Macro-symbiosis triggered by a defence-reproduction tradeoff in a social insect

Symbiotic associations underlie hierarchical evolutionary transitions being crucial to understanding biological complexity. But which proximate triggers promote the first successful contact between guests and their hosts? We tackle this problem, studying the macro-symbiotic model system comprised by two termite species (Blattodea: Isoptera) cohabiting termitaria as a host and its obligatory inquiline. We tested the hypothesis that ergonomic adjustments in resource allocation force termite colonies to trade current defence for future reproduction, thence easing inquiline infiltration. To do so, we combined mathematical modelling and field bioassays. Initially, we created a dynamic model to inspect colony’s resource allocation as a result of the competition between a physical “defence specialist” caste (soldiers) competing for resources with a reproductive caste (alates) and with a physical resource-gatherer specialist caste (workers). This model differs from Oster & Wilson’s “bang–bang” model by the explicit inclusion of solders as a physical defence specialist. Then, we sought empirical support for the end results of our model (i) censusing the population and (ii) measuring the patrolling efforts by soldiers, in 154 mature field termite colonies along a year-long reproductive season. Finally, we verified in the field whether reproducing termite colonies would be more likely to house inquilines than colonies still not at reproductive stage. Modelling and field results matched closely, supporting our hypothesis. Inquiline termites (Inquilinitermes microcerus) sneaked into nests of host termites (Constrictotermes cyphergaster) as these latter colonies undergone a defence-reproduction tradeoff. As the host colony entered reproduction, their soldier numbers and patrolling waned, enhancing the proneness of infiltration by obligatory inquilines. Our results indicate that defence-reproduction tradeoffs, more than a strategy to optimise resource use, can be important initiators of symbioses by loosening self/non-self discrimination and enhancing tolerance. We speculate that, if changes in the internal stasis of an organism or superorganism can enhance tolerance, it could be invoked to explain why symbioses are frequently enhanced by stress and disturbance.