From individual to collective immunity: The role of the venom as antimicrobial agent in the Stenogastrinae wasp societies

Abstract

a b s t r a c tSociality is associated with an increased risk of disease transmission and one of the first defense of the insect colonies is represented by antimicrobial secretions. In many eusocial hymenopteran species venom glands represent one of the most important source of antimicrobial substances. It is known that in highly eusocial species the venom is spread on both the cuticle of insects and the comb, thus becoming a component of the so called ''social immunity''. So far, it is never been ascertained whether this phenomenon is also present in more primitively eusocial and incipiently eusocial groups. Using incipiently eusocial hover wasps as model, we demonstrate that venom is present on insect cuticles and that it strongly acts against microorganisms. By contrast, the nest, regardless of materials, does not represent a ''medium'' where the venom is deposited by wasps in order to act as a social antiseptic weapon. Our findings discussed in an evolutionary perspective indicate that a certain degree of sociality or a sufficient number of individuals in an insect society are thresholds to be reached for the rise of complex and efficient forms of collective and social immunity as mechanisms of resistance to diseases.

Insect immunology and hematopoiesis

“…Subsequent studies broadened this definition to include non-eusocial insects, and defined social immunity as (1) immune responses that have been selected to increase the fitness of a challenged individual and one or more recipient (Cotter and Kilner, 2010), or (2) collective and personal mechanisms that are maintained at least in part by the anti-pathogen defense they provide to other members of the group (Meunier, 2015). Examples of social immunity include, but are not limited to, avoiding contaminated habitats (Rozen et al, 2008), collecting antimicrobial substances (Simone-Finstrom and Spivak, 2010), depositing materials with antimicrobial properties on the nest or brood (Baracchi et al, 2012; Reavey et al, 2014), removing infected or dead individuals (Diez et al, 2012), allogrooming (Walker and Hughes, 2009), social fever (Starks et al, 2000), transgenerational immune priming (Moret and Schmid-Hempel, 2001; Rosengaus et al, 2013; Trauer-Kizilelma and Hilker, 2015), and immune priming of nestmates (Traniello et al, 2002; Ugelvig and Cremer, 2007). …”

Venom as a Component of External Immune Defense in Hymenoptera

“…The presence of venom compounds with strong antimicrobial activity on insect surfaces suggests that the venom acts also as a chemical barrier providing a first line of protection against microorganisms. Besides Polistes paper wasps (Turillazzi 2006;Turillazzi et al 2006), the presence of venom components with strong antimicrobial activity on the epicuticle has been recently documented in Stenogastrinae wasps (Baracchi et al , 2012b. Stenogastrinae wasps are a subfamily of tropical facultative eusocial wasps, closely related to Polistinae and Vespinae, forming simple societies that are very small in size.…”

“…The most likely explanation is the use of cleaning movements during grooming to smear venom on the body. Self-grooming observations in Stenogastrinae wasps suggest the possibility that little drops of venom released from the sting can be collected with the legs by the wasps and applied all over the body surface (Baracchi et al 2012b). The importance of grooming for the spread of antimicrobial active substances derived from the venom gland has recently also been shown in the ant Lasius neglectus (Tragust et al 2013a).…”

“…On the other hand, factors such as the relative contribution of social lifestyle and of phylogenetic relationships to the evolution of external immune defense clearly need to be considered and disentangled. For example, the primitive social hover wasps Stenogastrinae lack venom compounds on the nest surface, despite the fact that not a single species excavates burrows (Baracchi et al 2012b). The following section of this chapter will explore whether lifehistory traits of social insects, namely, the high number of often closely related individuals living in high …”

“…Since the increase in antimicrobial strength on the cuticle found in the study of Stow and coworkers (Stow et al 2007) was not linear, with the greatest increment being between smaller group sizes, it was suggested that selection pressure from microbial pathogens is so intense that even minimal sociality requires substantially stronger antimicrobials. Support for this hypothesis comes from the fact that even minimal societies such as those of the hover wasps Metischnogaster drewseni, whose colonies count a maximum of two to three females, have strong antimicrobial venoms (Baracchi et al 2012b). The same link between the strength of antimicrobial compounds and level of sociality has been established in both wasps (Hoggard et al 2011) and bees (Stow et al 2007), but information is lacking for ants.…”