Lena Grinsted

Individual personalities shape task differentiation in a social spider

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.

Wax on, wax off: nest soil facilitates indirect transfer of recognition cues between ant nestmates.

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.

Questioning evidence of group selection in spiders

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.

COOPERATIVE BREEDING FAVORS MATERNAL INVESTMENT IN SIZE OVER NUMBER OF EGGS IN SPIDERS

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.

Effects of within-colony competition on body size asymmetries and reproductive skew in a social spider

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.

Subsocial behaviour and brood adoption in mixed-species colonies of two theridiid 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.

Market forces influence helping behaviour in cooperatively breeding paper wasps

Biological market theory is potentially useful for understanding helping behaviour in animal societies. It predicts that competition for trading partners will affect the value of commodities exchanged. It has gained empirical support in cooperative breeders, where subordinates help dominant breeders in exchange for group membership, but so far without considering one crucial aspect: outside options. We find support for a biological market in paper wasps, Polistes dominula. We first show that females have a choice of cooperative partners. Second, by manipulating entire subpopulations in the field, we increase the supply of outside options for subordinates, freeing up suitable nesting spots and providing additional nesting partners. We predicted that by intensifying competition for help, our manipulation would force dominants to accept a lower price for group membership. As expected, subordinates reduce their foraging effort following our treatments. We conclude that to accurately predict the amount of help provided, social units cannot be viewed in isolation: the surrounding market must also be considered.

Temporarily social spiders do not show personality-based task differentiation

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.

Predictors of nest growth: diminishing returns for subordinates in the paper wasp Polistes dominula

In cooperative breeders, subordinates that have alternative reproductive options are expected to stay and help dominant breeders only as long as they contribute to group productivity, if their fitness is linked with colony success. Female Polistes dominula paper wasps live as cooperative breeders in small groups of typically fewer than 10 females. Subordinates tend to have high-quality outside options, and so could choose alternative breeding tactics if their work efforts increased productivity negligibly. In the founding stage before workers emerge, we tested the effect of various predictors on nest growth, as a proxy for group productivity, and explored the shape of the relationship between group size and nest growth. We found group size to be the only significant predictor of nest growth: variation among body sizes within the group showed no effect, suggesting a lack of size-dependent task specialization in this species. Average body size and average genetic relatedness between group members similarly showed no effects on nest growth. Group size had a non-linear effect so that per-capita benefits to nest growth decreased in larger groups, and groups of 10 or more would benefit negligibly from additional group members. Hence, females might be better off pursuing other options than joining a large group. This finding helps to explain why P. dominula groups are usually relatively small in our study population. Further studies may illuminate the mechanisms behind the smaller per-capita nest growth that we found in larger groups.Significance statementIdentifying which factors influence the productivity of animal groups is key to understanding why different species breed cooperatively in groups of varying sizes. In the paper wasp Polistes dominula, we investigated the growth rate of nests as a measure of group productivity. We found that average body size, the variation in body sizes within the group, and average genetic relatedness between group members did not affect nest growth, while group size had a strong, positive effect: nests grew faster with more group members, but the per-capita benefit decreased in larger groups. The addition of extra group members in groups of 10 or more had negligible effects on nest growth. Hence, wasps may be better off pursuing other options than joining large groups. This finding helps to explain why groups normally consist of fewer than 10 wasps in this population.