Repeated global migrations on different plant hosts by the tropical pathogen Phytophthora palmivora

Abstract

The genetic structure and diversity of plant pathogen populations are the outcomes of evolutionary interactions with hosts and local environments, and migration at different scales, including human-enabled long-distance dispersal events. As a result, patterns of genetic variation in present populations may elucidate the history of pathogens. Phytophthora palmivora is a devastating oomycete that causes disease in a broad range of plant hosts in the tropics and subtropics worldwide. The center of diversity of P. palmivora is in Southeast Asia, but it is a destructive pathogen of hosts native to South America. Our objective was to use multilocus sequence analysis to resolve the origin and historical migration pathways of P. palmivora. Our analysis supports Southeast Asia as a center of diversity of P. palmivora and indicates that a single colonization event was responsible for the global pandemic of black pod disease of cacao. Analysis using the structured coalescent indicated that P. palmivora emerged on cacao and that cacao has been the major source of migrants to populations in Asia, Africa, and Pacific Islands. To explain these results, we hypothesize widespread introgression between the pandemic cacao lineage and populations native to Asia and the Pacific Islands. The complex evolutionary history of P. palmivora is a consequence of geographic isolation followed by long-distance movement and host jumps that allowed global expansion with cacao, coconut and other hosts.