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)).