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.     

Behavioral Interactions of Two Solitary,Halictine Bees with Comparisons among Solitary,Communal and Eusocial Species

Laboratory behavioral experiments were conducted with two solitary, halictine bee species, in the genus Lasioglossum, to examine the nature of behavioral interactions between non-nestmate females. The experimental design of this study was identical to previous work on both a communal (Kukuk 1992) and a eusocial Lasioglossum species (Breed et al. 1978), thereby providing data for comparison of female-female interactions in species within a single, very large genus that exhibit different sociality. Both solitary species exhibited low levels of aggressive behavior yet nearly all females were reproductively active, as determined by subsequent dissections. Neither ovarian width nor size was associated with aggression in either species. Interspecific comparisons reveal large differences in cooperation and aggression among the four congeneric species. The communal species exhibits significantly more cooperative and less aggressive behavior than all other species suggesting that communal social behavior in Lasioglossum is not phenetically intermediate between the behavior of solitary and eusocial species.     

Communal Nesting in Asocial Abert's Squirrels: the Role of Social Thermoregulation and Breeding Strategy

The social thermoregulation hypothesis states that endothermic species will communally nest to reduce energy expenditures on thermoregulation. The hypothesis predicts that the frequency of communal nesting should increase with decreasing ambient temperature. The potential costs of communal nesting (e.g., increased predation risk, resource competition, cuckoldry, parasite/disease transmission, or infanticide) could decrease the frequency of communal nesting especially for asocial breeding females with dependent offspring. We examined the effects of ambient temperature and seasonal reproductive activities on the probability of communal nesting in Abert's squirrels (Sciurus aberti) in the Pinaleño Mountains, Arizona. Most squirrels nested consistently with the same partner in mixed‐sex pairs. The proportion of individuals engaging in communal nesting increased with decreasing ambient temperature as predicted by the social thermoregulation hypothesis. The onset of the breeding season greatly reduced the proportion of individuals communally nesting. The negative relationship between ambient temperature and communal nesting supports the use of communal nesting in Abert's squirrels as a mechanism to reduce thermoregulatory costs during cold conditions. The abrupt drop in the frequency of communal nesting during the breeding season is likely due to female abandonment of this behavior. By avoiding communally nesting during the breeding season, females may prevent males from mating with them outside of mating chases, reduce resource competition, and protect offspring from infanticide, diseases, and parasites. Males may gain additional fitness benefits from nesting with females because familiarity with females increases dominance rank in mating activities.     

Effects of familiarity and nestmate number on social interactions in two communal bees, Andrena scotica and Panurgus calcaratus (Hymenoptera, Andrenidae)

Summary: Communality is considered a widespread form of social organization in bees and wasps, one in which two or more females of the same generation share a common nest and amongst whom there is no reproductive division of labor. The evolution and maintenance of egalitarian communal societies poses theoretical difficulties where 'cheating' amongst nestmates is practised. Yet there is little knowledge of the intranidal social interactions among communal conspecifics that allow an understanding of the degree of cooperation versus exploitation amongst nestmates in such societies. Using a circle-tube arena, we staged interactions in the laboratory among pairs of female conspecifics using two communal andrenid species, Andrena scotica and Panurgus calcaratus, to score their cooperative and aggressive behaviors. For both species, females did not discriminate between familiar (nestmate) and unfamiliar (non-nestmate) conspecifics in their cooperative and aggressive behaviors, suggesting that there is universal acceptance of conspecifics. Levels of cooperation and aggression did not vary with the number of nestmates in the nest of origin for either species. In addition, frequencies of social interactions did not vary with body size, wing wear or ovarian development in P. calcaratus. Interspecific comparisons were made with published data on social interactions of other bee species at varying levels of social organization (solitary to eusocial) derived from analogous circle-tube experiments. Panurgus calcaratus displayed highly cooperative behavior, similar to that of a previously studied communal bee, Lasioglossum hemichalceum (Kukuk, 1992a). Andrena scotica displayed lower levels of cooperation, and was in this sense more similar to solitary species and to interactions amongst non-nestmate individuals of eusocial species. Both A. scotica and P. calcaratus displayed very low levels of aggressive behavior, again similar to L. hemichalceum. As a working hypothesis, we suggest the existence of a communal behavioral syndrome comprising high levels of intranidal cooperation and low aggression, both directed indiscriminately at conspecifics.     

