Laurent Keller

In social animals, open wounds pose a risk not only for the injured individual but also for its wider social context, especially when the probability of infection transmission is high. To mitigate this danger, different strategies have evolved across species, with ants representing one of the few taxa beyond humans that engage in social wound care. Yet, who provides this care and what drives care provision remains unexplored. To answer these questions, we combined controlled injury experiments with automated behavioral tracking and simulations across six colonies of the ant Camponotus fellah . Our results demonstrate that caregivers are workers in a transitional state between nursing and foraging roles, characterized by elevated activity and broad nest coverage. Being in this transitional state, however, is required but not sufficient to explain the temporal dynamics of individual care provision. Instead, care provisioning is best explained by preinjury spatial overlap, encounter rates, and social interactions, which together constitute an affinity index that predicts both the frequency and duration of subsequent wound care events. We further show that the treatment of open wounds is not the result of a generalized increase in social behaviors directed to the injured ants but part of a care response toward injuries that also involves an increase in allogrooming. Taken together, our findings reveal the necessary conditions for an individual to act as a caregiver and highlight affinity-driven dyadic interactions as an underexplored mechanism for the behavioral coordination of social immunity strategies in decentralized caste-based insect societies.

Understanding how a single genome creates distinct phenotypes remains a fundamental challenge for biologists. Social insects provide a striking example of polyphenism, with queen and worker castes exhibiting morphological, behavioral, and reproductive differences. Here, we show that trophic eggs, which do not contain an embryo and are primarily regarded as a source of food, play a role in the process of caste determination in the harvester ant Pogonomyrmex rugosus. When first instar larvae were given access to trophic eggs, they mostly developed into workers. By contrast, larvae without access to trophic eggs developed into queens. We found that trophic eggs differ in many ways from viable eggs, including texture, morphology, and their contents of protein, triglycerides, glycogen, sugar, and small RNAs. Moreover, comparison of miRNA fragment size distributions suggests differences in the composition of miRNAs between the two egg types. This is the first demonstration of trophic eggs playing a role in caste determination in social insects.

Understanding how a single genome creates distinct phenotypes remains a fundamental challenge for biologists. Social insects provide a striking example of polyphenism, with queen and worker castes exhibiting morphological, behavioural, and reproductive differences. Here we show that trophic eggs, which do not contain an embryo and are primarily regarded as a source of food, play a role in the process of caste determination in the harvester ant Pogonomyrmex rugosus. When first instar larvae were given access to trophic eggs, they mostly developed into workers. By contrast, larvae without access to trophic eggs developed into queens. We found that trophic eggs differ in many ways from viable eggs, including texture, morphology and their contents of protein, triglycerides, glycogen, sugar and small RNAs. Moreover, comparison of miRNA fragment size distributions suggests differences in the composition of miRNAs between the two egg types. This is the first demonstration of trophic eggs playing a role in caste determination in social insects.

Gut microbes can impact cognition and behavior, but whether they regulate the division of labor in animal societies is unknown. We addressed this question using honeybees since they exhibit division of labor between nurses and foragers and because their gut microbiota can be manipulated. Using automated behavioral tracking and controlling for co-housing effects, we show that gut microbes influence the age at which bees start expressing foraging-like behaviors in the laboratory but have no effects on the time spent in a foraging arena and number of foraging trips. Moreover, the gut microbiota did not influence hallmarks of behavioral maturation such as body weight, cuticular hydrocarbon profile, hypopharyngeal gland size, gene expression, and the proportion of bees maturing into foragers. Overall, this study shows that the honeybee gut microbiota plays a role in controlling the onset of foraging-related behavior without permanent consequences on colony-level division of labor and several physiological hallmarks of behavioral maturation. IMPORTANCE: The honeybee is emerging as a model system for studying gut microbiota-host interactions. Previous studies reported gut microbiota effects on multiple worker bee phenotypes, all of which change during behavioral maturation—the transition from nursing to foraging. We tested whether the documented effects may stem from an effect of the microbiota on behavioral maturation. The gut microbiota only subtly affected maturation: it accelerated the onset of foraging without affecting the overall proportion of foragers or their average output. We also found no effect of the microbiota on host weight, cuticular hydrocarbon (CHC) profile, hypopharyngeal gland size, and the expression of behavioral maturation-related genes. These results are inconsistent with previous studies reporting effects of the gut microbiota on bee weight and CHC profile. Our experiments revealed that co-housed bees tend to converge in behavior and physiology, suggesting that spurious associations may emerge when rearing environments are not replicated sufficiently or accounted for analytically.

