increases in colony size. If this is the case for social thrips, then we may ask: did antimicrobial traits and microbes such as fungal entomopathogens play an integral part in the evolution of insect sociality in general?     

Evolving communicative complexity: insights from rodents and beyond

Social living goes hand in hand with communication, but the details of this relationship are rarely simple. Complex communication may be described by attributes as diverse as a species' entire repertoire, signallers' individualistic signatures, or complex acoustic phenomena within single calls. Similarly, attributes of social complexity are diverse and may include group size, social role diversity, or networks of interactions and relationships. How these different attributes of social and communicative complexity co-evolve is an active question in behavioural ecology. Sciurid rodents (ground squirrels, prairie dogs and marmots) provide an excellent model system for studying these questions. Sciurid studies have found that demographic role complexity predicts alarm call repertoire size, while social group size predicts alarm call individuality. Along with other taxa, sciurids reveal an important insight: different attributes of sociality are linked to different attributes of communication. By breaking social and communicative complexity down to different attributes, focused studies can better untangle the underlying evolutionary relationships and move us closer to a comprehensive theory of how sociality and communication evolve.     

ON THE EVOLUTION OF DISPERSAL AND ALTRUISM IN APHIDS

How competitive interactions and population structure promote or inhibit cooperation in animal groups remains a key challenge in social evolution. In eusocial aphids, there is no single explanation for what predisposes some lineages of aphids to sociality, and not others. Because the assumption has been that most aphid species occur in essentially clonal groups, the roles of intra- and interspecific competition and population structure in aphid sociality have been given little consideration. Here, I used microsatellites to evaluate the patterns of variation in the clonal group structure of both social and nonsocial aphid species. Multiclonal groups are consistent features across sites and host plants, and all species—social or not—can be found in groups composed of large fractions of multiple clones, and even multiple species. Between-group dispersal in gall-forming aphids is ubiquitous, implying that factors acting ultimately to increase between-clone interactions and decrease within-group relatedness were present in aphids prior to the origins of sociality. By demonstrating that between-group dispersal is common in aphids, and thus interactions between clones are also common, these results suggest that understanding the ecological dynamics of dispersal and competition may offer unique insights into the evolutionary puzzle of sociality in aphids.     

Social group size predicts the evolution of individuality

Discriminating among individuals is a critical social behavior in humans and many other animals and is often required for offspring and mate recognition, territorial or coalitional behaviors, signaler reliability assessment, and social hierarchies. Being individually discriminated is more difficult in larger groups, and large group size may select for increased individuality-signature information-in social signals, to facilitate discrimination. Small-scale studies suggest that more social species have greater individuality in their social signals, such as contact calls. However, this relationship has not been evaluated in a broader-scale evolutionary context or in social signals other than contact calls. It is not yet known whether social group size may be viewed as a general evolutionary driver of individuality. Here we show a strong positive evolutionary link between social group size in sciurid rodents and individuality in their social alarm calls. Social group size explained over 88% of the variation in vocal individuality in phylogenetic independent contrasts. Species living in larger groups, but not in more complex groups, had more signature information in their calls. Our results suggest that social group size may promote the evolution of individual signatures and that the sociality-individuality relationship may be a general phenomenon in nature.     

Mixed‐species aggregations in arthropods

This review offers the first synthesis of the research on mixed-species groupings of arthropods and highlights the behavioral and evolutionary questions raised by such behavior.Mixed-species groups are commonly found in mammals and birds.Such groups are also observed in a large range of arthropod taxa independent of their level of sociality. Several examples are presented to highlight the mechanisms underlying such groupings, particularly the evidence for phylogenetie proximity between members that promotes cross-species recognition.The advantages offered by such aggregates are described and discussed.These advantages can be attributed to the increase in group size and could be identical to those of nonmixed groupings,but competition-cooperation dynamics might also be involved,and such effects may differ between homo-and heterospecific groups.We discuss three extreme cases of interspecific recognition that are likely involved in mixed-species groups as vectors for cross-species aggregation:tolerance behavior between two social species,one-way mechanism in which one species is attractive to others and two-way mechanism of mutual attraction.As shown in this review,the study of mixed-species groups offers biologists an interesting way to explore the frontiers of cooperation-competition, including the process of sympatric speciation.     

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.     

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.     

