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Reconstructing the Invasion and the Demographic History of the Yellow-Legged Hornet, Vespa Velutina, in Europe M

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Reconstructing the Invasion and the Demographic History of the Yellow-Legged Hornet, Vespa Velutina, in Europe M Reconstructing the invasion and the demographic history of the yellow-legged hornet, Vespa velutina, in Europe M. Arca, F. Mougel, Thomas Guillemaud, S. Dupas, Q. Rome, A. Perrard, F. Muller, A. Fossoud, C. Capdevielle-Dulac, M. Torres-Leguizamon, et al. To cite this version: M. Arca, F. Mougel, Thomas Guillemaud, S. Dupas, Q. Rome, et al.. Reconstructing the invasion and the demographic history of the yellow-legged hornet, Vespa velutina, in Europe. Biological Invasions, Springer Verlag, 2015, 17 (8), pp.2357-2371. 10.1007/s10530-015-0880-9. hal-02370176 HAL Id: hal-02370176 https://hal.archives-ouvertes.fr/hal-02370176 Submitted on 15 Sep 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Reconstructing the invasion and the demographic history of the yellow-legged hornet, Vespa velutina, in Europe M. Arca • F. Mougel • T. Guillemaud • S. Dupas • Q. Rome • A. Perrard • F. Muller • A. Fossoud • C. Capdevielle-Dulac • M. Torres-Leguizamon • X. X. Chen • J. L. Tan • C. Jung • C. Villemant • G. Arnold • J.-F. Silvain Abstract The yellow-legged hornet, Vespa velutina, expansion. Analysis of the genetic data indicates that was accidentally introduced from Southeast Asia and French and Korean populations likely arose from two then invaded France and Korea over the last 10 years. independent introduction events. The most probable Since its introduction, its predation on honeybee source population is from an area between the Chinese colonies has rapidly become an economic problem in provinces of Zhejiang and Jiangsu. This invasion route invaded countries. Using mitochondrial cytochrome C is in agreement with knowledge on trade and historical oxidase and 22 nuclear microsatellite loci, we showed records. By studying colonies of V. velutina,we that native hornet populations were well differentiated demonstrated its polyandry, which is very rare among and highly diverse. In contrast, introduced populations Vespidae. This mating behavior could have favored from France and Korea suffered a genetic bottleneck, the success of this Asian hornet in Europe and Korea. which did not prevent their rapid geographic Combined, the population and colony results suggest that very few or possibly only one single multi-mated female gave rise to the invasion. Data accessibility DNA sequences: Genbank accessions JQ780449 JQ780462. Keywords Yellow-legged hornet Á Vespa velutina Á Invasive species Á Approximate Bayesian computation Electronic supplementary material The online version of this article (doi:10.1007/s10530 015 0880 9) contains supple mentary material, which is available to authorized users. M. Arca (&) Á S. Dupas Á A. Fossoud Á M. Arca Á F. Mougel Á G. Arnold C. Capdevielle Dulac Á M. Torres Leguizamon Á CNRS, UMR EGCE (Evolution, Ge´nome, Comportement J. F. Silvain et Ecologie) Univ. Paris Sud CNRS IRD, Univ. Paris IRD, UMR EGCE (Evolution, Ge´nome, Comportement et Saclay, Gif sur Yvette, France Ecologie) Univ. Paris Sud CNRS IRD, Univ. Paris Saclay, Gif sur Yvette, France T. Guillemaud e mail: [email protected] INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355 7254 Institut Sophia Agrobiotech, 400 Route des J. F. Silvain Chappes, BP 167, 06900 Sophia Antipolis, France e mail: Jean [email protected] gif.fr Q. Rome Á A. Perrard Á F. Muller Á C. Villemant M. Arca Á F. Mougel Á S. Dupas Á C. Capdevielle UMR7205, CP50, Muse´um National d’Histoire Naturelle, Dulac Á M. Torres Leguizamon Á G. Arnold Á 45 rue Buffon, 75005 Paris, France J. F. Silvain Universite´ Paris Sud 11, 91405 Orsay Cedex, France M. Arca et al. Introduction but most failed to become established (Beggs et al. 2011; Villemant et al. 2011). One Vespidae that has The increases of global trade and human mobility made rapid and high-profile invasions is the yellow- over the last century have resulted in unprecedented legged hornet, Vespa velutina, recently introduced numbers of invasions by non-native species all over and established in both France and Korea. This was the world. These biological invasions have severe the first successful invasion of an exotic vespid into impacts on agriculture and natural resources (Mack Europe (Villemant et al. 2011) and it was noticeable et al. 2000). Social insects are among the most for its velocity. Vespa velutina naturally occurs in successful invasive groups (Moller 1996). Their Asia, from Afghanistan to eastern China, Indo-China invasive success has been attributed to life-history and Indonesia (Carpenter and Kojima 1997), where it traits that facilitate their introduction and expansion is known as an active