WHERE THE RED QUEEN SLEEPS: HOW LABOULBENIOMYCETES CAN ELUCIDATE THE EVOLUTION OF FUNGAL PATHOGENS

Spread primarily through sex, members of the microfungal class Laboulbeniomycetes are parasitic on arthropods, where they form tiny, three-dimensional thalli on the host exoskeleton. While the study of Laboulbeniomycetes has had a renaissance in the age of molecular methods, so too has the Red Queen Hypothesis, a coevolutionary theory aimed at characterizing how biotic interactions shape the evolutionary trajectory of “players” over time. While the central dogma of “laboulbeniology” is that labouls do not cause a fitness disadvantage to the host in the wild, here we report the first genome annotation data of a Laboulbeniomycete genome, indicating the possibility of past antagonistic relationships with host species. Some of the genes predicted are homologous with that of highly pathogenic entomopathogenic species, such as those within Cordyceps. To understand why these seemingly benign parasites possess genes associated with pathogenicity, we reviewed recent advances in molecular methods for detecting Red Queen associations, and propose a new model we call “Sleeping Red Queens”. Using Laboulbeniomycete evolutionary history, we predict that antagonists who have adapted to each other over time to a benign state can “re-awaken” or transition to a more antagonistic mode due to environmental changes. The “Sleeping Red Queen” model of Laboulbeniomycetes is supported by research on laboul ecology under artificial conditions. The purpose of this work is to review the history of Laboulbeniomycetes, examine recent advances in molecular methods through the Red Queen lens, report on our new molecular data, and discuss how our new findings can be used to apply Red Queen theory to Laboulbeniomycetes, while also hypothesizing what these future analyses could reveal. With promising advances in next-generation sequencing, we believe our Sleeping Red Queen model will be advantageous for interpretation of future genomic and bioinformatic data of Laboulbeniomycetes.