The lose-to-win strategy of the weak: intraspecific parasitism via egg abduction in a termite

Abstract

Predation by larger conspecifics poses a major threat to small juveniles in many animal species. However, in social insects, raids perpetrated by large colonies may provide smaller colonies with opportunities for parasitization. Herein, in the termite Reticulitermes speratus , we demonstrate that small incipient colonies parasitize large mature colonies through egg abduction when attacked by raiding conspecifics. We observed that the eggs of incipient colonies were brought into raiding colonies while their parents were killed during the attack. In this species, unmated females found new colonies with female–female (FF) cooperation, in addition to the typical monogamous colony foundation. Interestingly, the abducted eggs of FF pairs developed into nymphs (reproductive caste) in the raiding colonies, whereas the eggs of male–female (MF) pairs developed into workers (non-reproductive caste). Parthenogenetic eggs are known to be developmentally predisposed to becoming female reproductives owing to genomic imprinting in termites. This study demonstrates that the plundering of small colonies by larger conspecific colonies not only results in the extinction of the weaker colonies, but also serves as a strategy that incipient colonies use to obtain the reproductive position in large colonies by stealth. The results elucidate the diversity and complexity of inter-colonial interactions in social insects.

Inter-clonal competition over queen succession imposes a cost of parthenogenesis on termite colonies

“…Because parthenogenetic offspring are all females and have an epigenetic predisposition to develop into the nymph pathway [20,21], their caste fate is either to become neotenic secondary queens or to become female alates. Our earlier studies of genotyping queens in field mature colonies identified all successful primary queens as being derived from sexually produced alates [14,18,20], which has concealed the existence of parthenogenetic alates.…”

“…The parthenogenetically produced daughters carrying only maternal chromosomes almost exclusively develop along the nymph pathway, i.e. the reproductive pathway, due to genomic imprinting [20,21]. Therefore, there should be a severe conflict between secondary queen clones over the production of subsequent secondary queens, a conflict we have termed 'cloneflict'.…”

Ancestral sex-role plasticity facilitates the evolution of same-sex sexual behavior

“…Nest establishment by a single individual is less successful (22) or impossible (21) because termites cannot self-groom their entire body and require a grooming partner (23). After nest establishment, female-female pairs can reproduce via parthenogenesis (23,24) (SI Appendix, Text S6), and male-male pairs can invade neighboring incipient colonies to gain reproductive opportunities (21). Same-sex pairs establish nests as rapidly as heterosexual pairs (21), and nests with same-sex pairs have been observed in (semi)natural conditions (25,26).…”