Feces production as a form of social immunity in an insect with facultative maternal care

Janina MC Diehl, Maximilian Körner, Michael Pietsch, Joël Meunier

Social animals have the unique capability of mounting social defenses against pathogens. Over the last decades, social immunity has been extensively studied in species with obligatory and permanent forms of social life. However, its occurrence in less derived social systems and thus its role in the early evolution of group-living remains unclear. Here, we investigated whether lining nests with feces is a form of social immunity against microbial growth in the European earwig Forficula auricularia, an insect with temporary family life and facultative maternal care. Using a total of 415 inhibition zone assays, we showed that earwig feces inhibit the growth of two GRAM+ bacteria, two fungi, but not of a GRAM- bacteria. These inhibitions did not result from the consumed food or the nesting environment. We then demonstrated that the antimicrobial activity against fungus was higher in offspring than maternal feces, but that this difference was absent against bacteria. Finally, we showed that family interactions inhibited the antibacterial activity of maternal feces against one of the two GRAM+ bacteria, whereas it had no effect on the one of nymphal feces. By contrast, antifungal activities of the feces were independent of mother-offspring interactions. These results demonstrate that social immunity occurs in a species with simple and facultative social life, and thus shed light on the general importance of this process in the evolution of group-living. These results also emphasize that defecation can be under selection for other life-history traits than simple waste disposal.