Nonrelatives inherit colony resources in a primitive termite

Abstract

The evolution of eusociality, especially how selection would favor sterility or subfertility of most individuals within a highly social colony, is an unresolved paradox. Eusociality evolved independently in diverse taxa, including insects (all ants and termites; some bees, wasps, thrips, and beetles), snapping shrimp, and naked mole rats. Termites have received comparatively less focus than the haplodiploid Hymenoptera (ants, bees, and wasps); however, they are the only diploid group with highly complex colonies and an extraordinary diversity of castes. In this study we staged encounters between unrelated colonies of primitive dampwood termites, Zootermopsis nevadensis, mimicking natural meetings that occur under bark. During encounters, kings and/or queens were killed and surviving members merged into one colony. After encounters, members of both unrelated colonies cooperated as a single social unit. We determined the colony of origin of replacement reproductives that emerged after death of kings and/or queens. Here, we document that replacement reproductives developed from workers in either or both original colonies, inherited the merged resources of the colony, and sometimes interbred. Because this species shares many characteristics with ancestral termites, these findings demonstrate how ecological factors could have promoted the evolution of eusociality by accelerating and enhancing direct fitness opportunities of helper offspring, rendering relatedness favoring kin selection less critical.

Fig. 1.

Colony of origin, as determined by genetic markers, of newly differentiated replacement reproductives after interactions (n = 25) between pairs of unrelated colonies. None, replacement reproductives did not differentiate after the colony interaction; One, replacement reproductives differentiated from termites belonging to only one of the two interacting colonies; and Both, replacement reproductives differentiated from both interacting colonies. Interactions that resulted in a surviving king and queen (“intact royal pair”) from one of the preinteraction colonies (n = 14) are shown in black; interactions resulting in only a single surviving king or queen from either colony (n = 11), including two interactions resulting in a surviving king from one colony and queen from the other, are shown in white.

Fig. 2.

Effect of colony of origin of kings and queens that survive interactions on mean number and colony of origin of replacement reproductives. Data are represented as mean ± SEM. Interactions resulted in a surviving king and queen from the same colony (K & Q Same), only one surviving king or one surviving queen (K or Q Only), or only one surviving king from one colony and one surviving queen from the other colony (K & Q Different). In the K & Q Same and K or Q Only, black bars indicate replacement reproductives differentiating from the surviving king and/or queen's colony (surviving primaries; Table 1); white bars indicate replacement reproductives differentiating from the colony whose king and queen were killed (deposed primaries; Table 1). In K & Q Different, crosshatched bar indicates replacement reproductives differentiating from the surviving king's colony, and stippled bar indicates replacement reproductives differentiating from the surviving queen's colony.