Colony size evolution and the origin of eusociality in corbiculate bees (Hymenoptera: Apinae)

Recently, it has been proposed that the one of the main determinants of complex societies in Hymenoptera is colony size, since the existence of large colonies reduces the direct reproductive success of an average individual, given a decreased chance of being part of the reproductive caste. In this study, we evaluate colony size evolution in corbiculate bees and their relationship with the sociality level shown by these bees. Specifically i) the correlation between colony size and level of sociality considering the phylogenetic relationship to evaluate a general evolutionary tendency, and ii) the hypothetical ancestral forms of several clades within a phylogeny of corbiculate bees, to address idiosyncratic process occurring at important nodes. We found that the level of social complexity in corbiculate bees is phylogenetically correlated with colony size. Additionally, another process is invoked to propose why colony size evolved concurrently with the level of social complexity. The study of this trait improves the understanding of the evolutionary transition from simple to complex societies, and highlights the importance of explicit probabilistic models to test the evolution of other important characters involved in the origin of eusociality.     

Communal roosting,thermoregulatory benefits and breeding group size predictability in cooperatively breeding sociable weavers

Extreme temperatures impose energy costs on endotherms through thermoregulation and different adaptations help individuals to cope with these conditions. In social species, communal roosting and huddling are thought to decrease the energetic requirement of thermoregulation under low temperatures. This is likely to represent an important mechanism by which individuals save energy during the coldest parts of the year and hence to represent a non‐breeding benefit of sociality. Here, we investigate the potential thermoregulatory benefits of group living in roosting groups of sociable weavers Philetairus socius, a colonial cooperatively breeding passerine that builds communally a massive nest structure with several independent chambers wherein individuals breed and roost throughout the year. To investigate the benefits of sociality during the non‐breeding season, we studied the thermal environment during roosting in relation to group size. In addition, to understand the link between non‐breeding and breeding sociality in this species we studied group size stability between the pre‐breeding and breeding periods. As expected, we found that the nest chamber's night‐time temperature is strongly related to the number of birds roosting together, especially during cold nights. Specifically, birds in larger groups spent less time below the critical thermal minimum temperature (i.e. the temperature below which energy expenditure increases substantially). They were less exposed to external temperature variations. We also found a positive relationship between the number of birds roosting during winter and the breeding group size, indicating breeding group size predictability. In cooperative breeders such as the sociable weaver, the costs and benefits of sociality are usually studied during the breeding period. This study shows that a better understanding of non‐breeding benefits of group membership and group dynamics between the non‐breeding and breeding periods are necessary for a comprehensive understanding of the benefits of sociality.     

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.     

Phylogeography of the socially polymorphic sweat bee Halictus rubicundus (Hymenoptera: Halictidae)

The evolution of sociality in insects holds a central place in evolutionary theory. By examining the phylogenetic patterns of solitary and social behavior and how they correlate with ecological variables, we may identify factors important in the evolution of sociality. In this study, we investigated historical and biogeographical patterns of sociality in a socially polymorphic bee species (one that demonstrates both social and solitary nesting behavior). This unique system allows for a more powerful examination of evolutionary transitions in sociality than interspecific studies of obligately social and solitary species. We conducted a phylogenetic analysis among populations of the halictine bee Halictus rubicundus and then identified relationships among mitochondrial DNA sequence data, sociality, environmental conditions at the nesting site, and geographic location of populations of this species. Within North America, populations of H. rubicundus expressing social and solitary behavior belong to different genetic lineages. Sociality is also correlated with at least one environmental variable used in this study. Taken together, the results support the predictions for genetic control of sociality, but they are still consistent with social behavior at some level being determined by the environmental conditions at the nesting site.     

Energetic Benefits of Sociality Offset the Costs of Parasitism in a Cooperative Mammal

Sociality and particularly advanced forms of sociality such as cooperative breeding (living in permanent groups with reproductive division of labour) is relatively rare among vertebrates. A suggested constraint on the evolution of sociality is the elevated transmission rate of parasites between group members. Despite such apparent costs, sociality has evolved independently in a number of vertebrate taxa including humans. However, how the costs of parasitism are overcome in such cases remains uncertain. We evaluated the potential role of parasites in the evolution of sociality in a member of the African mole-rats, the only mammal family that exhibits the entire range of social systems from solitary to eusocial. Here we show that resting metabolic rates decrease whilst daily energy expenditure and energy stores (i.e. body fat) increase with group size in social Natal mole rats (Cryptomys hottentotus natalensis). Critically, larger groups also had reduced parasite abundance and infested individuals only showed measurable increases in energy metabolism at high parasite abundance. Thus, in some circumstances, sociality appears to provide energetic benefits that may be diverted into parasite defence. This mechanism is likely to be self-reinforcing and an important factor in the evolution of sociality.     

