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

Quaresma, Andreia; Henriques, Dora; Godinho, Joana; Maside, Xulio; Bortolotti, Laura; Pinto, M. Alice

doi:10.1007/s10530-022-02730-9

Original Paper
Published: 29 January 2022

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

Andreia Quaresma¹,
Dora Henriques¹,
Joana Godinho²,
Xulio Maside^3,4,
Laura Bortolotti⁵ &
M. Alice Pinto ORCID: orcid.org/0000-0001-9663-8399¹

Biological Invasions volume 24, pages 1479–1494 (2022)Cite this article

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A Correction to this article was published on 26 March 2022

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Abstract

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.

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Change history

26 March 2022
A Correction to this paper has been published: https://doi.org/10.1007/s10530-022-02760-3

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Acknowledgements

The authors are grateful to the many people who graciously contributed with V. velutina specimens, namely: Marco PortoCarrero, Tiago Moreira, Miguel Maia, Bruno Moreira, Ester Ordóñez Dios, David Outeiro, Egoitz Galarza, Nicole Filipe, Inês Madeira, Carla Teixeira, Carlos Cadime, Andrea Chasqueiro, Ana Paula Vale, Carla Brites, João Valente, Paulo Russo, Mónica Lopes, João Mesquita, and Sílvia Rodrigues. We are also deeply grateful to Florence Mougel (Laboratoire Evolution Génome Spéciation, CNRS) for providing DNA samples from France. D.H. was supported by the project BeeHappy (POCI-01-0145-FEDER-029871) funded by FEDER (Fundo Europeu de Desenvolvimento Regional) through the program COMPETE 2020—POCI (Programa Operacional para a Competividade e Internacionalização), and by Portuguese funds through FCT (Fundação para a Ciência e a Tecnologia). FCT provided financial support by national funds (FCT/MCTES) to CIMO (UIDB/00690/2020). 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”.

Funding

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).

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Authors and Affiliations

Centro de Investigação de Montanha, Instituto Politécnico de Bragança, Bragança, Campus de Santa Apolónia, 5300-253, Bragança, Portugal
Andreia Quaresma, Dora Henriques & M. Alice Pinto
National Institute of Agrarian and Veterinary Research, I.P. (INIAV), Oeiras, Portugal
Joana Godinho
Grupo de Medicina Xenómica, CIMUS, Universidade de Santiago de Compostela, Santiago de Compostela, Galiza, 15781, Spain
Xulio Maside
Instituto de Investigación Sanitaria de Santiago (IDIS), Santiago de Compostela, Galiza, 15076, Spain
Xulio Maside
Honey Bee and Silkworm Research Unit (CRA-API), Council for Agricultural Research and Economics, Research Centre for Agriculture and Environment (CREA-AA), Bologna, Italy
Laura Bortolotti

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Andreia Quaresma
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Dora Henriques
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Joana Godinho
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Xulio Maside
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Laura Bortolotti
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M. Alice Pinto
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Contributions

MAP conceived the ideas and designed the methodology. AQ performed the laboratorial work as well as most of the analyses with assistance of DH and MAP. All the authors contributed with data interpretation. MAP and AQ wrote the manuscript. DH, JG, XM and LB critically revised the manuscript for important intellectual content.

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Correspondence to M. Alice Pinto.

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Quaresma, A., Henriques, D., Godinho, J. et al. Invasion genetics of the Asian hornet Vespa velutina nigrithorax in Southern Europe. Biol Invasions 24, 1479–1494 (2022). https://doi.org/10.1007/s10530-022-02730-9

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Received: 24 June 2021
Accepted: 01 January 2022
Published: 29 January 2022
Issue Date: May 2022
DOI: https://doi.org/10.1007/s10530-022-02730-9

Keywords

Yellow-legged hornet
Alien species
Biological invasion
Genetic diversity
Microsatellites
mtDNA