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Biology of UnderGround Symbioses (BUGS): studies of a subterranean ant-aphid-microbe cooperative network

Periodic Report Summary 1 - BUGS (Biology of UnderGround Symbioses (BUGS): studies of a subterranean ant-aphid-microbe cooperative network)

Mutualism, cooperative interactions between species, forms the basis of life as we know it. For example, ancient mutualism between early prokaryotes drove the evolution of eukaryotic cells, whereas present day mutualism promotes biodiversity and resilience of diverse ecosystems and governs our everyday interactions with our cattle, crops, and gut microbiota.
Given this ubiquity, it is surprising that the evolutionary biology of mutualism is still not well understood. In project BUGS we aim to understand mutualism evolution and stability by (1) mapping a community of North-American ant, aphid and bacterial mutualists, (2) unravelling the mechanisms that underlie these mutualisms, such as these insects’ behaviours and their nutritional relationships and (3) developing theoretical models which combine novel insights on mutualism evolution with existing network theory.
The interactions among subterranean ants and the aphids and mealybugs they farm in their nest are classic examples of mutualism. The aphids and mealybugs are considered ‘trophobionts’: The ants depend on them for food, because they ‘milk’ them for their excrement, the so-called honeydew. In turn, the trophobionts depend on the constant and safe environment provided by the ants. Traditionally, such ant-trophobiont interactions have been viewed as pairwise mutualism only, with a single ant species farming a single aphid species. In this project, we take the novel approach of considering these interactions in their wider ecological community. Not only do we extend our view towards considering multiple species of ants and trophobionts, we also take into account other organisms these insects interact with, such as their gut bacteria and, for the trophobionts, their host plants.
Here we report on the project progress over the last 24 months, with regard to each of BUGS’ three main objectives. First, in a recent literature review we demonstrated that viewing individual mutualistic (and even parasitic) interactions as subsets of larger ecological communities in which partners are represented by multiple species (Ivens et al. 2016) can indeed be a tool to improve our understanding of mutualism and parasitism evolution. We also developed a network analytic quick guide to ant-myrmecophile networks to facilitate similar studies in the future, for which we adopted metrics from existing network theory as indicators of co-evolution.
Second, we used these tools in field sampling studies on North American subterranean ant-trophobiont interactions. Indeed we found that pairwise interactions are embedded in multi-species communities, in this case including five species of ants farming nine species of aphids and five species of mealybugs (Fig. 1). Most of the aphid and mealybug species involved in this network are new to science and will be taxonomically described as part of this project. In addition, we showed that these communities also include potential ‘mutualism modulator’ organisms that may render mutualistic exchange of food or services worthwhile by modulating nutrient uptake and excretion. For example, our results show that both aphids and mealybugs indeed harbour highly specific gut bacteria, which presumably enable them to live off nutrient poor plant sap of specific host trees, which we also identified in our DNA barcoding experiments (Fig. 1). Similarly, ants harbour sugar-processing gut bacteria, which presumably enable them to live off the honeydew, the prime commodity of the mutualism (Fig. 1). The net benefits accrued by the ants in this mutualism may thus depend on their partner, as well as their partner’s partners.
Third, we have now developed laboratory set-ups that allow studies of the behavioural and biochemical mechanisms underlying the observed species interactions. Preliminary results show that the two main aphid species not only differ in their host tree and gut bacteria, but also produce honeydew with different amino acid content. Yet, in line with our field observations, the ants do not show a clear preference for one of these aphids in our preliminary choice experiments.
In sum, mutualism is ubiquitous in nature and plays important roles in fields as diverse as ecosystem dynamics under climate change, agriculture and medicine. Together our theoretical and empirical results indicate that a novel extended view of mutualistic communities may indeed hold the long-sought key to understanding the evolutionary origin and persistence of mutualism.

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