Genetic tracing reveals the role of ornamental plant trade in the simultaneous spread of three invasive ant species in Western Europe

Understanding how human activities trigger biological invasions is crucial to prevent the environmental and socioeconomic costs of invasive species. The Tapinoma nigerrimun complex comprises five species of ants, three of which ( T. darioi , T. ibericum , T. magnum ) exhibit biological and ecological characteristics of invasive ant species. These three species are native to Western Mediterranean Europe and North Africa, but have been reported as invasive in northern Europe. The ornamental plant trade is a common invasion pathway for many taxa, but its role in the continental spread of invasive Tapinoma species remains unknown. This study aims to identify the role of Ornamental Plant Sales Outlets (OPSOs) in the introduction of these three species and to determine the potential geographical origin of populations present in French OPSOs. Tapinoma colonies were sampled in 103 OPSOs across four French urban areas and one Corsican locality, with a specific focus on the Mediterranean region. Collected ant workers were identified to the species level using 15 microsatellite markers. Genotypes were compared to genetic profiles of European and North African populations to trace the geographical origin of introduced populations. We found a high prevalence of invasive species in OPSOs, with 66% (16/24) of invaded OPSOs in the urban area of Montpellier and 31% (19/61) in the urban area of Lyon, suggesting an important role of OPSOs in the introduction of the three species. Multiple introductions were detected in Montpellier OPSOs, both at species level (seven OPSOs with two or three invasive species) and between genetic clusters within species (five OPSOs with more than one genetic cluster for T. magnum ). Based on genetic clustering, populations with probable origins in Spain or Italy were detected in the French OPSOs. These results are particularly worrying as multiple simultaneous introductions might promote a rapid genetic recovery from founder effects for one species or result in hybridization between species. Overall, our findings highlight the importance of the trade in ornamental plants in shaping insect invasions and increasing the risk of genetic mixing with unforeseeable consequences on species invasiveness.