Social Prophylaxis: Group Interaction Promotes Collective Immunity in Ant Colonies

Abstract

Life in a social group increases the risk of disease transmission. To counteract this threat, social insects have evolved manifold antiparasite defenses, ranging from social exclusion of infected group members to intensive care. It is generally assumed that individuals performing hygienic behaviors risk infecting themselves, suggesting a high direct cost of helping. Our work instead indicates the opposite for garden ants. Social contact with individual workers, which were experimentally exposed to a fungal parasite, provided a clear survival benefit to nontreated, naive group members upon later challenge with the same parasite. This first demonstration of contact immunity in Social Hymenoptera and complementary results from other animal groups and plants suggest its general importance in both antiparasite and antiherbivore defense. In addition to this physiological prophylaxis of adult ants, infection of the brood was prevented in our experiment by behavioral changes of treated and naive workers. Parasite-treated ants stayed away from the brood chamber, whereas their naive nestmates increased brood-care activities. Our findings reveal a direct benefit for individuals to perform hygienic behaviors toward others, and this might explain the widely observed maintenance of social cohesion under parasite attack in insect societies.

Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies

“…Deformed wing virus infected bees pose a threat for the colony as: (1) quite all the A. mellifera colonies are naturally infested by the Varroa destructor mite and the phoretic mites are able to horizontally transmit DWV to adult healthy bees when feeding on the bees' haemolymph (Santillán-Galicia et al, 2010); (2) DWV can be transmitted horizontally to larvae via larval food containing DWV (Gisder et al, 2009;Yue and Genersch, 2005); (3) the detection of DWV in the midgut content (Fievet et al, 2006) and bee faeces implies the possibility of a faecal-oral-route of transmission between adult bees. Even if handling sick individuals could increase horizontal transmission risk, there are evidence that this behaviour could be also trigger immunization of the hygenic individuals as demonstrate in termites (Traniello et al, 2002), in ants (Ugelvig and Cremer, 2007) and in bumblebee (Sadd and Schmid-Hempel, 2006). As consequence, removing sick nestmates from the colony could represent a better solution to counteract epidemics than leave them into the nest.…”

“…On the other hand, sociality provides protection from parasites at the colony level as well as collective behavioural defence achieved by all the group members cooperating together, avoiding or eliminating parasitic infections Ugelvig and Cremer, 2007;Wilson-Rich et al, 2009) and reducing the parasite load (Rosengaus et al, 1998;Hughes et al, 2002;Traniello et al, 2002).…”

Rapid anti-pathogen response in ant societies relies on high genetic diversity

“…This suggests that hygienic behaviour may be at least equally important in ants as in honeybees. The ants in our experiment excluded larvae from the brood chamber over the duration of a week (figure 3), which covers the time course of a typical Metarhizium infection (Ugelvig & Cremer 2007). The expression of this hygienic behaviour is a direct consequence of our treatment of larvae with fungal spores, as it did not occur in an additional control set-up where colonies had received only fungus-free control larvae (electronic supplementary material).…”

Opposing effects of allogrooming on disease transmission in ant societies

“…Twenty-four nests of L. neglectus were collected from four populations (Jena, Germany; Volterra, Italy; Bellaterra and Seva, Spain; six nests per population; as detailed in [25]). From each nest, we set up two subnests (in individual Petri dishes of Ø 9 cm and a 2 Â 1 cm brood chamber indentation in the plaster ground), each containing three larvae and six individually colour-marked workers to allow scoring of individual behaviour and survival throughout the experiment.…”

“…Changes in the behaviour of infectious individuals, or their group members, are likely to be reflected in their social interaction network (though experimental confirmation is scarce, see [15]), as some connections may be intensified and others eliminated, for example through caretaking [19 -21] or isolation [22][23][24][25] of diseased individuals. Such behavioural modulations, in addition to the direction in which behaviours are performed, can strongly impact the routes of disease spread in the group, by affecting the risk of pathogen exposure and transmission of the disease.…”