Any field study showing convincing evidence of group selection would be a significant contribution to the field of evolutionary biology. Pruitt and Goodnight1 claim to provide such evidence in a 14–18-month field experiment on spiders. However, we contend that apparent flaws in their predictions, assumptions, methods and interpretations undermine this claim. We believe that the data presented are unreliable and are equally consistent with both group selection and individual-level selection; thus, we question the conclusion of Pruitt and Goodnight1 that group selection has produced the observed patterns.

Task differentiation in cooperative groups can arise through a wide range of mechanisms. A recent hypothesis, supported by empirical studies of social spiders, suggests that a variation in individual personalities might be one such mechanism. Personality-based task differentiation can either arise as an emergent property of group living based on inherent behavioural variation among individuals, or alternatively it could be an adaptation to permanent sociality favoured by individual fitness benefits arising from increased group efficiency and productivity. We tested whether personality-based task differentiation is present in the temporarily social spider Stegodyphus tentoriicola which represents the ancestral state from which permanent sociality in spiders has evolved. This species is closely related to the permanently social Stegodyphus sarasinorum in which personality-based task differentiation has been documented. We measured individual boldness and investigated individual participation in simulated prey capture events twice per day on 5 consecutive days. We found no evidence for personality-based task differentiation: S. tentoriicola spiders did not exhibit consistent personalities in boldness or consistent task differentiation in prey attack. Our results lend support for the hypothesis that personality-based task differentiation is an adaptation to permanently social living in spiders as their ancestral representative lacks this trait.

Dispatch: In social animals, group efficiency is often assumed to increase with task differentiation, but this requires that individuals are better than generalists at the task they specialize in. A new study finds that individual Anelosimus studiosus spiders do predominantly perform the task they excel at, in line with their individual personality type, when they are placed in groups.

The transition to cooperative breeding may alter maternal investment strategies depending on density of breeders, extent of reproductive skew, and allo-maternal care. Change in optimal investment from solitary to cooperative breeding can be investigated by comparing social species with nonsocial congeners. We tested two hypotheses in a mainly semelparous system: that social, cooperative breeders, compared to subsocial, solitarily breeding congeners, (1) lay fewer and larger eggs because larger offspring compete better for limited resources and become reproducers; (2) induce egg size variation within clutches as a bet-hedging strategy to ensure that some offspring become reproducers. Within two spider genera, Anelosimus and Stegodyphus, we compared species from similar habitats and augmented the results with a mini-meta-analysis of egg numbers depicted in phylogenies. We found that social species indeed laid fewer, larger eggs than subsocials, while egg size variation was low overall, giving no support for bet-hedging. We propose that the transition to cooperative breeding selects for producing few, large offspring because reproductive skew and high density of breeders and young create competition for resources and reproduction. Convergent evolution has shaped maternal strategies similarly in phylogenetically distant species and directed cooperatively breeding spiders to invest in quality rather than quantity of offspring.

Deciphering the mechanisms involved in shaping social structure is key to a deeper understanding of the evolutionary processes leading to sociality. Individual specialization within groups can increase colony efficiency and consequently productivity. Here, we test the hypothesis that within-group variation in individual personalities (i.e. boldness and aggression) can shape task differentiation. The social spider Stegodyphus sarasinorum (Eresidae) showed task differentiation (significant unequal participation) in simulated prey capture events across 10-day behavioural assays in the field, independent of developmental stage (level of maturation), eliminating age polyethism. Participation in prey capture was positively associated with level of boldness but not with aggression. Body size positively correlated with being the first spider to emerge from the colony as a response to prey capture but not with being the first to attack, and dispersal distance from experimental colonies correlated with attacking but not with emerging. This suggests that different behavioural responses to prey capture result from a complex set of individual characteristics. Boldness and aggression correlated positively, but neither was associated with body size, developmental stage or dispersal distance. Hence, we show that personalities shape task differentiation in a social spider independent of age and maturation. Our results suggest that personality measures obtained in solitary, standardized laboratory settings can be reliable predictors of behaviour in a social context in the field. Given the wealth of organisms that show consistent individual behavioural differences, animal personality could play a role in social organization in a diversity of animals.

Understanding how colony-level behaviour is determined is of evolutionary significance because colony-level traits can influence individual fitness and group success. Here we explore how the composition of individual behavioural types within colonies influences colony-level behaviour in the social spider Stegodyphus sarasinorum. First, we tested whether S. sarasinorum show stable individual differences in behaviour (i.e. individual personalities) and whether aspects of individuals' behaviour are correlated across contexts, in the form of a behavioural syndrome. As documented in many other animals, S. sarasinorum showed stable individual differences in behaviour that were repeatable across time, and correlated across contexts (i.e. aggressiveness, boldness). Second, we tested for and confirmed the presence of consistent intercolony variation (i.e. colony-level personalities) in collective foraging behaviour. Third, we generated artificially reconstituted colonies of known group size and personality composition to test for associations between colonies' personality composition and their collective foraging behaviour. In experimental colonies, we found that the average phenotypes of colony constituents were associated with colony-level behaviour, where colonies composed of smaller and bolder spiders were more responsive during foraging. However, the single best predictor of colony-level behaviour was the behavioural type of the single most extreme individual, where the boldness score of boldest individuals explained 66–69% of the variation in colony-level behaviour. Together, our results suggest that variation in the personality composition of social groups may be an important driver of variation in colony-level personality.

