Recombination of standing variation in a multi-hybrid swarm drove adaptive radiation in a fungal pathogen and gave rise to two pandemic plant diseases

Abstract

Adaptive radiations fuel speciation and are characterized by rapid genetic diversification and expansion into new ecological niches. Historically, these processes were believed to be driven by selection on novel mutations but genomic analyses now indicate that standing variation and gene flow often have prominent roles. How "old" variation is combined, however, and its resulting genetic architecture within newly-adapted populations is not well understood. We reconstructed a recent radiation in the fungus, Pyricularia oryzae, that spawned a population pathogenic to eleven grass genera, and caused two new plant diseases: wheat blast - already a serious threat to global agriculture - and gray leaf spot of ryegrasses. We show that the new population evolved in a multi-hybrid swarm using only the standing variation that was present in seven individuals from five distinct, host-specialized lineages. Sexual and parasexual recombination within the swarm reassorted key host-specificity factors and generated more diversity in possibly just a few weeks than existing lineages had accumulated over hundreds to thousands of years. We suggest that the process was initiated by sexual opportunity arising when a fertile fungal strain was imported into Brazil on Urochloa introduced as forage for beef production; and we further contend that the host range expansion was largely fortuitous, with host selection playing little, if any, role in driving the process. Finally, we believe that our findings point to an overlooked role for happenstance in creating situations that allow organisms to skirt rules that would normally hold evolution in check. Commercial Endorsement DisclaimerMention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. Equal Opportunity/Non-Discrimination StatementUSDA is an equal opportunity provider and employer.