Can a solitary avian species use collective detection? An assay in semi-natural conditions

Collective detection (e.g., enhanced predator detection through the vigilance of conspecifics) is expected to have evolved particularly in social species. However, we assessed the degree to which an avian territorial species (California towhee Pipilo crissalis) would use social cues about predation in a semi-natural assay. We also exposed a social species (house finch Carpodacus mexicanus) to similar conditions. California towhees increased scanning rates when foraging with conspecifics, whereas house finches increased scanning rates when foraging solitarily, suggesting that vigilance in these species is regulated mostly through interference competition and through predation risk, respectively. California towhees did not show early detection, and actually the last detector in the group delayed detection in relation to solitary individuals. House finches benefited from early detection, but the second and last detectors maintained detection at the level of solitary individuals. California towhees increased the chances of fleeing when in groups in relation to solitary conditions, but this effect was less pronounced in the last detector. House finches always fled across conditions. Overall, an asocial avian species may use collective detection, but limited to certain types of cues: responses were more pronounced to overt (conspecifics walking or fleeing) rather than subtle (conspecifics becoming alert or crouching) social cues.     

Use of artificial arenas to predict the social organisation of halictine bees: Data for fourteen species from Chile

I studied the behavioural profiles of fourteen species of Chilean halictine bee using the circle tube apparatus. Interactions were classified as aggressive, avoidance or cooperative. One species, Corynura chloris, is believed to be semisocial and its behaviour was largely aggressive, Ruizantheda mutabilis is known to be communal and its behaviour was predominantly cooperative whereas Penapis toroi is a member of a subfamily from which only solitary behaviour is known and it primarily exhibited avoidance behaviours. As a result, I suggest that the relative frequency of these different behaviours may be useful in establishing the social organisation of species. Based upon comparisons of behavioural profiles, I predict the social organizations of the remaining species and suggest that at least some of the bees in the populations of Ruizantheda proxima, Caenohalictus dolator, Ca. species A and Pseudagapostemon pississi investigated exhibit communal behaviour; those of Co. patagonica and Co. herbsti likely have a reproductive division of labour, probably within semisocial societies, and that the populations of Co. corinogaster, Co. melanocladius, Ca. pygosinuatum, Ca. cuprellus and Lasioglossum aricense studied are probably solitary. Phylogenies suggest that solitary behaviour in Ca. pygosinuatum and Ca. cuprellus is reversed from communal behaviour and solitary behaviour in L. aricense may be a reversal from eusociality. The response “back and follow” is not indicative of dominance or cooperation as it correlated only with the frequency of avoidance interactions among the taxa studied. I discuss the utility of the circle tube apparatus in the identification of populations worthy of more detailed sociobiological investigation. Received 10 August 2005; revised 8 March 2006; accepted 21 March 2006.     

Social isolation increases male aggression toward females in the field cricket Gryllus bimaculatus

Social isolation has often been reported to facilitate male aggressiveness in various animal species. If social isolation also escalates male aggressive behavior towards females, the mating success of the aggressive males will be low. This study evaluated the effect of social isolation on mating behavior in the field cricket Gryllus bimaculatus, which has traditionally been considered to be an asocial species. The results showed that social isolation from same-sex individuals enhanced male aggressiveness to females, and the mating success of aggressive males was reduced under the experimental conditions. More aggressive males exhibited a longer latency to court than less aggressive males. These results suggest that because male aggressiveness causes a delay in courtship, aggressive males may have reduced mating success. This demonstrated that social relationships are a critical factor affecting male mating success, even if the species is normally considered solitary.     