Communicative roots of complex sociality and cognition

Mammals living in more complex social groups typically have large brains for their body size and many researchers have proposed that the primary driver of the increase in brain size through primate and hominin evolution was the selection pressures associated with sociality. Many mammals, and especially primates, use flexible signals that show a high degree of voluntary control and these signals may play an important role in forming and maintaining social relationships between group members. However, the specific role that cognitive skills play in this complex communication, and how in turn this relates to sociality, is still unclear. The hypothesis for the communicative roots of complex sociality and cognition posits that cognitive demands behind the communication needed to form and maintain bonded social relationships in complex social settings drives the link between brain size and sociality. We review the evidence in support of this hypothesis and why key features of cognitively complex communication such as intentionality and referentiality should be more effective in forming and maintaining bonded relationships as compared with less cognitively complex communication. Exploring the link between cognition, communication and sociality provides insights into how increasing flexibility in communication can facilitate the emergence of social systems characterised by bonded social relationships, such as those found in non‐human primates and humans. To move the field forward and carry out both within‐ and among‐species comparisons, we advocate the use of social network analysis, which provides a novel way to describe and compare social structure. Using this approach can lead to a new, systematic way of examining social and communicative complexity across species, something that is lacking in current comparative studies of social structure.     

Evolution of ungulate mating systems: Integrating social and environmental factors

Ungulates exhibit diverse mating systems that range from monogamous pair territories to highly polygynous leks. We review mating systems and behaviors across ungulates and offer a new approach synthesizing how interacting factors may shape those mating systems. Variability exists in mating systems among and within species of ungulates and likely is affected by predation risk, availability of resources (food and mates), habitat structure, and sociality. Ungulate mating systems may be labile as a consequence of the varying strength of those interacting factors. In addition, degree of polygyny and sexual dimorphism in size are associated with the evolution of mating systems. Neither male–male combat nor paternal care, however, can completely explain differences in sexual size dimorphism for ungulates, a necessary component in understanding the development of some mating systems. Whatever the evolutionary pathway, sexual segregation limits paternal care allowing more intense male–male competition. Selection of habitat structure, because it modifies risk of predation, is a major determinant of sociality for ungulates. Likewise, ruggedness and steepness of terrain limit the types of mating systems that can occur because of limitations in group size and cohesiveness, as well as the ability of males to herd even small groups of females effectively. The quality and defensibility of resources affect mating systems, as does the defensibility of females. Population density of females also may be a critical determinant of the types of mating systems that develop. Size of groups likewise constrains the types of mating tactics that males can employ. Our aim was to use those relationships to create a broad conceptual model that predicts how various environmental and social factors interact to structure mating systems in ungulates. This model provides a useful framework for future tests of the roles of both ecological and social conditions in influencing the social systems of ungulates.     

Both social and ecological factors predict ungulate brain size

Among mammals, the members of some Orders have relatively large brains. Alternative explanations for this have emphasized either social or ecological selection pressures favouring greater information-processing capacities, including large group size, greater foraging efficiency, higher innovation rates, better invasion success and complex problem solving. However, the focal taxa for these analyses (primates, carnivores and birds) often show both varied ecological competence and social complexity. Here, we focus on the specific relationship between social complexity and brain size in ungulates, a group with relatively simple patterns of resource use, but extremely varied social behaviours. The statistical approach we used, phylogenetic generalized least squares, showed that relative brain size was independently associated with sociality and social complexity as well as with habitat use, while relative neocortex size is associated with social but not ecological factors. A simple index of sociality was a better predictor of both total brain and neocortex size than group size, which may indicate that the cognitive demands of sociality depend on the nature of social relationships as well as the total number of individuals in a group.     

Antimicrobial strength increases with group size: implications for social evolution

We hypothesize that aggregations of animals are likely to attract pathogenic micro-organisms and that this is especially the case for semisocial and eusocial insects where selection ultimately led to group sizes in the thousands or even millions, attracting the epithet 'superorganism'. Here, we analyse antimicrobial strength, per individual, in eight thrips species (Insecta: Thysanoptera) that present increasing innate group sizes and show that species with the largest group size (100-700) had the strongest antimicrobials, those with smaller groups (10-80) had lower antimicrobial activity, while solitary species showed none. Species with large innate group sizes showed strong antimicrobial activity while the semisocial species showed no activity until group size increased sufficiently to make activity detectable. The eusocial species behaved in a similar way, with detectable activity appearing once group size exceeded 120. These analyses show that antimicrobial strength is determined by innate group size. This suggests that the evolution of sociality that, by definition, increases group size, may have had particular requirements for defences against microbial pathogens. Thus, increase in group size, accompanied by increased antibiotic strength, may have been a critical factor determining the 'point of no return', early in the evolution of social insects, beyond which the evolution of social anatomical and morphological traits was irreversible. Our data suggest that traits that increase group size in general are accompanied by increased antimicrobial strength and that this was critical for transitions from solitary to social and eusocial organization.