A double-edged sword? The cost of proctodeal trophallaxis in termites

Abstract

The evolution of insect sociality has likely been shaped by pathogenic pressures. Previous research has indicated that social interactions among nestmates can ameliorate risks of infection. We hypothesized that proctodeal trophallaxis (anus-to-mouth exchanges of proctodeal fluid) and coprophagy, both common phenomena across termites, result in the passive transfer of immune elicitors, antimicrobial compounds, and/or immune proteins that could render the recipient of these fluids less susceptible to disease. If true, this would represent a prime example of social immunization. Our results show that in Zootermopsis angusticollis, recipients of proctodeal fluid collected from naive, control, and vaccinated donors have similar susceptibility to a subsequent Serratia marcescens challenge. However, nestmates feeding on proctodeal fluid from donors injected with sub-lethal dosages of live bacteria were significantly more susceptible to a subsequent challenge. These data indicate unanticipated costs associated with proctodeal trophallaxis when exploiting infectious environments. That termites frequently engage in these exchanges in spite of the heightened survival costs reveals possible evolutionary trade-offs between the nutritional benefits accrued through these exchanges and the risks of disease transmission. This work represents a first attempt to identify the role of proctodeal trophallaxis within a socio-immunological context.