The impact of environmental and social factors on learning abilities: a meta-analysis

Since the 1950s, researchers have examined how differences in the social and asocial environment affect learning in rats, mice, and, more recently, a variety of other species. Despite this large body of research, little has been done to synthesize these findings and to examine if social and asocial environmental factors have consistent effects on cognitive abilities, and if so, what aspects of these factors have greater or lesser impact. Here, we conducted a systematic review and meta-analysis examining how different external environmental features, including the social environment, impact learning (both speed of acquisition and performance). Using 531 mean-differences from 176 published articles across 27 species (with studies on rats and mice being most prominent) we conducted phylogenetically corrected mixed-effects models that reveal: (i) an average absolute effect size |d| = 0.55 and directional effect size d = 0.34; (ii) interventions manipulating the asocial environment result in larger effects than social interventions alone; and (iii) the length of the intervention is a significant predictor of effect size, with longer interventions resulting in larger effects. Additionally, much of the variation in effect size remained unexplained, possibly suggesting that species differ widely in how they are affected by environmental interventions due to varying ecological and evolutionary histories. Overall our results suggest that social and asocial environmental factors do significantly affect learning, but these effects are highly variable and perhaps not always as predicted. Most notably, the type (social or asocial) and length of interventions are important in determining the strength of the effect.     

Sexual Differences in Chimpanzee Sociality

Scientists usually attribute sexual differences in sociality to sex-specific dispersal patterns and the availability of kin within the social group. In most primates, the dispersing sex, which has fewer kin around, is the less social sex. Chimpanzees fit well into the pattern, with highly social philopatric males and generally solitary dispersing females. However, researchers in West Africa have long suggested that female chimpanzees can be highly social. We investigated whether chimpanzees in the Taï Forest (Côte d’Ivoire) exhibit the expected sexual differences in 3 social parameters: dyadic association, party composition, and grooming interactions. Though we found a significant sexual difference in each of the 3 parameters, with males being more social than females, the actual values do not reveal striking differences between the sexes and do not support the notion of female chimpanzees as asocial: females had dyadic association indices comparable to mixed-sex dyads, spent ca. 82% of their time together with other adult chimpanzees, and had a comparable number of grooming partners. Further, female associations can be among the strongest bonds within the community, indicating that both sexes can have strongly favored association partners. The findings are in contrast to reports on East African chimpanzees, the females of which are mainly solitary and rarely interact with other females. Our results suggest that researchers cannot generally regard chimpanzee females as asocial and need to redefine models deriving patterns of sociality from dispersal patterns to integrate the possibility of high female sociality in male philopatric systems.     

Mother-infant relations and infant development in captive chimpanzees and orang-utans

Four chimpanzee (Pan troglodytes)mother—infant dyads and four orangutan (Pongo pygmaeus)motherinfant dyads were studied for the first 11 months of the infants’ lives. For both species, ventroventral contact and nipple contact decreased over time at a similar rate, but total contact decreased earlier in the orangutans and was 50% lower than for the chimpanzees at the end of the study. Social play between the mothers and the infants did not differ in frequency between the species, but orangutans played above the ground and chimpanzees on the ground. Solitary play differed in form between the species and, like social play, reflected their differences in arboreal and terrestrial proclivities. In addition, the orangutans engaged in solitary play considerably more frequently than the chimpanzees during the second half-year of life. The developmental differences in mother-infant contact and solitary play of these apes are consistent with the differences in their speciestypical social organization. The data may reflect, therefore, early development of species differences in the social and relatively solitary natures of chimpanzees and orangutans, respectively. An erratum to this article is available at .     