The ecological success of social insects makes their colony organization fascinating to scientists studying collective systems. In recent years, the combination of automated behavioural tracking and social network analysis has deepened our understanding of many aspects of colony organization. However, because studies have typically worked with single species, we know little about interspecific variation in network structure. Here, we conduct a comparative network analysis across five ant species from five subfamilies, separated by more than 100 Myr of evolution. We find that social network structure is highly conserved across subfamilies. All species studied form modular networks, with two social communities, a similar distribution of individuals between the two communities, and equivalent mapping of task performance onto the communities. Against this backdrop of organizational similarity, queens of the different species occupied qualitatively distinct network positions. The deep conservation of the two community structure implies that the most fundamental behavioural division of labour in social insects is between workers that stay in the nest to rear brood, and those that leave the nest to forage. This division has parallels across the animal kingdom in systems of biparental care and probably represents the most readily evolvable form of behavioural division of labour.

Animals have evolved various sex determination systems. Here, we describe a newly found mechanism. A long noncoding RNA (lncRNA) transduces complementary sex determination (CSD) signal in the invasive Argentine ant. In this haplodiploid species, we identified a 5-kilobase hyper-polymorphic region underlying CSD: Heterozygous embryos become females, while homozygous and hemizygous embryos become males. Heterozygosity at the CSD locus correlates with higher expression of ANTSR , a gene that overlaps with the CSD locus and specifies an lncRNA transcript. ANTSR knockdown in CSD heterozygotes leads to male development. Comparative analyses indicated that, in Hymenoptera, ANTSR is an ancient yet rapidly evolving gene. This study reveals an lncRNA involved in genetic sex determination, alongside a previously unknown regulatory mechanism underlying sex determination based on complementarity among noncoding alleles.

Division of labour is widely thought to increase the task efficiency of eusocial insects. Workers can switch their task to compensate for sudden changes in demand, providing flexible task allocation. In combination with automated tracking technology, we developed a robotic system to precisely control and spatiotemporally manipulate floor temperature over days, which allowed us to predictably drive brood transport behaviour in colonies of the ant Camponotus floridanus. Our results indicate that a small number of workers, usually minors belonging to the nurse social group, are highly specialised for brood transport. There was no difference in the speed at which workers transported brood, suggesting that specialisation does not correlate with efficiency. Workers often started to transport the brood only after having identified a better location. There was no evidence that workers shared information about the presence of a better location. Notably, once brood transporters had been removed, none of the remaining workers performed this task, and the brood transport completely stopped. When brood transporters were returned to their colony, brood transport was immediately restored. Taken together, our study reveals that brood transport is an inflexible task, achieved through the synchronous actions of a few privately informed specialist workers.

Summary: Greenbeards are selfish genetic elements that make their bearers behave either altruistically towards individuals bearing similar greenbeard copies or harmfully towards individuals bearing different copies. They were first proposed by W. D. Hamilton over 50 yr ago, to illustrate that kin selection may operate at the level of single genes. Examples of greenbeards have now been reported in a wide range of taxa, but they remain undocumented in plants. In this paper, we discuss the theoretical likelihood of greenbeard existence in plants. We then question why the greenbeard concept has never been applied to plants and speculate on how hypothetical greenbeards could affect plant–plant interactions. Finally, we point to different research directions to improve our knowledge of greenbeards in plants.