|Russell, Jacob -|
|Moreau, Corrie -|
|Kautz, Stephanie -|
|Sullam, Karen -|
|Hu, Yi -|
|Basinger, U. -|
|Buck, N. -|
|Wheeler, D. -|
Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: December 17, 2011
Publication Date: April 15, 2012
Repository URL: http://www.handle.nal.usda.gov/10113/54238
Citation: Anderson, K.E., Russell, J.A., Moreau, C.S., Kautz, S., Sullam, K.E., Hu, Y., Basinger, U., Mott, B.M., Buck, N., Wheeler, D. 2012. Highly similar microbial communities are shared among related and trophically similar ant species. Molecular Ecology. 21: 2282-2296. Interpretive Summary: Although ants dominate many ecosystems across the globe, their nutritional interactions are poorly understood. Many tree-dwelling and cavity-nesting ant species in the Cephalotini group are classified as herbivores because they feed primarily on sugar rich plant secretions, substances abundant in carbohydrates and deficient in nitrogen. While the vast majority of Cephalotini occur in the tropical regions of North and South America, Cephalotes rohweri occurs in the Southwestern United States, primarily in the Sonoran desert where it nests in insect carved cavities of Palo Verde trees. We used informative gene sequences to investigate the gut bacteria of C. rohweri and infer the evolutionary history of bacterium-host interactions within the group Cephalotini. Based on bacterial sequences from the guts of queens, workers, and males, we detected five major groups of ant-associated bacteria. According to comparisons with related free living bacteria and bacteria occurring in the guts of closely related ants, our results suggest that some of these bacterial groups have been associated exclusively with Cephalotini for over 60 million years. New-born ants acquire the bacteria as they share food with older colony members. The bacterial community is composed of several different groups related to putative nitrogen processing bacteria. Unlike tropical relatives, C. rohweri has no access to sugar rich plant secretions, suggesting that pollen provides the bulk of its nutritional requirements. A strict diet of pollen and limited access to water has likely shaped many aspects of ant colony growth and survival, as well as the composition and evolution of the ant-associated bacteria.
Technical Abstract: Ants dominate many terrestrial ecosystems, yet we know little about their nutritional physiology and ecology. While traditionally viewed as predators and scavengers, recent isotopic studies revealed that many dominant ant species are functional herbivores. As with other insects with nitrogen-poor diets, it is hypothesized that these ants rely on symbiotic bacteria for nutritional supplementation. In this study, we used cloning and 16S sequencing to further characterize the bacterial flora of several herbivorous ants, while also examining the beta diversity of bacterial communities within and between ant species from different trophic levels. Through estimating phylogenetic overlap between these communities, we tested the hypothesis that ecologically or phylogenetically similar groups of ants harbor similar microbial flora. Our findings reveal: (i) clear differences in bacterial communities harbored by predatory and herbivorous ants; (ii) notable similarities among communities from distantly related herbivorous ants and (iii) similar communities shared by different predatory army ant species. Focusing on one herbivorous ant tribe, the Cephalotini, we detected five major bacterial taxa that likely represent the core microbiota. Metabolic functions of bacterial relatives suggest that these microbes may play roles in fixing, recycling, or upgrading nitrogen. Overall, our findings reveal that similar microbial communities are harbored by ants from similar trophic niches and, to a greater extent, by related ants from the same colonies, species, genera, and tribes. These trends hint at coevolved histories between ants and microbes, suggesting new possibilities for roles of bacteria in the evolution of both herbivores and carnivores from the ant family Formicidae.