One of the major advances in evolutionary biology in recent years is the recognition that the origins of the incredible diversity of life on earth lie largely in the interactions organisms have with each other. Yet, we know remarkably little about what might be described as "the ecology of diversification". This project seeks to understand the process of adaptive diversification in a complex ecological system consisting of a fly, its host-plant, a symbiotic fungus, and its parasitic enemies. We will use DNA data along with behavioral assays and ecological experiments to determine the processes that are involved in this incipient adaptive radiation.
This work bridges a crucial divide between evolutionary studies of adaptive diversification and ecological interactions, in particular by providing insight into the determinants of insect specialization, the influence of enemies on insect populations, and role of symbiotic interactions in diversification. Importantly, the focal species are related to important agricultural pests and our research into their interactions and diversification will benefit both applied and basic scientific fields. This study will foster collaboration between laboratories at Wright State and Vanderbilt Universities. It will train four graduate students, at least four undergraduates, and provide additional students with training in scientific research.
Midges are small and very specialized flies, many of which attack cereal crop plants in the United States. The Hessian fly, for example, is one of the most important insect pests of wheat, barley and rye. Since the 1940's, there have been active efforts to breed crop plants that are resistant to midges such as the Hessian fly. Midges are an extremely diverse group, with over 5000 described species. Like many insects that attack on plants, midges are specialists, such that only certain midge species attack certain plant species. This sets up a process of co-evolution between midges and plants. The diversity of midges is noteworthy because midges consistently develop the ability to overcome resistant crops. What mechanisms underlie the pattern of specialization, co-evolution and diversification in midges? Since 2006, we have been studying a midge known as Asteromyia carbonifera, which attacks goldenrod species. An often overlooked fact is that many midges use fungi as partners when they attack plants. Moreover, many midges are also attacked by specialists predatory wasps known as parasitoids. Our motivation for this work has been to add this complexity to studies of interactions like that which happens between midges and plants. We want to understand the roles of fungi and predators in the specialization/co-evolution scenario for midge diversification outlined above. Not only would this work enhance our understanding of the factors that favor or disfavor specialization in midges (and thus help us understand such interactions exemplified by the Hessian fly and wheat), but it would add a new system in which to study the complex interactions between microbes, plants, herbivores and predators in terrestrial environments. We first showed that A. carbonifera is hyperdiverse, composed of many different lineages on its host plant. We also discovered a similar pattern at a larger scale - e.g., the entire genus Asteromyia is composed of many cryptic lineages - practically an explosion of new genetic potential. Where does this cryptic diversity come from? What is the cause? We predicted that Asteromyia is co-evolving with fungi, and that it is able to colonize and attack novel and presumably "resistant" plant species with help from it's fungal partner. Essentially, the midges use fungi as a tool to evade plant defenses. To our surprise, we found that the species we studied all utilize exactly the same fungus, no matter what the host plant is. But that doesn't prevent the midge from being dependent on the fungus. Rather, we showed that the flies cannot survive without it. Finally, we have shown that the likely cause of this explosive diversification is that midges are constantly under attack from predatory wasps. They probably move between different host plant species- carrying their fungal partners with them - in an effort to escape attack by these predators, which tend to search for their prey on their "ancestral" host. The hide and seek that midges play with wasps sets up a scenario of recurrent isolation and diversification by midges. Their fungal partner - a generalist plant pathogen and important cause of economic losses of fruits and crops in its own right - facilitates these moves to new host plants by providing the nutrition midges need as they adapt to their new circumstances. Eventually, the midges are discovered by the predators, and the cycle continues anew. We described this process in a conceptual publication that draws all of the various strings together. The importance of this work can be seen in a recent publication on the role of bacteria in facilitating the interaction between the Hessian fly and wheat (Bansal et al. 2011). Microbes are overlooked agents in the interactions between plants and insect pests. Understanding their role in facilitating or inhibiting the development of diversity may be key to a broader understanding of how plant-associated insects adapt to changing traits and environments, including those we breed into our plants to enhance agricultural productivity and, ultimately, food security.