Understanding the social organization of group-living organisms is crucial for the comprehension of the underlying selective mechanisms involved in the evolution of cooperation. Division of labour and caste formation is restricted to eusocial organisms, but behavioural asymmetries and reproductive skew is common in other group-living animals. Permanently, social spiders form highly related groups with reproductive skew and communal brood care. We investigated task differentiation in nonreproductive tasks in two permanently and independently derived social spider species asking the following questions: Do individual spiders vary consistently in their propensity to engage in prey attack? Are individual spiders' propensities to engage in web maintenance behaviour influenced by their previous engagement in prey attack? Interestingly, we found that both species showed some degree of task specialization, but in distinctly different ways: Stegodyphus sarasinorum showed behavioural asymmetries at the individual level, that is, individual spiders that had attacked prey once were more likely to attack prey again, independent of their body size or hunger level. In contrast, Anelosimus eximius showed no individual specialization, but showed differentiation according to instar, where adult and subadult females were more likely to engage in prey attack than were juveniles. We found no evidence for division of labour between prey attack and web maintenance. Different solutions to achieve task differentiation in prey attack for the two species studied here suggest an adaptive value of task specialization in foraging for social spiders.

Cooperation and group living often evolves through kin selection. However, associations between unrelated organisms, such as different species, can evolve if both parties benefit from the interaction. Group living is rare in spiders, but occurs in cooperative, permanently social spiders, as well as in territorial, colonial spiders. Mixed species spider colonies, involving closely related species, have rarely been documented. We examined social interactions in newly discovered mixed-species colonies of theridiid spiders on Bali, Indonesia. Our aim was to test the degree of intra- and interspecific tolerance, aggression and cooperation through behavioural experiments and examine the potential for adoption of foreign brood. Morphological and genetic analyses confirmed that colonies consisted of two related species Chikunia nigra (O.P. Cambridge, 1880) new combination (previously Chrysso nigra) and a yet undescribed Chikunia sp. Females defended territories and did not engage in cooperative prey capture, but interestingly, both species seemed to provide extended maternal care of young and indiscriminate care for foreign brood. Future studies may reveal whether these species adopt only intra-specific young, or also inter-specifically. We classify both Chikunia species subsocial and intra- and interspecifically colonial, and discuss the evolutionary significance of a system where one or both species may potentially benefit from mutual tolerance and brood adoption.

Social animals use recognition cues to discriminate between group members and non-members. These recognition cues may be conceptualized as a label, which is compared to a neural representation of acceptable cue combinations termed the template. In ants and other social insects, the label consists of a waxy layer of colony-specific hydrocarbons on the body surface. Genetic and environmental differences between colony members may confound recognition and social cohesion, so many species perform behaviors that homogenize the odor label, such as mouth-to-mouth feeding and allogrooming. Here, we test for another mechanism of cue exchange: indirect transfer of cuticular hydrocarbons via the nest material. Using a combination of chemical analysis and behavioral experiments with Camponotus aethiops ants, we show that nest soil indirectly transfers hydrocarbons between ants and affects recognition behavior. We also found evidence that olfactory cues on the nest soil influence nestmate recognition, but this effect was not observed in all colonies. These results demonstrate that cuticular hydrocarbons deposited on the nest soil are important in creating uniformity in the odor label and may also contribute to the template.

Reproductive partitioning is a key component of social organization in groups of cooperative organisms. In colonies of permanently social spiders of the genus Stegodyphus less than half of the females reproduce, while all females, including nonreproducers, perform suicidal allo-maternal care. Some theoretical models suggest that reproductive skew is a result of contest competition within colonies, leading to size hierarchies where only the largest females become reproducers. We investigated the effect of competition on within-group body size variation over six months in S. dumicola, by manipulating food level and colony size. We found no evidence that competition leads to increased size asymmetry within colonies, suggesting that contest competition may not be the proximate explanation for reproductive skew. Within-colony body size variation was high already in the juvenile stage, and did not increase over the course of the experiment, suggesting that body size variation is shaped at an early stage. This might facilitate task specialization within colonies and ensure colony-level reproductive output by early allocation of reproductive roles. We suggest that reproductive skew in social spiders may be an adaptation to sociality selected through inclusive fitness benefits of allo-maternal care as well as colony-level benefits maximizing colony survival and production.

In animal societies, recognition of group members and relatives is an important trait for the evolution and maintenance of social behavior. In eusocial insects, nest mate recognition is based on cuticular hydrocarbons and allows colony members to reject competitors and parasites. The study of recognition cues in subsocial species can provide insights into evolutionary pathways leading to permanent sociality and kin-selected benefits of cooperation. In subsocial spiders, empirical evidence suggests the existence of both kin recognition and benefits of cooperating with kin, whereas the cues for kin recognition have yet to be identified. However, cuticular hydrocarbons have been proposed to be involved in regulation of tolerance and interattraction in spider sociality. Here, we show that subsocial Stegodyphus lineatus spiderlings have cuticular hydrocarbon profiles that are sibling-group specific, making cuticular hydrocarbons candidates for kin recognition cues. Our behavioral assays indicate that spiderlings can discriminate between cuticular cues from kin and nonkin: In a choice set-up, spiderlings more often chose to reside near cuticular chemical extracts of siblings compared with nonsiblings. Furthermore, we show that cuticular chemical composition changes during development, especially around the stage of dispersal, supporting the hypothesis that cuticular cues are involved in regulating conspecific tolerance levels. Lastly, our results indicate that the potential kin recognition cues might be branched alkanes that are influenced very little by rearing conditions and may be genetically determined. This indicates that a specific group of cuticular chemicals, namely branched alkanes, could have evolved to act as social recognition cues in both insects and spiders