A prevalent hypothesis is that ‘strict genetic monogamy’ was a universal prerequisite for the origin of eusociality in Hymenoptera and Isoptera. Termites, however, do not fit easily into this scenario, particularly since the sister group of termites, the wood-feeding cockroach Cryptocercus, was recently found to be socially but not genetically monogamous. Termites likely evolved from large, physically robust, obligately subsocial cockroaches in an ecological setting where nitrogen conservation was prioritized. The shift to eusociality can originate from such a starting point via sequential delegation of brood care and defensive parental duties to young alloparents and soldiers, respectively, facilitated by reallocation of available nitrogenous resources. Each social transition was dependent on the prior state, and the final step, the shift from parental defense to origination of a soldier caste, coevolved with a decrease in parental body size and cuticular investment, thus freeing nitrogen for channeling into parental reproduction and cuticular armoring of soldiers. One consequence of this reallocation of critical reserves, however, was on the mating system: the now smaller, vulnerable alates were subjected to relentless predation pressure during dispersal and colony foundation. Swarming, tandem running, hasty mate choice, and immediate and permanent sequestration can be viewed as countermeasures to this selection pressure, enforcing genetic monogamy. We propose that any genetic monogamy detected in incipient colonies of extant termites may be a consequence, rather than a cause, of the initial transition to eusociality; if so, it is a derived mating system that may be a fitness cost in termite evolution.
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