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Arion Vulgaris Moquin-Tandon, 1855 (Gastropoda: Pulmonata: Arionidae) in Europe

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Arion Vulgaris Moquin-Tandon, 1855 (Gastropoda: Pulmonata: Arionidae) in Europe View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Brage Nord Open Research Archive Organisms Diversity & Evolution (2020) 20:37–50 https://doi.org/10.1007/s13127-019-00417-z ORIGINAL ARTICLE A comprehensive phylogeographic study of Arion vulgaris Moquin-Tandon, 1855 (Gastropoda: Pulmonata: Arionidae) in Europe Kamila S. Zając1 & Bjørn A. Hatteland2,3 & Barbara Feldmeyer4 & Markus Pfenninger4 & Anna Filipiak5 & Leslie R. Noble6 & Dorota Lachowska-Cierlik7 Received: 30 April 2019 /Accepted: 25 September 2019 /Published online: 17 December 2019 # The Author(s) 2019 Abstract Arion vulgaris Moquin-Tandon, 1855 is regarded as one of the 100 most invasive species in Europe. The native distribution range of this species is uncertain, but for many years, the Iberian Peninsula has been considered as the area of origin. However, recent studies indicate that A. vulgaris probably originated from France. We have investigated the genetic structure of 33 European populations (Poland, Norway, Germany, France, Denmark, Switzerland) of this slug, based on two molecular markers, mito- chondrial cytochrome c oxidase subunit I (COI, mtDNA) and nuclear zinc finger (ZF, nDNA). Our investigation included published data from two previous studies, giving a total of 95 populations of A. vulgaris from 26 countries. This comprehensive dataset shows comparable haplotype diversity in Central, North and Western Europe, and significantly lower haplotype diversity in the East. All haplotypes observed in the East can be found in the other regions, and haplotype diversity is highest in the Central and Western region. Moreover, there is strong isolation by distance in Central and Western Europe, and only very little in the East. Furthermore, the number of unique haplotypes was highest in France. This pattern strongly suggests that A. vulgaris has originated from a region spanning from France to Western Germany; hence, the slug is probably alien/invasive in other parts of Europe, where it occurs. Our results indicate the necessity to cover as much of the distribution range of a species as possible before making conclusive assumptions about its origin and alien status. Keywords Invasive species . Gastropods . mtDNA . nDNA . Pest species . Phylogeography Electronic supplementary material The online version of this article (https://doi.org/10.1007/s13127-019-00417-z) contains supplementary material, which is available to authorized users. * Kamila S. Zając 2 Department of Biological Sciences, University of Bergen, [email protected] Bergen, Norway * Dorota Lachowska-Cierlik 3 Biotechnology and Plant Health, Norwegian Institute of Bioeconomy [email protected] Research (NIBIO), NIBIO Ullensvang, Lofthus, Bjørn A. Hatteland Ullensvang, Norway [email protected] 4 Biodiversity und Climate Research Centre by Senckenberg Barbara Feldmeyer Naturforschende Gesellschaft, Goethe-Universität, [email protected] Frankfurt, Germany Markus Pfenninger 5 Institute of Plant Protection - National Research Institute, [email protected] Władysława Węgorka 20, 60-318 Poznań, Poland Leslie R. Noble 6 Faculty of Biosciences and Aquaculture, Nord University, [email protected] 8049 Bodø, Norway 1 Institute of Environmental Sciences, Faculty of Biology, Jagiellonian 7 Institute of Zoology and Biomedical Research, Faculty of Biology, University, Gronostajowa 7, 30-387 Kraków, Poland Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland 38 ZającK.S.etal. Introduction basis of molecular analyses, mating behaviour or genital mor- phology (Noble 1992; Quinteiro et al. 2005;Barretal.2009; Alien species can have negative effects on natural ecosystems Kałuski et al. 2011; Slotsbo et al. 2012; Hatteland et al. 2015). including the displacement of endemic taxa (Sax et al. 2005; Moreover, in these three species, introgression has been ob- Davis 2009; Hatteland et al. 2013), which in turn can adverse- served and so far two types of hybrids have been discovered ly affect food security by impacting ecosystem services. A. ater × A. rufus and A. vulgaris × A. rufus (Evans 1986;Roth Therefore, alien and invasive species may be a threat to global et al. 2012;Dreijersetal.2013; Hatteland et al. 2015). biodiversity because of their impact on biological communi- Introgression seems to be commonest between A. ater and ties and economic costs (Walther et al. 2009;Kozłowski and A. rufus, and also occurs between A. ater and A. vulgaris Kozłowski 2011). Anthropogenic activity strongly increases (Hatteland et al. 2015). the spread and impact of many aliens, especially gastropods Recently, two contradictory studies about the origin, migra- and