Rapid Evolution of Introduced Plant Pathogens via Interspecific Hybridization

Abstract

P lant disease epidemics resulting from introduction of exotic fungal pathogens are a well-known phenom- enon. Limited resistance in the host and excessive aggres- siveness in the pathogen (reflecting their lack of prior co- evolution) can result in an explosive outbreak of disease. Introduction events also present a window of evolutionary op- portunity for the pathogen. In its endemic location, a plant pathogen tends to be subject to routine selection constraints, favoring maintenance of a relatively stable, if fluctuating, population structure over time. When introduced into a new environment, it will often be subject to novel or episodic se- lection, reflecting sudden exposure to new biotic and abiotic influences, such as a new host population, new vectors, new competitors, or a different climate. These influences provide the potential for rapid evolution (Brasier 1995). Falling within the category of episodic selection is the sud- den contact that can occur between closely related but pre- viously geographically isolated pathogens as a result of in- troductions. Theoretically, this process presents an opportunity for rapid emergence of new or modified pathogens via interspecific gene flow (Brasier 1995). Until recently, this phenomenon has been little studied. Now Dutch elm disease, a major ecological accident of the 20th century (Heybroek 1993), is providing remarkable insights into rapid evolution of a plant pathogen outside its en- demic environment. This article describes the migratory events and unusual genetic events that have occurred in this fungus and other new examples of rapid pathogen evo- lution via interspecific gene flow, and discusses some of the wider environmental, evolutionary, and quarantine impli- cations. The Dutch elm disease pathogens Elm trees (Ulmus) are confined mainly to the temperate re- gions of the Northern Hemisphere. China and Japan have a total of about 25 elm species, while Eurasia, North Amer- ica, and the Himalayas each have about five or six species. Dutch elm disease (so called because the early seminal re- search was in The Netherlands (Holmes and Heybroek 1990)) is the elm's main enemy. It is a wilt disease, caused by ascomycete fungi of the genus Ophiostoma, that spreads within the tree's vascular system. The pathogens are trans- mitted from diseased to healthy elms by elm bark beetles of the genus Scolytus (Fransen 1935, Webber and Brasier 1984).