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First Record of the Slug Species Semperula Wallacei (Issel, 1874) (Gastropoda: Eupulmonata: Veronicellidae) in Japan

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First Record of the Slug Species Semperula Wallacei (Issel, 1874) (Gastropoda: Eupulmonata: Veronicellidae) in Japan BioInvasions Records (2019) Volume 8, Issue 2: 258–265 CORRECTED PROOF Research Article First record of the slug species Semperula wallacei (Issel, 1874) (Gastropoda: Eupulmonata: Veronicellidae) in Japan Takahiro Hirano1,*, Daishi Yamazaki2, Shota Uchida2, Takumi Saito2 and Satoshi Chiba2,3 1Department of Biological Sciences, University of Idaho, Moscow, Idaho, USA 2Graduate school of Life Sciences, Tohoku University, Miyagi, Japan 3Center for Northeast Asian Studies, Tohoku University, Miyagi, Japan Author e-mails: [email protected] (TH), [email protected] (DY), [email protected] (SU), [email protected] (TS), [email protected] (SC) *Corresponding author Citation: Hirano T, Yamazaki D, Uchida S, Saito T, Chiba S (2019) First record of Abstract the slug species Semperula wallacei (Issel, 1874) (Gastropoda: Eupulmonata: In this study, we focus on veronicellid slugs in the Ryukyu and Ogasawara Islands Veronicellidae) in Japan. BioInvasions of Japan. We conducted phylogenetic analyses of these slugs, incorporating GenBank Records 8(2): 258–265, https://doi.org/10. data from several veronicellid species. A molecular phylogeny based on the 3391/bir.2019.8.2.07 mitochondrial COI gene revealed that three clades inhabit these islands. We report Received: 18 June 2018 here the first record of Semperula wallacei in Japan, which represents an introduced Accepted: 18 September 2018 species in this region. Published: 16 October 2018 Key words: introduced species, terrestrial mollusc, Ryukyu Islands, Ogasawara Handling editor: April Blakeslee Islands, phylogeny Copyright: © Hirano et al. This is an open access article distributed under terms of the Creative Commons Attribution License (Attribution 4.0 International - CC BY 4.0). Introduction OPEN ACCESS. The Veronicellidae is a family of terrestrial slugs (Barker 2001). There are currently 23 recognized genera in this family, and they are globally distributed throughout the tropics and subtropics (Gomes et al. 2010). Veronicellid slugs have also been introduced outside of their native range for example oceanic islands (Brodie and Barker 2011; Kim et al. 2016). Some veronicellid slugs are known to be a medium to high risk pest to humans and feed on the leaves and stems of young dry-bean plants, defoliating and often killing crops (Rueda et al. 2001; Brodie and Barker 2011). In addition, veronicellid slugs are considered to be major intermediate hosts of Angiostrongylus nematodes (Brodie and Barker 2011; Kim et al. 2014), which causes the disease angiostrongyliasis (Kim et al. 2014) or rat lung worm. In the worst cases, angiostrongyliasis can result in death in humans. The Ryukyu Islands and Ogasawara Islands of Japan are hotspots of land snail species diversity (Kameda et al. 2007; Chiba et al. 2009; Hoso et al. 2010; Hirano et al. 2014; Ministry of Environment 2014; Chiba and Cowie 2016). However, many introduced species of snails have been recorded on Hirano et al. (2019), BioInvasions Records 8(2): 258–265, https://doi.org/10.3391/bir.2019.8.2.07 258 First record of Semperula wallacei in Japan Figure 1. Images of representative individuals of lineages. A. Laevicaulis alte (Okinawa Island; photograph by H. Fukumori). B. Semperula wallacei (Chichijima Island, photo by T. Hirano). C. Veronicellidae sp. (Ishigaki Island, photo by T. Hirano). Scale bar indicates 10 mm. both island groups (Chiba et al. 2009; Chiba and Cowie 2016; Nature Conservation Division, Department of Environmental Affairs, Okinawa Prefectural Government 2017). For example, Laevicaulis alte (Férussac, 1822) was introduced on the Ryukyu Islands (Azuma 1982) and more recently in mainland Japan (Nishi and Matsuoka 2007). Here, we focus on veronicellid slugs on the Ryukyu Islands and Ogasawara Islands that differ from L. alte based on their external morphology (Figure 1). Compared with L. alte, these individuals differ in their ochre or brown body color and small body size. According to Schilthuizen and Liew (2008), L. alte is generally recognized by its dark gray or almost black body with a thin pale median dorsal line in contrast to the other slugs, which do not have this dorsal line. But, identifications