Comparing patterns and scales of plant virus phylogeography: Rice yellow mottle virus in Madagascar and in continental Africa

Rice yellow mottle virus (RYMV) in Madagascar Island provides an opportunity to study the spread of a plant virus disease after a relatively recent introduction in a large and isolated country with a heterogeneous host landscape ecology. Here, we take advantage of field survey data on the occurrence of RYMV disease throughout Madagascar dating back to the 1970s, and of virus genetic data from ninety-four isolates collected since 1989 in most regions of the country to reconstruct the epidemic history. We find that the Malagasy isolates belong to a unique recombinant strain that most likely entered Madagascar through a long-distance introduction from the most eastern part of mainland Africa. We infer the spread of RYMV as a continuous process using a Bayesian statistical framework. In order to calibrate the time scale in calendar time units in this analysis, we pool the information about the RYMV evolutionary rate from several geographical partitions. Whereas the field surveys and the phylogeographic reconstructions both point to a rapid southward invasion across hundreds of kilometers throughout Madagascar within three to four decades, they differ on the inferred origin location and time of the epidemic. The phylogeographic reconstructions suggest a lineage displacement and unveil a re-invasion of the northern regions that may have remained unnoticed otherwise. Despite ecological differences that could affect the transmission potential of RYMV in Madagascar and in mainland Africa, we estimate similar invasion and dispersal rates. We could not identify environmental factors that have a relevant impact on the lineage dispersal velocity of RYMV in Madagascar. This study highlights the value and complementarity of (historical) nongenetic and (more contemporaneous) genetic surveillance data for reconstructing the history of spread of plant viruses.