Gut microbial pulse provides nutrition for parental provisioning in incipient termite colonies

Abstract

Success in aerial dispersal involves a trade-off between propagule size and dispersal ability, such that reducing weight may increase dispersal capability. Therefore, dispersing propagules such as plant seeds, fungal spores, and insect alates need to settle in new habitats with very limited resources. In termites, the time from alate dispersal to colony foundation is the most critical period in their life cycle, because a male and female pair establishes a new colony without help from others. In addition, termites depend largely on gut microbes for their nutrition. However, little is known about how termite founding pairs with limited resources establish new colonies and raise their first brood in association with their gut symbionts. Here, we provide an integrated analysis of the reproduction schedule, gut microbial fluctuations, and resource allocation of founding pairs in incipient colonies of the subterranean termite Reticulitermes speratus. There was a steep increase followed by a rapid decrease in the numbers of intestinal protozoa (hereafter, gut microbial pulse) at the time of larval hatching. Besides the monogamous pairs, same-sex (male-male and female-female) pairs also form tentative colonies in this species. Comparisons of changes in the amounts of protein and lipids in the different pair types revealed that the gut microbial pulse played an essential role in the parental feeding of the first-brood larvae. It was also observed that founders utilized stored protein and lipids for brood production. Our study highlights a significant role for intestinal symbionts during the early stage of the termite life cycle. Propagules of most animals and plants encounter resource limitations after dispersal. This is especially true for termite alates; monogamous pairs found new colonies without help from workers. How do they manage the limited resources, including their nutritional reserves and gut microbes, during colony foundation? To gain a better understanding, we analyzed time-series data of reproduction schedules, gut microbial fluctuations, and resource allocation patterns in the founders of incipient termite colonies. We identified a “gut microbial pulse”, i.e., a steep increase followed by a rapid decrease in the number of intestinal protozoa, that occurred at the time of larval hatching. Our data imply that resources derived from the pulse play an essential role in parental provisioning to larvae. This study highlights a novel strategy of termites to overcome resource-limited situations and successfully establish a new colony.