Reduced Environmental Microbial Diversity on the Cuticle and in the Galleries of a Subterranean Termite Compared to Surrounding Soil.

Termites are intimately tied to the microbial world, as they utilize their gut microbiome for the conversion of plant cellulose into necessary nutrients. Subterranean termites must also protect themselves from the vast diversity of harmful microbes found in soil. However, not all soil microbes are harmful, such as Streptomyces and methanotrophic bacteria that some species of termites harbor in complex nest structures made of fecal material. The eastern subterranean termite, Reticulitermes flavipes, has a simple nest structure consisting of fecal lined galleries. We tested the hypothesis that R. flavipes maintains a select microbial community in its nests to limit the penetration of harmful soilborne pathogens and favor the growth of beneficial microbes. Using Illumina sequencing, we characterized the bacterial and fungal communities in the surrounding soil, in the nest galleries, and on the cuticle of workers. We found that the galleries provide a more beneficial microbial community than the surrounding soil. Bacterial and fungal diversity was highest in the soil, lower in the galleries, and least on the cuticle. Bacterial communities clustered together according to the substrate from which they were sampled, but this clustering was less clear in fungal communities. Most of the identified bacterial and fungal taxa were unique to one substrate, but the soil and gallery communities had very similar phylum-level taxonomic profiles. Notably, the galleries of R. flavipes also harbored both the potentially beneficial Streptomyces and the methanotrophic Methylacidiphilales, indicating that these microbial associations in fecal material pre-date the emergence of complex fecal nest structures. Surprisingly, several pathogenic groups were relatively abundant in the galleries and on the cuticle, suggesting that pathogens may accumulate within termite nests over time while putatively remaining at enzootic level during the lifetime of the colony.

Natural variation in colony inbreeding does not influence susceptibility to a fungal pathogen in a termite.

Reduced genetic diversity through inbreeding can negatively affect pathogen resistance. This relationship becomes more complicated in social species, such as social insects, since the chance of disease transmission increases with the frequency of interactions among individuals. However, social insects may benefit from social immunity, whereby individual physiological defenses may be bolstered by collective-level immune responses, such as grooming or sharing of antimicrobial substance through trophallaxis. We set out to determine whether differences in genetic diversity between colonies of the subterranean termite, Reticulitermes flavipes, accounts for colony survival against pathogens. We sampled colonies throughout the United States (Texas, North Carolina, Maryland, and Massachusetts) and determined the level of inbreeding of each colony. To assess whether genetically diverse colonies were better able to survive exposure to diverse pathogens, we challenged groups of termite workers with two strains of a pathogenic fungus, one local strain present in the soil surrounding sampled colonies and another naïve strain, collected outside the range of this species. We found natural variation in the level of inbreeding between colonies, but this variation did not explain differences in susceptibility to either pathogen. Although the naïve strain was found to be more hazardous than the local strain, colony resistance was correlated between two strains, meaning that colonies had either relatively high or low susceptibility to both strains regardless of their inbreeding coefficient. Overall, our findings may reflect differential virulence between the strains, immune priming of the colonies via prior exposure to the local strain, or a coevolved resistance toward this strain. They also suggest that colony survival may rely more upon additional factors, such as different behavioral response thresholds or the influence of a specific genetic background, rather than the overall genetic diversity of the colony.

Increased genetic diversity from colony merging in termites does not improve survival against a fungal pathogen.

In some species of social insects the increased genetic diversity from having multiple breeders in a colony has been shown to improve pathogen resistance. Termite species typically found colonies from single mated pairs and therefore may lack the flexibility to buffer pathogen pressure with increased genetic diversity by varying the initial number of reproductives. However, they can later increase group diversity through colony merging, resulting in a genetically diverse, yet cohesive, workforce. In this study, we investigate whether the increased group diversity from colony fusion benefits social immunity in the subterranean termite Reticulitermes flavipes. We confirm previous findings that colonies of R. flavipes will readily merge and we show that workers will equally groom nestmates and non-nestmates after merging. Despite this, the survival of these merged colonies was not improved after exposure to a fungal pathogen, but instead leveled to that of the more susceptible or the more resistant colony. Our study brings little support to the hypothesis that colony fusion may improve immunity through an increase of genetic diversity in R. flavipes. Instead, we find that following exposure to a lethal pathogen, one colony is heavily influential to the entire group's survival after merging.