Opportunity to Usurp Reproductive Power of Royal Throne Keeps Worker Termites Home

In research published in the Proceedings of the National Academy of Sciences Early Edition (October 5, 2009), Professor Barbara L. Thorne and colleagues reveal how unrelated termites originating from two different families or colonies join forces after the death of their kings and queens, and then cooperate in a larger, stronger group in which new “reproductives” can emerge from the worker ranks of either or both original colonies, thus enabling both lineages to thrive.

“When young dampwood termite colonies nest in the same piece of wood, their interactions result in assassination and cannibalism of one or both sets of queens and kings followed by fusion of the two families into a single colony,” said Thorne.

These findings help unravel an evolutionary mystery that Charles Darwin himself recognized as a special problem to reconcile with fundamental concepts of natural selection. The majority of individuals in a termite (or ant, bee, or wasp) colony are “workers” who stay to help out in their parents’ colony their entire lives, but never reproduce. Why would natural selection (“survival of the fittest”) favor traits that reduce reproductive success? This research shows that unrelated families both benefit following colony encounters and that competition among families living within limited food and nesting resources played a prominent role in the evolution of the complex social structure in termites.

For this study, Thorne and her colleagues Philip Johns and Ken Howard, now at Bard College, and Nancy Breisch and Anahi Rivera at the University of Maryland, staged meetings between unrelated dampwood termite colonies (from the Termopsidae family) that mimicked natural meetings that occur under wood bark, and analyzed genetic markers.

These termites are members of the genus Zootermopsis, and share social, developmental, and habitat characteristics with ancient ancestors. They thus serve as a model system to draw inferences regarding how highly social behavior evolved in these insects 140 million years ago.

Termite colonies begin as a nuclear family: the queen, the king, and their offspring (workers and soldiers). Although most termite workers never reproduce, if either or both of the original parents die, one or more of their offspring can become a ‘replacement reproductive’ to carry on (usually incestuous) reproduction and growth of the colony. When young dampwood termite colonies nest in the same piece of wood, the neighbors meet and the two families merge into a single colony after a violent process during which one or both sets of queens and kings may be killed and eaten.

After the carnage, worker offspring may usurp the throne and the reproductive power and resources that go with it. Despite the original colonies being unrelated, individuals within the merged colony cooperate. This cooperation is best explained by the key finding of this paper, revealed through analysis of genetic markers: offspring in both original colonies have opportunities to develop into new (replacement) reproductives within the larger, merged colony, and termites from the two families may even interbreed. Thus both lineages (i.e. both original, unrelated families or young colonies) can ‘win’ and propagate in this dynamic.

Data in this PNAS paper add genetic evidence to support a theory that Thorne and her lab first proposed in a 2003 PNAS paper– the theory of “Accelerated Inheritance” to explain the evolution of highly social behavior and nonreproductive castes in termites.

The paper “Nonrelatives inherit colony resources in a primitive termite” was written by Philip M. Johns, Kenneth J. Howard, Nancy L. Breisch, Anahi Rivera, and Barbara L. Thorne. This research was supported by a National Science Foundation grant to Barbara L. Thorne, Department of Entomology, College of Chemical & Life Sciences, University of Maryland, College Park, Maryland.