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Social networks formed via play interactions offer a powerful framework for investigating the social dynamics of animals and the functions of play behavior. Using this framework in mantled howler monkeys ( Alouatta palliata ), we examined whether social play might fulfil some of the affiliative and bonding functions typically addressed to allogrooming. We analyzed play networks in seven groups of mantled howler monkeys (89 individuals), analyzing group and individual-level patterns based on 1774 observation hours collected over approximately 3 years. We examined the relationship between group size and network complexity using edge density (the proportion of connections), modularity (the degree to which the network is subdivided into clusters), and average path lengths (the number of steps required to reach others in the network). We analyzed centrality across age-sex classes using betweenness, closeness, and eigenvector metrics. We tested which centrality measure best predicted play evenness, defined as the degree to which individuals distributed their playtime across partners. We found that network interconnectivity generally declined with group size, though average path lengths were not significantly different from those of random networks. Immatures showed the highest centrality values, while adult females exhibited the highest play evenness. However, centrality measures did not significantly predict play evenness. These patterns suggest age-specific functions of social play: immatures may benefit from frequent play to support development, while adult females may use evenly distributed play to navigate social competition. Our findings support the hypothesis that social play serves similar functions to allogrooming, contributing to social bonding.

Social insects employ venom as an external immune defence against pathogens and parasites. Like other Hymenopterans, the venom gland of honey bee ( Apis mellifera ) serves as a reservoir of antimicrobial substances, primarily melittin. This study investigated the presence and origin of venom on honey bee body that could act as an external immune defence in honey bee workers infested by the ectoparasite mite, Varroa destructor . Using a multi-step approach, we first confirmed the presence of venom on bees’ bodies using melittin as a marker. We then examined how grooming could facilitate the distribution of venom on the bee’s body through behavioural observations. Further assays were used to compare melittin levels on the bodies of Varroa -free and Varroa -infested workers and assess the effects of bee-venom on mite activity. Our findings confirmed the occurrence of “venom bathing” in A. mellifera , excluding social components or environmental contamination, with bees likely coating their bodies with antimicrobial substances through self-grooming. Our results further suggest that infested bees spread higher amount of venom on their bodies compared to uninfested bees, and bee-venom significantly reduced mite activity, suggesting that the venom functions as an external defence. However, Varroa negatively impacted melittin production. Our study reveals a previously unknown negative effect of V. destructor : impairment of honey bees’ external immune defence through reduced melittin production.

Termites, being vulnerable to parasitic or pathogenic infections due to large number of individuals living together in colonies, have evolved various behavioral and physiological tactics to resist the infections by those pathogens. Locomotion can help termites collect information on parasites and accordingly exhibit hygienic behaviors. Termites inevitably encounter entomopathogenic fungi during nesting and foraging. However, how these fungal pathogens influence locomotion of termites and how hygienic behavior benefits their survival remains unknown. Here, we examined locomotion alteration of the termite Reticulitermes chinensis (Isoptera: Rhinotermitidae) after infections with different concentrations of the entomopathogenic fungus Metarhizium anisopliae (Hypocreales: Clavicipitaceae). When R. chinensis was isolated, the low concentration (5 × 103 conidia/ml) significantly increased termite locomotion after 6, 12, and 24 h compared with control. However, the high concentrations (5 × 107, 5 × 109 conidia/ml) significantly decreased termite locomotion after 48 h, and termite survival was also significantly lower at 5 × 107 and 5 × 109 conidia/ml compared with the low concentrations and the control. When R. chinensis was in group, however, the locomotion significantly increased 24 h after exposure to 5 × 103 and 5 × 109 conidia/ml but was normalized after 48 h of exposure compared with the control. Allogrooming was significantly higher at 5 × 103 and 5 × 109 conidia/ml compared with the control. The fungal infection did not result in significantly higher mortality of the group termites probably owing to their allogrooming. These findings enhance our understanding on how a termite species copes with biotic stress (i.e., fungal infections) via adaptive behaviors. Graphical Abstract

Background Animals exhibit a wide range of social behaviors, including positive actions that promote social cohesion and negative behaviors associated with asserting dominance. While these behaviors are often viewed as opposites, they can also exist independently or coexist in complex ways, necessitating further investigation into their interrelationships. Results To study the interplay between these two types of behaviors, we examined mouse social behaviors using resident-intruder assays and revealed a negative correlation between social aggression and prosocial allogrooming. Suppressing aggressive motivation through various manipulations, including social subordination, olfaction ablation, and inhibition of aggressive neural circuits, led to an increased display of allogrooming behavior. The mouse findings prompted us to further explore the relationship between aggression and prosocial behaviors in preschool children. Similarly, we observed a negative association between aggression and prosocial behaviors, which were potentially influenced by their inhibitory control abilities. Conclusions Through this cross-species study, we uncovered the inhibitory impact of aggressive neural circuits on mouse allogrooming and established a link between aggression and prosocial behaviors in children. These insights offer valuable implications for understanding and potentially influencing social interactions in both animal and human contexts, with potential applications in preschool education practices.