A Quantitative Index of Sociality and Its Application to Group‐Living Spiders and Other Social Organisms

Species are often classified in discrete categories, such as solitary, subsocial, social and eusocial based on broad qualitative features of their social systems. Often, however, species fall between categories or species within a category may differ from one another in ways that beg for a quantitative measure of their sociality level. Here, we propose such a quantitative measure in the form of an index that is based on three fundamental features of a social system: (1) the fraction of the life cycle that individuals remain in their social group, (2) the proportion of nests in a population that contain multiple vs. solitary individuals and (3) the proportion of adult members of a group that do not reproduce, but contribute to communal activities. These are measures that should be quantifiable in most social systems, with the first two reflecting the tendencies of individuals to live in groups as a result of philopatry, grouping tendencies and intraspecific tolerance, and the third potentially reflecting the tendencies of individuals to exhibit reproductive altruism. We argue that this index can serve not only as a way of ranking species along a sociality scale, but also as a means of determining how level of sociality correlates with other aspects of the biology of a group of organisms. We illustrate the calculation of this index for the cooperative social spiders and the African mole‐rats and use it to analyse how sex ratios and interfemale spacing correlate with level of sociality in spider species in the genus Anelosimus.     

ROGERS' PARADOX RECAST AND RESOLVED: POPULATION STRUCTURE AND THE EVOLUTION OF SOCIAL LEARNING STRATEGIES

We explore the evolution of reliance on social and asocial learning using a spatially explicit stochastic model. Our analysis considers the relative merits of four evolved strategies, two pure strategies (asocial and social learning) and two conditional strategies (the "critical social learner," which learns asocially only when copying fails, and the "conditional social learner," which copies only when asocial learning fails). We find that spatial structure generates outcomes that do not always conform to the finding of earlier theoretical analyses that social learning does not enhance average individual fitness at equilibrium (Rogers' paradox). Although we describe circumstances under which the strategy of pure social learning increases the average fitness of individuals, we find that spatial structure introduces a new paradox, which is that social learning can spread even when it decreases the average fitness of individuals below that of asocial learners. We also show that the critical social learner and conditional social learner both provide solutions to the aforementioned paradoxes, although we find some conditions in which pure (random) social learning out-competes both conditional strategies. Finally, we consider the relative merits of critical and conditional social learning under various conditions.     

Individual differences in learning behaviours in humans: Asocial exploration tendency does not predict reliance on social learning

A number of empirical studies have suggested that individual differences in asocial exploration tendencies in animals may be related to those in social information use. However, because the ‘exploration tendency’ in most previous studies has been measured without considering the information-gathering processes, it is yet hard to conclude that the animal asocial exploration strategies may be tied to social information use. Here, we studied human learning behaviour in both asocial and social two-armed bandit tasks. By fitting reinforcement learning models including asocial and/or social decision processes, we measured each individual's (1) asocial exploration tendency and (2) social information use. We found consistent individual differences in the exploration tendency in the asocial tasks. We also found substantive heterogeneity in the adopted learning strategies in the social task: Nearly one-third of participants used predominantly the copy-when-uncertain strategy, while the remaining two-thirds were most likely to have relied only on asocial learning. However, we found no significant individual association between the exploration frequency in the asocial task and the use of the social information in the social task. Our results suggest that the social learning strategies may be independent from the asocial exploration strategies in humans.     

The significance of relatedness and gene flow on population genetic structure in the subsocial spider Eresus cinnaberinus (Araneae: Eresidae)

