Open Access

Task allocation in social insect colonies is generally organised into an age-related division of labour, termed the temporal polyethism schedule, which may in part have evolved to reduce infection of the colony's brood by pests and pathogens. The temporal polyethism schedule is sensitive to colony perturbations that may lead to adaptive changes in task allocation, maintaining colony homeostasis. Though social insects can be infected by a range of parasites, little is known of how these parasites impact within-colony behaviour and the temporal polyethism schedule. We use honey bees (Apis mellifera) experimentally infected by two of their emerging pathogens, Deformed wing virus (DWV), which is relatively understudied concerning its behavioural impact on its host, and the exotic microsporidian Nosema ceranae. We examined parasite effects on host temporal polyethism and patterns of activity within the colony. We found that pathogens accelerated the temporal polyethism schedule, but without reducing host behavioural repertoire. Infected hosts exhibited increased hyperactivity, allocating more time to self-grooming and foraging-related tasks. The strength of behavioural alterations we observed was found to be pathogen specific; behavioural modifications were more pronounced in virus-treated hosts versus N. ceranae-treated hosts, with potential benefits for the colony in terms of reducing within-colony transmission. Investigating the effects of multiple pathogens on behavioural patterns of social insects could play a crucial role in understanding pathogen spread within a colony and their effects on colony social organisation.

While sociality is present in a taxonomically diverse number of species, most animals remain solitary (Bourke, 2011). Over the last centuries, this apparent imbalance in social and non-social animals has led to a great deal of research aimed at shedding light on the biotic and abiotic factors explaining the emergence and maintenance of sociality in nature (West et al., 2015). Among them, microbes were quickly identified as a major problem for the evolution of social life, because frequent contact between group members typically facilitates the transmission of pathogens, high nest fidelity favours the establishment of microbial pathogens close to their social hosts and, finally, because social groups often exhibit limited genetic diversity and thus limited genetic resistance against certain pathogen strains (Schmid-Hempel, 1998; Cremer et al., 2007). However, this long-standing view has changed considerably over the last few years. Recent research indeed revealed that group living may be more effective than solitary living to Limit the risk of infection by pathogenic microbes because group living also allows the development of an additional layer of defence against pathogens in the form of social immunity (Cremer et al., 2007; Cotter and Kilner, 2010). Under strong pressure from pathogens, microbes could therefore promote, rather than hinder, the evolutionary transition from solitary to group Living (Meunier, 2015; Biedermann and Rohlfs, 2017). Moreover, we are increasingly aware that many microbes provide essential benefits to their hosts by performing critical digestive, physiological, and reproductive functions (Engel and Moran, 2013; McFall-Ngai et al., 2013). The need to Access beneficial microbes may thus have played a role in the expression of frequent and tight interactions between conspecifics and ultimately promoted social evolution (Wilson, 1971; Onchuru et al., 2018). Finally, a growing number of studies suggest that microbes could enforce the Aggregation and expression of cooperative behaviours of the hosts to increase their chance of reaching new hosts and may therefore be involved in the evolution of host sociality (Lewin-Epstein et al., 2017) (but see Johnson and Foster, 2018).

The evolution of biological complexity is associated with the emergence of bespoke immune systems that maintain and protect organism integrity. Unlike the well-studied immune systems of cells and individuals, little is known about the origins of immunity during the transition to eusociality, a major evolutionary transition comparable to the evolution of multicellular organisms from single-celled ancestors. We aimed to tackle this by characterizing the immune gene repertoire of 18 cockroach and termite species, spanning the spectrum of solitary, subsocial and eusocial lifestyles. We find that key transitions in termite sociality are correlated with immune gene family contractions. In cross-species comparisons of immune gene expression, we find evidence for a caste-specific social defence system in termites, which appears to operate at the expense of individual immune protection. Our study indicates that a major transition in organismal complexity may have entailed a fundamental reshaping of the immune system optimized for group over individual defence.

There are viral, fungal, bacterial and trypanosomal pathogens that negatively impact the individual and superorganismal health of the western honey bee. One fungal pathogen, Ascosphaera apis , affects larvae and causes the disease chalkbrood. A previous genome analysis of As. apis revealed that its genome encodes for RNA interference genes, similar to other fungi and eukaryotes. Here, we examined whether As. apis -targeting double-stranded RNA species could disrupt the germination of As. apis. We observed that when spores were co-incubated with As. apis -targeting dsRNA, fewer spores were activated for germination, suggesting an uptake of exogenous genetic material at the very onset of germination and consequent damage to essential transcripts needed for germination. Overall, these results indicate that the causative agent of chalkbrood disease, As. apis , can be successfully targeted using an RNAi-based strategy.