The evolution of termite eusociality has been influenced by their nesting and foraging ecology. This includes the evolution of a separate developmental line for specialized workers that forego direct reproduction (true workers), which coincides with the transition from inhabiting a dead-wood nest to foraging for food outside the nest. Foraging for extranidal food requires that termites move through an entomopathogen-rich rhizosphere. This suggests that improved defenses against these pathogens were required for the successful transition to foraging outside the nest. Soil is especially rich in insect pathogens such as Metarhizium, and termites use secreted salivary β-1,3-glucanases for protection from this fungus. These enzymes are likely to be dependent on hygiene behaviors, such as allogrooming of external surfaces after contact with fungal conidial spores or ingestion or burying of infected nestmates prior to sporulation of the cadaver. These social mechanisms of defense could compensate for internal innate mechanisms of defense and even relax selective pressure on these innate mechanisms. Here, we investigated whether the selective pressure was intensified or relaxed on secreted β-1,3-glucanases as well as internal innate immune proteins, especially those putatively involved in antifungal defense. An analysis of the molecular evolution of two termite β-1,3-glucanases (GNBP1,2) indicates that the intensity of selection on them significantly increased with the transition to foraging. The shift to foraging for extranidal food apparently required adaptive modification of secreted GNBPs to help cope with increased exposure to pathogenic conidia in the soil. This included modification of a conserved binding site in GNBP2. In contrast, there was either significant relaxation or no change of selection pressure on Toll and phenoloxidase pathway immune genes with the transition to foraging. Relaxation was also observed with the evolution of drywood termites, but this likely reflects a transition to a microhabitat with fewer pathogens. Selection intensified on a subset of immune genes that regulate intestinal microbes with the more recent radiation of the Termitidae and the diversification of their feeding strategies.Significance statementThe evolution of termite worker eusociality coincides with a relaxation of selective pressure on innate components of the immune system, especially those involved in antifungal defense. In contrast, the selective pressure intensified on two β-1,3-glucanases that contribute to the elimination of fungal pathogens by social behaviors such as allogrooming, cannibalism, and undertaking. This change in selective pressure appears to reflect an increased reliance on social immunity by dedicated altruistic workers in response to novel or enhanced threat by fungal pathogens. This supports other studies in social insects that indicate that the evolution of social immunity not only compensates for an increased vulnerability to infectious disease associated with living in crowded conditions but relaxes selective pressure on components of the internal innate immune system. Our results also indicate that a shift to microbially depauperate habitats relaxed selective pressure on termite immune defenses whereas a more recent diversification of diet intensified selection on mechanisms for regulating intestinal microbes.

In group-living animals, allogrooming is a common, heterogeneously distributed affiliative behaviour. Among non-human primates, Barrett et al. (1999) predicted ways in which Biological Markets principles interact with competitive regimes to influence grooming reciprocity and interchange. Most tests of these predictions, done at a group level, have produced inconsistent results. Here we take a novel approach by testing these predictions across individuals within a group. This is based on the premise that in groups facing moderate-to-high within-group-competition, individuals vary in their abilities to access resources based on their competitive abilities, causing them to pursue different grooming exchange strategies. We examine evidence for grooming reciprocity and interchange for tolerance at drinking sources among adult females within a group of rhesus macaques (Macaca mulatta) on Cayo Santiago. We test the above premise by assessing hierarchical steepness, and the relationship between individuals' David's scores (DS) and access to drinking sources. Finally, we examine the relationship of DS with grooming reciprocity and interchange to see whether they are consistent with the operation of market forces among individuals. Social network comparisons revealed that giving grooming was strongly predicted by both receiving drinking tolerance (interchange) and receiving grooming (reciprocity), despite strong associations with proximity and maternal kinship. The group showed a moderately steep hierarchy, and negative correlations between individuals' David's scores and difficulties in accessing drinking stations. Finally, we found partial support for a market-based explanation. Individuals with relatively low David's scores were more likely to interchange grooming with drinking tolerance. However, grooming reciprocity wasn't greater among individuals with higher David's scores. Our findings suggest that multiple explanatory frameworks - reciprocity, market-based interchange, and/or proximity-mediated interchange/social bond investment - may all shape rhesus grooming exchange patterns. Future directions include examining evidence for additional forms of grooming interchange, and the influence of between-group-competition and stress-indicators on grooming reciprocity.

