Inbreeding is only a risk for small incipient colonies
Inbreeding acts differently upon colonies depending on their stage of development, and may therefore not play an important role in partner choice. Inbreeding depression only occurs in small colonies. In our study founding couples experienced drastic mortality in the first weeks, even though the risks associated with nuptial flights mentioned above were limited under laboratory conditions. The presence of strong selection against inbreeding during pairing is also discredited by the common occurrence of inbreeding through neotenic reproduction observed in mature colonies. Remarkably, while inbreeding is prevented in vertebrate social species via parental inhibition of sexual activity by the parent of the opposing sex, the opposite is found in termites. The removal of one of the parents triggers the development of neotenics of the opposite sex, therefore resulting in inbreeding to maintain the life of the colony. Neotenic inbreeding may be tolerated in populous colonies, when social immunity becomes more important than individual immunity in managing pathogen pressure (Cremer et al. 2007; Cotter & Kilner 2010; Cremer et al. 2018; Van Meyel et al. 2018; Liu et al. 2019). Social immunity in termites strongly relies on allogrooming, cannibalism, burial behavior and self-exclusion of infected individuals (Chouvenc & Su 2012; Davis et al. 2018). Although these behaviors may be adequate for mature colonies, they may be costly in incipient colonies, and cannot be applied to reproductive individuals. These behaviors may therefore be more prevalent and efficient in large groups (Rosengaus & Traniello 2001), accounting for the higher influence of individual immunity (related to individual genetic diversity as determined by inbreeding) in small incipient colonies. Interestingly, individual immunity is negatively correlated with colony-level immune behaviors in an ant, suggesting a trade-off between individual and social immunity in regulating overall parasite protection in this species (Cassidy et al. 2021). Similarly, the development of social immunity in shaping disease resistance in termites (also in social Hymenoptera (López-Uribe et al. 2016)) seems to occur at the expense of individual immunity, as the evolution of sociality is associated with a reduction in their immune gene repertoire (Viljakainen et al. 2009; Meusemann et al. 2020; Heet al. 2021) (but see (Barribeau et al. 2015; Otaniet al. 2016)).