Invasion genetics of the Asian hornet Vespa velutina nigrithorax in Southern Europe

In 2004, Vespa velutina was first seen in France. Since then, this fierce honey bee predator spread across many countries, giving rise to one of the most phenomenal insect invasions in Europe. An early study in France showed a genetically depauperate population, originating from a single multi-mated queen introduced from China. Here, we further unveil V. velutina invasion genetics in Europe by surveying the Iberian and Italian peninsulas using cytonuclear markers. Our results show that the French population acted as the colonists’ source in Spain, Portugal and Italy, leading to rejecting the hypothesis of multiple introductions from the native range. While Spain and Italy were colonized predominantly by leading-edge expansions from the French core population, in Portugal the invasion started from long-distance jump. Both processes were accompanied by a significant reduction in genetic diversity, with stronger losses for Portugal (Ar = 17.4%; uHe = 42.3%) than for Spain (Ar = 9.0%; uHe = 20.6%) or Italy (Ar = 16.3%; uHe = 26.8%). Signatures of differentiation and population structure, associated to the founding event in Portugal, enabled detection of secondary contact between the front derived from the primary propagule introduced in France and the front derived from the secondary propagule introduced in Portugal. Detection of first-generation migrants in the three countries suggests continuous gene flow that is bringing in new alleles, and this effect is stronger in Portugal, as reflected by a 20.3% increase in allelic richness. Overall, this study provides further insights into the invasion genetics of V. velutina in Europe, which can aid developing strategies to manage this major threat to beekeeping.This research was funded by the program POSEUR- 03-2215-FC-000008, through the project ‘‘GesVespa: Estratégias de gestão sustentável da Vespa velutina no Norte de Portugal’’. Fundação para a Ciência e a Tecnologia provided financial support by national funds (FCT/MCTES) to CIMO (UIDB/00690/2020).