Grape Phylloxera Genetic Structure Reveals Root–Leaf Migration within Commercial Vineyards

SIMPLE SUMMARY: In most wine regions around the world, commercial vineyards are planted with Vitis vinifera scions grafted on grape phylloxera-tolerating rootstocks. Root-feeding phylloxera populations still thrive on such rootstocks and occasionally leaf-feeding phylloxera populations are observed. The cause for these foliar infestations is thought to reside at the thickets of abandoned rootstock vines that grow on the risers of vineyard terraces and constitute a different habitat with large leaf-feeding populations. Besides, it is unclear if root and leaf populations within commercial vineyards are genetically connected, which may indicate a process of adaption that could lead to large foliar phylloxera populations and better-adapted phylloxera biotypes. To shed light on these issues, phylloxera root- and leaf-feeding larvae from commercial vineyards and larvae from nearby thickets were genetically compared, focusing on population structure and genetic association. Our study showed that foliar populations in commercial vineyards not only originate from leaf-feeding populations on nearby abandoned rootstock vines, but also from root populations within the vineyard. The results suggest that sexual recombination is rare in the study area and that direct root–leaf migration creates population bottlenecks based on founder effects or host plant adaption. ABSTRACT: Depending on their life cycle, grape phylloxera (Daktulosphaira vitifoliae Fitch) leaf-feeding populations are initiated through asexually produced offspring or sexual recombination. The vine’s initial foliar larvae may originate from root-feeding phylloxera or wind-drifted foliar larvae from other habitats. Though some studies have reported phylloxera leaf-feeding in commercial vineyards, it is still unclear if they are genetically distinct from the population structure of these two sources. Using seven SSR-markers, this study analyzed the genetic structure of phylloxera populations in commercial vineyards with different natural infestation scenarios and that of single-plant insect systems that exclude infestation by wind-drifted larvae. We saw that during the vegetation period, phylloxera populations predominately go through their asexual life cycle to migrate from roots to leaves. We provided evidence that such migrations do not exclusively occur through wind-drifted foliar populations from rootstock vines in abandoned thickets, but that root populations within commercial vineyards also migrate to establish V. vinifera leaf populations. Whereas the former scenario generates foliar populations with high genotypic diversity, the latter produces population bottlenecks through founder effects or phylloxera biotype selection pressure. We finally compared these population structures with those of populations in their native habitat in North America, using four microsatellite markers.