insects, which are easily spread with various trade goods. tion routes and status (invasive or native) of A. vulgaris have Among terrestrial invertebrates, Arion vulgaris Moquin- been published (Pfenninger et al. 2014;Zemanovaetal. Tandon, 1855 (Gastropoda: Pulmonata: Arionidae), also 2016). Pfenninger et al. (2014) used two molecular markers, known as the Iberian or Spanish slug, is regarded by one mitochondrial, cytochrome c oxidase subunit I (COI), and DAISIE organization (Delivering Alien Invasive Species one nuclear, zinc finger (ZF), together with species distribu- Inventories for Europe) as one of the 100 most invasive spe- tion modelling, to investigate the invasive status of this pest cies in Europe (Rabitsch 2006). It is of huge economic signif- species. Based on these results, Pfenninger et al. (2014)sug- icance because it causes serious damage to agricultural crops gested that A. vulgaris is probably native to Central Europe, and orchard cultivation resulting in financial losses (Frank because haplotypes from Spain or western France did not co- 1998;Grenetal.2009;Kozłowski 2010, 2012). occur with those from Central Europe. On the other hand, a For many years A. vulgaris has been regarded as Arion lack of data prevented testing for Eastern Europe as a place of lusitanicus (Mabille 1868), thought to have spread from the origin for A. vulgaris. area of the Iberian Peninsula (Spain, Portugal and Azores) to Zemanova et al. (2016) focused on A. vulgaris’ status to other countries (Simroth 1891;Quick1952, 1960;van verify whether it is invasive or native to Central Europe. Their Regteren Altena 1971; Chevallier 1972). However, analyses of mtDNA sequences (COI and ND1 markers) and Castillejo (1997)showedthatA. lusitanicus sampled outside microsatellites, obtained from European populations across Iberia was very different from the A. lusitanicus (Mabille the distribution range of this slug, indicated that classification 1868) originally described from Portugal based on internal of A. vulgaris as non-invasive would be premature. morphology. Phylogenetic studies by Quinteiro et al. (2005) The main aim of our study was to make a comprehensive and Hatteland et al. (2015) came to the same conclusion; thus, comparison of genetic variability between and within A. vulgaris has been recognized as distinct from A. lusitanicus European populations of A. vulgaris to shed light of the origin species, as also suggested by Falkner et al. (2002). Due to the of this species. Moreover, this study aimed to explore and morphological similarities and confusing taxonomy of older summarize the genetic structure of A. vulgaris populations in studies, the name A. lusitanicus often refers to the so called Europe. pest slug A. vulgaris commonlyoccurringinEurope. Currently, A. vulgaris is considered to be common in many European countries, from south to north, and up to now has Materials and methods been reported from France (in 1855), Great Britain (1952), Germany (1970), Slovenia (1970), Italy (1971), Switzerland Material collection (1971), Austria (1972), Sweden (1975), Bulgaria (1983), Austria (1984), Norway (1988), Belgium (1989), the Adult specimens of Arion slugs were collected into plastic Netherlands (1989), Finland (1990), Denmark (1991), boxes in 2014 from 42 populations across eight European Poland (1993), Iceland (2003–2004), Greenland, Latvia, countries: Norway (13), Poland (12), France (4), Denmark Lithuania, Faroe Islands and Romania (Weidema 2006; (3), Germany (3), Switzerland (3) and Netherlands (1) (see Zającetal.2017). Table 1, Supplementary Materials for details on sampling A. vulgaris is regarded as an invasive species in most stud- localities). Only mature slugs with genital morphology corre- ies, whereas another two species of terrestrial slugs, which sponding to the original description of A. vulgaris Moquin- have similar external appearance—A. ater (L., 1758) and Tandon, 1855 and A. lusitanicus (Welter-Schultes 2012)were A. rufus (L., 1758)—are considered as native to North- collected (5–15 slugs from each locality). All individuals were Western Europe (Welter-Schultes 2012; Hatteland et al. sent to the Institute of Environmental Sciences (Jagiellonian 2015;Zającetal.2017). These three species may co-exist in University), or the Norwegian Institute of Bioeconomy natural habitats and their differentiation is possible on the Research (NIBIO), or University of Bergen, and subsequently A comprehensive phylogeographic study of Arion vulgaris Moquin-Tandon, 1855 (Gastropoda: Pulmonata:... 39 prepared for further morphological and molecular analyses. 1-μl sample of PCR product was run on a 1.4% agarose gel for Remaining soft body parts were stored in 70% ethanol and 30 min at 100 V to check DNA quality. PCR products were material was deposited in the Institute of Environmental
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