Multiple invasions,Wolbachiaand human-aided transport drive the genetic variability ofAedes albopictusin the Iberian Peninsula
Authors: Lucati Federica , Delacour Sarah , Palmer John R.B. , Caner Jenny , Oltra Aitana , Paredes-Esquivel Claudia , Mariani Simone , Escartin Santi , Roiz David , Collantes Francisco , Bengoa Mikel , Montalvo Tomàs , Delgado Juan Antonio , Eritja Roger , Lucientes Javier , Timor Andreu Albó , Bartumeus Frederic , Ventura Marc 
Published: July 2022

The Asian tiger mosquito,Aedes albopictus, is a highly invasive species that has been spreading rapidly throughout tropical and temperate regions worldwide since the late 1970s. On the Iberian Peninsula, it was first recorded in 2004 near Barcelona. Since then, the species has spread along the Mediterranean coast and is now colonising the Peninsula’s inner territories. As with other species of the genusAedes, the spread of the tiger mosquito has been linked to global shipping routes and road networks. In particular, the transport of adult mosquitoes by car has been shown to augment its natural spreading capacity by orders of magnitude. Much remains unknown, however, about the impact of human-mediated dispersal on the genetic variability of this species. This study aimed to ascertain the factors that have contributed to the spread and the current genetic variation ofAe. albopictusacross the Iberian Peninsula, through complex dispersal mechanisms and endosymbiosis with bacteria likeWolbachia. We do so through population genetic analysis of mitochondrial (COI) and nuclear (ITS2) DNA sequences. Overall, both COI and ITS2 markers showed a lack of genetic structure among sampled regions and the presence of worldwide dominant haplotypes, suggesting a pattern of multiple introductions from abroad. We found extremely low levels of variation in COI compared to ITS2, and this lack of mitochondrial polymorphism is likely explained by highWolbachiaprevalence (79%). Multilevel models revealed that greater mosquito fluxes (estimated from commuting patterns and tiger mosquito population distribution) and spatial proximity between sampling sites were associated with lower ITS2 genetic distance, suggesting that rapid short- and medium-distance dispersal is facilitated by humans through vehicular traffic. This study highlights the significant role of human transportation in shaping the genetic attributes ofAe. albopictusand promoting regional gene flow, and underscores the need for a territorially integrated surveillance across scales of this disease-carrying mosquito.

Author Summary

The tiger mosquito,Aedes albopictus, is one of the most invasive species in the world. Native to the tropical forests of Southeast Asia, over the past 30 years it has rapidly spread throughout tropical and temperate regions of the world. Its dramatic expansion has resulted in public health concerns as a consequence of its vector competence for at least 16 viruses. Previous studies showed thatAe. albopictusspread has been facilitated by human-mediated transportation, but much remains unknown about how this has affected its genetic attributes. Here we examined the factors that contributed to shaping the current genetic constitution ofAe. albopictusin the Iberian Peninsula, where the species was first found in 2004, by combining population genetics and Bayesian modelling. We found that both mitochondrial and nuclear DNA markers showed a lack of genetic structure and the presence of worldwide dominant haplotypes, suggesting regular introductions from abroad. Mitochondrial DNA showed little genetic diversity compared to nuclear DNA, likely explained by infection with maternally transmitted bacteria of the genusWolbachia. Our models indicated that human transportation plays a role in shapingAe. albopictusnuclear genetic structure by means of passive dispersal of adult tiger mosquitoes through the road network.