Interdemic selection, inbreeding and highly structured populations have been invoked to explain the evolution of cooperative social behaviour in the otherwise solitary and cannibalistic spiders. The family Eresidae consists of species ranging from solitary and intermediate subsocial to species exhibiting fully cooperative social behaviour. In this study we, in a hierarchical analysis, investigated relatedness of putative family clusters, inbreeding and population genetic structure of the subsocial spider Eresus cinnaberinus. Five hierarchical levels of investigation ranging from large scale genetic structure (distances of 250 and 50 km level 1 and 2) over microgeographic structure (20 km² and 4 km², level 3 and 4) to a single hill transect of 200 m (level 5) were performed. The purpose of level 5 was two-fold: (1) to investigate the relatedness of putative family groups, and (2) to evaluate the influence of both family living and sampling design on higher level estimates. Relatedness estimates of putative family groups showed an average relatedness of R=0.26. There was no indication of inbreeding. In contrast to social spiders, genetic variation was abundant, H_e?0.10. The population genetic structure was intermediate between social and asocial spiders. Genetic variance increased continually across hierarchical levels. Family structured neighbourhoods biased differentiation estimates among level 5 samples (F_ST? 0.04) and level 3 and 4 samples (0.07ST<0.18), and apparent inbreeding among level 3 and 4 samples, F_IS>0, was caused by disjunct sampling from separate neighbourhoods. Larger scale samples were highly differentiated 0.12ST<0.26, depending on level and sampling design. Due to a distance effect family living did not influence estimates of the higher level 1. Although the dispersing sex among social spiders and the subsocial E. cinnebarinus differ, females versus males, female behaviour of both sociality classes lead to high genetic variance.     

Evolution of conflict and cooperation of nematodes associated with solitary and social sweat bees

Parasites and mutualists can wield great influence on the fitness of social organisms, yet the effect that the host’s social structure has on the evolution of parasites, commensals, and mutualists (collectively referred to here as symbionts) is poorly known. Evolutionary theory suggests that host social structure may select for more cooperative symbiont strains in comparison to symbionts of solitary hosts. We compared the productivity of one social and one solitary bee species (Halictus ligatus and Augochlora pura) in the family Halictidae with and without the presence of their nematode symbionts (Acrostichus halicti and Acrostichus puri, respectively). We measured the number of offspring produced, the number of cells provisioned, and nesting activity (for Au. pura) to test the hypothesis that symbionts specific to a social host exhibit greater cooperation than symbionts specific to a solitary host. Infected and uninfected nests of both species did not differ in any fitness estimates indicating that: (1) Acrostichus species are commensals, or at least lack large fitness effects on their hosts, and (2) the transition from association with a solitary host to association with a social host that lives in small colonies does not have detectable effects on the evolution of conflict and cooperation in this system. This is the first comparative study to test the idea that host social structure may influence the evolution of symbionts; future work should compare closely related mutualists and parasites of more advanced eusocial insects to mutualists and parasites of solitary insects.     

Antifungal skin bacteria,embryonic survival,and communal nesting in four-toed salamanders, <Emphasis Type="Italic">Hemidactylium scutatum</Emphasis>

We examined a novel hypothesis for the maintenance of communal nesting in the salamander, Hemidactylium scutatum, namely that communal nests are more likely than solitary nests to be associated with cutaneous antifungal bacteria, which can inhibit fungal infections of embryos. A communal nest contains eggs of two or more females of the same species. The nesting behavior of H. scutatum females and survival of embryos were determined by frequent nest surveys at three ponds. For communal nests, embryonic survival tended to be higher and catastrophic nest failure was lower. Pure bacterial cultures of resident species were obtained from the salamanders’ skins by swabbing and tested against a fungal pathogen of embryos (Mariannaea sp.) in laboratory assays. We found that 27% of females had skin bacteria inhibitory to Mariannaea sp. Communal nests were more likely to have at least one female with antifungal bacteria than were solitary nests. Using a culture-independent assay (denaturing gradient gel electrophoresis of 16S rRNA gene fragments), we found that bacterial species on females and embryos were more similar to each other than they were to bacterial species found in soil within the nest, suggesting that females transmitted skin bacteria to embryos. The presence of anti-Mariannaea skin bacteria identified from the laboratory assays did not prevent fungal presence in field nests. However, once a nest was visibly infected with fungi, presence of anti-Mariannaea bacteria was positively correlated with survival of embryos. Microbe transmission is usually thought to be a cost of group living, but communal nesting in H. scutatum may facilitate the transmission of antifungal bacteria to embryos.     

