The Physiological Genomics of Diet Switching in Mammalian Herbivores

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At every meal, animals that feed on plants (herbivores) such as deer, cattle, and rabbits, face the possibility of being poisoned by naturally-occurring toxic chemicals in their food. Nevertheless, how herbivores process natural toxins remains poorly understood. For example, remarkably little is known about the specific genes that control an animal's ability to process potentially toxic compounds in plants. To address these fundamental problems, this research will focus on a dramatic dietary change: woodrats normally eat juniper and cactus, but several populations in the American southwest have switched to a diet of creosote bush. Creosote bush produces natural toxins that radically differ from juniper and cactus, and therefore the specialized woodrat populations must detoxify their diets differently than the juniper and cactus-eaters. The goal of this project is to identify DNA-level changes that are associated with woodrats' ability to feed on a toxic diet of creosote bush. This project will develop new genomic tools that will be useful to the broader scientific community. A better understanding of how animals process toxins can also impact decisions about pharmaceutical development for humans and other animals, and influence feeding options to improve production of free-ranging domestic herbivores like cattle. Results of this work will be communicated to the public through an interactive display about the ecology of woodrats at the Utah Museum of Natural History. Despite decades of pharmacological research on model species and humans, the mechanisms used by mammalian herbivores to metabolize plant secondary compounds and the genomic basis underlying adaptation to new diets remain poorly understood. This research will investigate the evolution of dietary adaptation and specialization in mammalian herbivores by capitalizing on a dramatic diet change event: the replacement of juniper (Juniperus spp.) and cactus (Opuntia spp.) with creosote bush (Larrea tridentata) in the diets of herbivorous woodrats. The project has three goals: 1) Identify genomic changes associated with a radical dietary shift in Neotoma lepida. 2) Test for the repeated involvement of similar genetic pathways for specialization on creosote diets in N. bryanti. 3) Characterize the transcriptomic response of parental and hybrid populations of N. lepida and N. bryanti to a creosote diet. The proposed work leverages modern evolutionary genomic approaches to address a long-standing question in physiological ecology: which mechanisms are important in the processing of toxic diets? The project will lead to a deeper understanding of the responses of organisms to changes in the environment, including fundamental information at the genomic level about how mammalian herbivores adapt to dietary toxins. The project specifically tests whether the same genomic regions are under selection in two species that independently evolved the ability to specialize on creosote diets. An interactive display about the ecology of woodrats and their importance to society will be developed in collaboration with the Utah Museum of Natural History. Genomic tools will be developed that will be useful to the broader scientific community. In addition, the PIs will mentor students (high school through graduate) and postdocs in physiological genomics research on non-model species.