In nature, the hidden things often make the most difference. For example, in the rainforests of South America, fungus-gardening ants consume more leafy vegetation than any other herbivore. In the forest canopy, other ants may compose more than 50% of all insect biomass. But how do these tiny herbivores affect the forest ecosystem? The answer may lie with an even more hidden player: bacteria. Like coral reefs, cows, and even humans, many insects rely on symbiotic microbes to augment their diets. There are hints that bacteria may play an especially important role for ?herbivorous? ants, or those ants whose diet consists primarily of nectar, extra-floral nectar, and other plant-derived resources. However, little is known about the evolution, ecology, and function of the microbial partners of herbivorous ants. This study aims to uncover some of the mysteries surrounding ant/bacteria symbioses using the canopy-dwelling tropical ant genus Cephalotes as a model system. Cephalotes are among the most herbivorous of known ants, and have long been known to host an unusually dense population of bacteria, or microbiome, in their guts. Using next-generation DNA sequencing technology, this study will address the following questions: Have Cephalotes gut bacteria co-evolved with their hosts? How does the Cephalotes gut microbiome change among host species, nests, locations, and across host development? What can the genomes of Cephalotes gut bacteria indicate about their function?

Broader Impacts: The answers to these questions will clarify the role played by bacterial symbionts in one of the most important and least understood elements of tropical rainforest ecology. Additionally, data and techniques from this study will help to disentangle the evolutionary and ecological dynamics operating within symbiotic gut communities themselves. These communities have both direct (via diseases like Inflammatory Bowel Disease) and indirect (via association with agricultural pests such as locusts and aphids) impacts on human society, and yet they remain poorly understood. This research will provide training opportunities for students in cutting-edge areas of sequencing and data analysis, and the results will be communicated to the public via ongoing museum- and K12-based outreach activities.

Project Report

We think we know our history. It’s written in our DNA. As humans, we began in Africa, our descent from ancient vertebrates recorded in an evolutionary tree we can trace all the way back to fish, and beyond. But we’re more than just vertebrates: each of us also carries around kilograms of microbes, trillions of cells in our gut, with enormous implications for our health. What is their history? How many have followed us out of Africa, followed our ancestors out of the sea? The problem is extraordinarily complex, but of potentially great importance. We think that microbes which coexist with the same hosts for millions of years are more likely to cooperate, providing benefits without turning parasitic. How do we disentangle these diverse histories? In this research project, we took advantage of a unique natural system to develop tools to explore the shared evolutionary history of hosts and their diverse microbial systems. Turtle ants, genus Cephalotes, host a dense community of microbes in their guts, much like we do. But unlike our gut microbes, the community in Cephalotes is relatively simple, making such broad exploration possible. We developed two different computational approaches to look at the impact of shared evolutionary history on gut microbiomes: one focuses on patterns in whole microbial communities, and one that examines the evolutionary trees of each microbial lineage in turn. Applying these tools to Cephalotes, we find a broad spectrum of fidelity with the host: some microbes are tightly coupled over millions of years, and other seem to jump around. What about the prediction that closely-linked microbes are more likely to be cooperators? That will be a primary focus of research in the Cephalotes system going forward. In the meantime, the tools we developed are being made publicly available so that other researchers can look at similar trends in the organisms they study. We also discovered that Cephalotes may be more unusual than we’d imagined -- not just because of which microbes they host in their gut, but because of how many. Looking at Cephalotes and a few other ant species we had around the lab, we were struck by how few bacterial cells could be seen in the guts of the other ants. Extending this survey to over a hundred ant species found in a single patch of rainforest, it became clear that most ants maintain almost undetectable numbers of bacteria in their guts. Correlations between bacterial abundance and host ant ecology suggest that these associations have played an important role in allowing ants to become the dominant members of tropical ecosystems that they are. Along the way, this grant has allowed us to mentor several undergraduate and high school students. These students have made real contributions to the science, with two presenting their research at a major scientific meeting.

National Science Foundation (NSF)
Division of Environmental Biology (DEB)
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Alan James Tessier
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Harvard University
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