Linking intercontinental biogeographic events to decipher how European vineyards escaped Pierce's disease

Global change is believed to be a major driver of the emergence of invasive pathogens. Yet, there are few documented examples that illustrate the processes that hinder or trigger their geographic spread. Here, we present phylogenetic, epidemiological and historical evidence to explain how European vineyards escaped Xylella fastidiosa (Xf), the vector-borne bacterium responsible for Pierce's disease (PD). Using Bayesian temporal reconstruction, we show that the export of American grapevines to France as rootstocks to combat phylloxera (~1872-1895) preceded the spread of the Xf grapevine lineage in the USA. We found that the time of the most recent common ancestor in California dates to around 1875, which agrees with the emergence of the first PD outbreak and the expansion into the southeastern US around 1895. We also show that between 1870 and 1990, climatic conditions in continental Europe were mostly below the threshold for the development of PD epidemics. However, our model indicates an inadvertent expansion of risk in southern Europe since the 1990s, which is accelerating with global warming. Our temporal approach identifies the biogeographical conditions that have so far prevented PD in southern European wine-producing areas and predicts that disease risk will increase substantially with increasing temperatures.