Collaborative Research: Testing the spatio-temporal repeatability of (co)evolution in Tasmanian devils and their transmissible cancer

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Emerging infectious diseases (EIDs) are a leading global challenge in the 21st century. In addition to their great concern for human health, EIDs are now a leading cause of biodiversity declines. A well-known example is a lethal, transmissible cancer that threatens Tasmanian devils with extinction. Typical of infectious diseases, the host evolves to resist the pathogen. In turn, the pathogen is pressured to evolve to overcome new host defenses. Indeed, long-term data show that devils and their tumors are evolving in response to one another, but the genetic pathways by which they respond remain poorly described. The goal of this research is to determine whether the genetic pathways underlying adaptive changes in devils, such as increased survival once infected, are similar or different among devil populations infected for different lengths of time. Similarly, the tumor has adapted, and tests of repeatability of tumor genetic evolution in time and space will also be conducted. The implications of this work are far reaching. If, for example, genetic pathways are similar among populations, then conservation and treatment options can be generalized. Conversely, if genetic pathways are different, treatment options may need to be tailored, with different treatments for different populations. Regardless, the work will lead to improved conservation and management of the iconic Tasmanian devil. Additionally, the Tasmanian devil cancer evolves quite similarly to human cancer, providing a unique opportunity to track tumor evolution in a natural population.One of the biggest challenges in the life sciences today is unraveling the genotype-phenotype relationship. Rapid global change necessitates assessments of species’ capacity to adapt and whether adaptive evolution is repeatable to guide appropriate management strategies. Owing to the polygenic nature of most phenotypic traits, this is a formidable task. However, virulent EIDs can levy intense selection pressure on multiple host populations as they spread, offering a way to test patterns of repeatability in host-pathogen evolution. Tasmanian devils and their lethal transmissible cancer are a model system for such tests. The east-to-west progression of disease emergence across Tasmania has created a natural experiment. Different devil populations have been infected for different numbers of generations and are at different evolutionary stages of disease progression. Thousands of phenotypic measurements of diseased and healthy devils, along with extensive tissue sampling of devil-tumor pairs, will enable robust tests of molecular signatures of (co)evolution. Genome scans and evolutionary concordance analyses will be used test whether the genomic architecture underlying adaptive phenotypic traits in devils and tumors are repeatable in time (i.e., across different stages of disease emergence) and space (i.e., across different populations). If concordant, the underlying mechanism (e.g., soft selective sweeps, hard sweeps or gene flow) will be tested.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.