Social networks strongly predict the gut microbiota of wild mice

The mammalian gut teems with microbes, yet how hosts acquire these symbionts remains poorly understood. Research in primates suggests that microbes can be picked up via social contact, but the role of social interactions in non-group-living species remains underexplored. Here, we use a passive tracking system to collect high resolution spatiotemporal activity data from wild mice (Apodemus sylvaticus). Social network analysis revealed social association strength to be the strongest predictor of microbiota similarity among individuals, controlling for factors including spatial proximity and kinship, which had far smaller or nonsignificant effects. This social effect was limited to interactions involving males (male-male and male-female), implicating sex-dependent behaviours as driving processes. Social network position also predicted microbiota richness, with well-connected individuals having the most diverse microbiotas. Overall, these findings suggest social contact provides a key transmission pathway for gut symbionts even in relatively asocial mammals, that strongly shapes the adult gut microbiota. This work underlines the potential for individuals to pick up beneficial symbionts as well as pathogens from social interactions.Subject terms: Microbial ecology, Zoology, Community ecology     

Evolution of Social Behavior in Spiders (Araneae; Eresidae and Theridiidae)

Whereas most spiders are asocial, species in eight familiesare known to live all their life in communities and are thus"permanent-social." Their special attributes are: tolerance,interattraction, and cooperation. These peculiarities must havebeen achieved step by step several times independently. Periodic-socialspiders have been studied as a link between asocial and permanent-socialspiders. In two families—the cribellate Eresidae and ecribellateTheridiidae—different steps of periodic sociality havebeen discovered, from brood-care to feeding by regurgitation.The comparative study of the phylogeny of social behavior inboth families uncovers remarkable convergences of patterns fromasocial to permanent-social via periodical-social species ofspiders.     

The effect of social learning in a small population facing environmental change: an agent-based simulation

Learning is defined as behavioral modification due to experience, social or asocial. Social learning might be less costly than asocial learning and allow the rapid accumulation of learned traits across generations. However, the benefits of social learning in a small population of individuals relying on local interactions and experiencing environmental change are not well understood yet. In this study, we used agent-based simulations to address this issue by comparing the performance of social learning to asocial learning and innate behavior, in both a static and a changing environment. Learning was modeled using neural networks, and innate behavior was modeled using genetically coded behaviors. The performance of 10 mobile simulated agents was measured under three environmental scenarios: static, abrupt change and gradual change. We found that social learning allows for a better performance (in terms of survival) than asocial learning in static and abrupt-change scenarios. In contrast, when changes are gradual, social learning delays achieving the correct alternative, while asocial learning facilitates innovation; interestingly, a mixed population (social and asocial learners) performs the best.     

The evolution of communal roosting in birds: origin and secondary losses

Three main benefits are thought to underlie communal roostingin birds: a reduction in thermoregulation demands, a decreasein predation risk, and an increase in foraging efficiency. Iinvestigated interspecific variation in communal roosting tendenciesacross categories of several ecological factors to examine therelevance of each functional hypothesis in the evolutionary transitionto communal roosting and the secondary reversal to solitary roostinghabits. The study phylogenetic tree included 30 families and437 species. Evolutionary transitions to communal roosting occurredmore often on branches with flocking species and with largerspecies but were not associated with diet, territoriality, geographicalarea, or time of day. The association with flocking activitiessuggests that increased foraging efficiency, a factor thoughtto operate through the formation of flocks, may have been akey factor in the origin of avian communal roosting. However,several transitions to communal roosting occurred on brancheswith nonflocking species, indicating that foraging efficiencymay not be the only factor involved in the evolution of communalroosting. Secondary losses of communal roosting habits occurredon several branches, with a concomitant loss of flocking behaviorand a tendency to exhibit territorial behavior and nocturnalforaging. Secondary losses suggest that communal roosting iscostly to perform and maintain and may be lost when an asocialselection regime operates. The large number of exceptions tothe above patterns may force a reevaluation of current functional hypothesesabout communal roosting in birds.