predator of honeybees (Abrol into new habitats (Holway et al. 2002). Sociality is 1994; Tan et al. 2007). The first field record of the generally associated with behavioral flexibility, yellow-legged hornet in France was obtained in the which may contribute to the invasive success of Lot-et-Garonne de´partement in 2005, although, ac- some social species. For example, introductions of cording to local testimonies, it was likely present as ants, which are among the most widespread and early as 2004 (Villemant et al. 2011). Following its damaging alien species, are often accompanied by introduction, the hornet spread rapidly across south- alterations in social behavior and colony structure that west France. The invaded area had reached about contribute to their success (Tsutsui et al. 2001; Suarez 190,000 km2 by 2010 (Villemant et al. 2011; Fig. 1) and Tsutsui 2008). and 360,000 by 2012 (Rome et al. 2013). The hornet Another key to the invasive success of social insects was also reported in northern regions of Spain and in is the ability of a single queen to found a large colony northern Portugal. One male was also recorded in and to produce many reproductive females that then Belgium in 2011 (Rome et al. 2013). Comparisons of offer a large dispersal capacity (Moller 1996; Chap- the climatic niches between the native and invasive man and Bourke 2001; Schmid-Hempel et al. 2007; range revealed that many countries of Western Mikheyev et al. 2009). Europe have climatic conditions suitable for V. Association with human activities such as pollini- velutina and, therefore, a high probability of being sation is another element that makes social insects invaded (Villemant et al. 2011). The first hornet successful invaders because of deliberate displace- observation in France was made by a French bonsai ment of large samples of individuals and often producer who regularly imported pots from Chinese repetitive events of introduction. This association is coastal areas close to Shanghai (Villemant et al. particularly relevant for bees (Bombus and Apis spp.), 2011). It has thus been suggested that the first which have been introduced to many new areas for introduction of the Asian yellow-legged hornet into economic reasons (Moller 1996; Ings et al. 2006). France was associated with an importation of horti- Among social hymenoptera, Vespa species are not cultural pots carried on cargo boats from these commonly considered invasive. Several species have Chinese provinces (Villemant et al. 2006). It is well been introduced to areas beyond their native ranges, known that social Vespidae are transported passively by man, as fertilized queens seek sheltered locations in which to undergo diapause. Such shelters are often X. X. Chen State Key Laboratory of Rice Biology and Ministry of found in human goods, which may then be trans- Agriculture Key Laboratory of Molecular Biology of Crop ported to new locations with the queens as passengers Pathogens and Insects, Institute of Insect Sciences, (Beggs et al. 2011). A full nest could not voyage in Zhejiang University, Hangzhou 310029, China this way as, under the same conditions, it would be J. L. Tan detected and destroyed. School of Life Sciences, Northwest University, 229 Taibai Little is known about the V. velutina introduction to North Road, Xi’an 710069, Shaanxi, China Korea. The hornet was found for the first time on the Bongrae Mountain, Yeong-do districts, near Busan, in C. Jung School of Bioresource Sciences, Andong National 2003. Vespa velutina appears to have spread much University, Andong 760 749, Korea more slowly in Korea (Choi et al. 2012) than in France History of the yellow legged hornet France (48†, 83‡) Korea (8†, 8‡) Zhejiang/Jiangsu (11†, 30‡) Yunnan (18†, 20‡) Haplotype F Haplotype K Haplotype Z Haplotype Y Vietnam Haplotype U (8†, 8‡) Haplotype A Haplotype I Haplotype D Haplotype N Haplotype V Haplotype T 100 Km 1000 Km Indonesia (3†, 21‡) Fig. 1 Map of the six regions sampled for the yellow legged haplotype names are associated with a color code as indicated in hornet Vespa velutina. Each point on the map represents a the legend. Dagger number of samples used for mitochondrial sampled locality. Grey areas indicate the known distribution analysis; double dagger number of samples for microsatellite range of V. velutina in 2010. The pie charts display haplotype analysis. All samples are listed in table S1 in which samples frequency for the mitochondrial COI marker in each sampled used for mtDNA characterization are in bold region and their size is proportional to the sampling effort. The (Rome et al. 2013). The reason for this might be that impact of V. velutina on insect diversity is difficult to the invasive hornet must contend with six other Vespa assess, while the damage to French apiaries is obvious: species in Korea, whereas only one, V.
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