Genetic signature of a range expansion and leap‐frog event after the recent invasion of Europe by the grapevine downy mildew pathogen Plasmopara viticola

Abstract

Biologic invasions can have important ecological, economic and social consequences, particularly when they involve the introduction and spread of plant invasive pathogens, as they can threaten natural ecosystems and jeopardize the production of human food. Examples include the grapevine downy mildew, caused by the oomycete Plasmopara viticola, an invasive species native to North America, introduced into Europe in the 1870s. We investigated the introduction and spread of this invasive pathogen, by analysing its genetic structure and diversity in a large sample from European vineyards. Populations of P. viticola across Europe displayed little genetic diversity, consistent with the occurrence of a bottleneck at the time of introduction. Bayesian coalescent analyses revealed a clear population expansion signal in the genetic data. We detected a weak, but significant, continental-wide population structure, with two geographically and genetically distinct clusters in Western and Eastern European vineyards. Approximate Bayesian computation, analyses of clines of genetic diversity and of isolation-by-distance patterns provided evidence for a wave of colonization moving in an easterly direction across Europe. This is consistent with historical reports, first mentioning the introduction of the disease in Bordeaux vineyards (France) and sub-sequently documenting its rapid spread across Europe. This initial introduction in the west was probably followed by a 'leap-frog' event into Eastern Europe, leading to the formation of the two genetic clusters we detected. This study shows that recent population genetics methods within the Bayesian and coalescence frameworks are extremely powerful for increasing our understanding of pathogen population dynamics and invasion histories.

Crop domestication facilitated rapid geographical expansion of a specialist pollinator, the squash beePeponapis pruinosa

“…While domestication invariably reduces genetic variation despite great increases in population size, the population structure of the pests, pathogens and mutualists associated with agriculturally important species do not change predictably. Reduced genetic variation found in populations of potato late blight (Phytophora infestans) in France was attributed to recent colonization from the British Isles [7], and in the grape pest, Plasmospara viticola, from a founder event in the 1870s [8]. By contrast, the softskinned fruit pest, Drosophila suzukii, was first reported in the continental USA in 2008, but retains comparable nucleotide variation to that observed from populations near its ancestral range [9].…”

“…R. Soc. B 283: 20160443 pest and pathogenic species of crops that spread with cultivation [7,8]. Demographic parameters estimated with coalescent analyses detected smaller present than ancestral effective populations sizes across the distribution of P. pruinosa.…”

Genome sequence of Plasmopara viticola and insight into the pathogenic mechanism

“…Plasmopara viticola is a strictly obligate biotrophic organism since its survival depends on living host cells and cannot be propagated on artificial media3. This pathogen is native to North America and was accidentally introduced into Europe via infected cuttings at the end of the 19 th century4. However, recent research56 has demonstrated the existence of a complex of cryptic P. viticola species specialized on different wild Vitis sp.…”

Microsatellites Reveal Genetic Homogeneity among Outbreak Populations of Crown-of-Thorns Starfish (Acanthaster cf. solaris) on Australia’s Great Barrier Reef

“…Elaborating on these patterns, model-based statistics can provide probabilistic estimations of the demographic and genetic history that are necessary to generate observed patterns of genetic structure e.g., [28,29]. Approximate Bayesian computation (ABC) approaches that incorporate the divergence and admixture of populations, as well as changes in population size and structure [30] can provide important information on the likely initiation and spread of species e.g., [31,32].…”