Animal internal states can be expressed via social behaviors that are known to shape group dynamics (i.e., allogrooming, social play, agonistic encounters) and that can be flexibly used after experiencing negative stimuli. In extensively bred domestic species, animals are not always used to human handling, and thus also mandatory health checks can alter group dynamics. Here, we investigated possible fluctuations in social behaviors according to the presence and distance from the health check in a group of young Maremmana heifers and steers in semi-extensive conditions. We found that aggression did not change in relation to the health check. On the contrary, the time individuals spent playing and affiliating with each other drastically reduced in the day after the routinary check (Post 1, 0–24 h) if compared to days far from the event (Control): after that, it reached the highest level in the following day (Post 2, 24–48 h). This rebound effect might allow animals to compensate for the previous lack of social interactions and to restore social homeostasis. The findings suggest that social interactions in Maremmana cattle are informative about their internal states. Additionally, social play and allogrooming appear to function as coping strategies for these cattle. Graphical abstract The routinary check for health status and performance can provoke distress in cattle. Social play and affiliation drastically reduced the day after the check (Post 1, 0–24 h). In the Post 2 (24–48 h), these social activities had a rebound effect. Aggression did not change in relation to the presence of the health check. On the whole, these findings suggest that social play and allogrooming could be effective coping strategies after handling procedures.

Social insects are prone to pathogen infection because of high exposure rates from social interactions. However, it remains unclear whether queens have enhanced pathogen resistance, because reproduction is largely confined to queens. Here, we used a natural host–pathogen system, the subterranean termite Reticulitermes chinensis and the entomopathogenic fungus Metarhizium anisopliae, to investigate the differences in allogrooming, locomotion, and immune gene expression between queens and workers against pathogen infection. We found that fungal infection significantly reduced survival in both queens and workers. Infected queens received significantly more grooming time from sanitary nestmates than infected workers, but they returned much less grooming time to sanitary nestmates than infected workers. Infection resulted in a reduction in the average locomotion speed and distance of queens but had no effect on worker locomotion. Infection resulted in upregulated expression of two immune genes (termicin and transferrin), two antioxidant genes (CAT and SOD), and phosphate genes CYP450 in queens but not in workers. Our results indicated that eusocial termites evolved strategies that prioritize the reproductive castes' welfare in defending against the pathogen infection to ensure continued reproduction and colony persistence.

ABSTRACT Allogrooming behavior is ubiquitous among nonhuman primates and considered to be highly preferences regarding to allogrooming postures and body sites. In order to investigate the allogrooming preference and seasonality of the white-headed black langurs (Trachypithecus leucocephalus), we studied the allogrooming posture and body site of the animal via focal animal sampling and continuous recording in the Chongzuo White-Headed Langur National Nature Reserve from February 2016 to January 2017. Results showed that totally proportions of non-eye contact and eye contact allogrooming postures of the animals accounted for 47.86% and 52.14%, respectively. The most frequently used allogrooming posture in the dry season was sprawl (32.73%), and that of in the rainy season was sit side (33.56%). There were significant differences among allogrooming postures throughout the year (p < 0.001). Proportion of allogrooming in inaccessible area in the dry season was higher than in the rainy season. The grooming preference index was greater than 0 in the dry season and less than 0 in the rainy season. The proportion of difficult to reach area was opposite and there was a significant difference between dry season and rainy season (p = 0.04), and both grooming preference index was greater than 0. The grooming preference index of easy to reach area was less than 0 in dry season and rainy season. Animals were selective in allogrooming sites, the anogenital area had the largest grooming preference index in both dry and rainy seasons. The allogrooming of white-headed black langur appeared to be consistent with the social function hypothesis. In addition, allogrooming was in line with the hygiene function hypothesis during dry season, but not in rainy season. The reason may be associated with variation of food supply between the two seasons. It is necessary to further study before generalizing the function of allogrooming of the langur.

This study presents an extended mathematical model, originally developed to explore biomass dynamics in Acromyrmex ants and their symbiotic fungus, which has been adapted to investigate biomass growth in Atta sexdens and its fungal partner. The model incorporates ant grooming as a defence against entomopathogenic fungi, building on experimental data where self-grooming and allogrooming were quantified across three groups: Metarhizium anisopliae , Escovopsis phialicopiosa , and a control. A second chamber was introduced to simulate biomass transfer between compartments. Inflection points in growth curves were identified to detect shifts in population dynamics, and bifurcation diagrams explored key parameters affecting system stability, namely worker allocation to fungal cultivation, ant mortality, and fungal mortality. Metarhizium anisopliae significantly reduced both ant and fungal biomass, even under optimal grooming conditions, owing to its direct virulence to workers. In contrast, E. phialicopiosa , an opportunistic pathogen, had minimal impact unless fungal mortality exceeded a critical threshold. Self-grooming proved more effective than allogrooming in mitigating M. anisopliae effects, likely owing to prioritisation of individual defences under high pathogen pressure. Spatial dynamics enhanced resilience: one-way transfer between chambers redistributed biomass, delaying inflection points and bolstering structural stability. Bifurcation analysis revealed that extreme proportions of workers cultivating the symbiotic fungus reduced the biomass for both partners, whilst ant and fungal mortality rates led to non-linear declines in most simulations. These findings underscore the role of multi-chamber architecture in mitigating pathogen impacts in Atta colonies and suggest potential applications for biological control strategies by identifying behavioural and structural factors that may limit or enhance the effectiveness of pathogenic fungi in field settings. The model provides a useful framework for understanding epidemiological dynamics in natural nests, integrating behavioural defences and spatial strategies to safeguard this mutualism.