of this family by external morphology are difficult (Cowie 1997; Kim et al. 2016). In particular, several veronicellid worms are similar to one another in external morphology, including Sarasinula plebeia (Fischer, 1868), Semperula wallacei (Issel, 1874), and Veronicella cubensis (Pfeiffer, 1840). Previous molecular studies have been useful for identifying and clarifying the phylogenetic relationships within the family (Gomes et al. 2010; Kim et al. 2016). However, the phylogenetic position Hirano et al. (2019), BioInvasions Records 8(2): 258–265, https://doi.org/10.3391/bir.2019.8.2.07 259 First record of Semperula wallacei in Japan among veronicellid species of the Ryukyu Islands and Ogasawara Islands is unclear. Therefore, we reconstructructed the molecular phylogeny of these slug species and report, for the first time a species of Veronicellidae other than L. alte in Japan. Materials and methods We collected five individuals of unidentified Veronicellidae species (Table 1) from the Ryukyu Islands and Ogasawara Islands (Figure 2) and a single individual of L. alte from Amami Island in the Ryukyu Islands. We also obtained sequence data of 25 individuals of 14 veronicellid species from GenBank (Table 1). We used two individuals from Onchidiid genera as outgroups (Dayrat et al. 2011). A fragment of the foot muscle of each living individual was stored in 99.5% ethanol for DNA extraction. Total DNA from the six individuals was extracted using a NucleoSpin Tissue Kit (Macherey-Nagel), following the manufacturer’s standard protocol. To estimate the phylogenetic relationships among the collected slugs, we sequenced fragments of the Cytochrome oxidase I (COI) mitochondrial gene. Polymerase chain reaction (PCR) conditions and the primers used are listed in Table 2. The PCR products were purified using Exo-SAP-IT (Amersham Biosciences, UK). The sequencing was performed using the BigDye Terminator Cycle Sequencing Ready Reaction Kit (Applied Biosystems) and electrophoresed using an ABI 3130xl sequencer (Applied Biosystems). The newly generated sequences have been deposited in the DDBJ/EMBL/GenBank databases (Table 1). The COI sequences were aligned using MUSCLE v3.8 (Edgar 2004), and summarized to limit node density artifacts (Fitch and Bruschi 1987; Fitch and Beintema 1990). Three individuals from the Ogasawara and Miyako Islands, and Semperula wallacei from GenBank (DQ897673) shared the same haplotype. Based on 470 bp of the sequence, we generated a maximum likelihood (ML) phylogenetic tree using MEGA6 (Tamura et al. 2013). Prior to the ML analysis, we selected the appropriate model (HKY+G+I) for sequence evolution also using MEGA6. Nodal support for the ML analysis was assessed using bootstrap analysis with 1000 replications. Only bootstrap values higher than 75% were considered to be strongly supported. Results The phylogenetic analysis recovered seven major clades (Figure 3). Clades A, B, and D only included one genus each (Colosius, Veronicella, and Sarasinula, respectively). Clade C was composed of the genera Phyllocaulis and Vaginulus. Semperula wallacei from the GenBank data (2 individuals), and four individuals from Okinawa Island (1), the Ogasawara (1) and Miyako Islands (2) constituted a well-supported clade F. However, the lone Hirano et al. (2019), BioInvasions Records 8(2): 258–265, https://doi.org/10.3391/bir.2019.8.2.07 260 First record of Semperula wallacei in Japan Table 1. Slug sampling sites and GenBank accession number of DNA sequences. Sampling site Accession Specimen ID No. Name number Samples collected by authors Laevicaulis alte 1 Amami, Kagoshima, Japan HC2445 LC415570 Semperula wallacei 2 (Miyako Islands) Taira, Miyakojima, Okinawa, Japan HC6220 LC415572 3 (Miyako Islands) Irabuikemasoe, Miyakojima, Okinawa, Japan HC6221 LC415573 6 (Chichijima Island) Chichijima, Ogasawara, Tokyo, Japan HC7454 LC415571 5 (Okinawa Island), Naha, Okinawa, Japan HC7455 LC415574 Veronicellidae sp. 4 (Ishigaki Island) Nagura, Ishigaki, Okinawa, Japan HC7456 LC415569 GenBank Colosius propinquus Imbabura, Ecuador JX532115 C. pulcher Pichincha, Ecuador JX532116 Napo, Ecuador JX532117 Colosius sp.1 Colombia JX532113 Napo, Ecuador JX532114 L. alte India KY774830 L. natalensis Natal, South Africa JX532110 L. sp. South Africa HQ660052 Phyllocaulis boraceiensis Sao Paulo, Brazil JX532111 Sarasinula linguaeformis Minas Gerais, Brazil JX532108 S. plebeia Iquitos, Loreto, Peru KM489401 Hawaii, USA KM489499 El Hatillo, Venezuela KM489393 S. sp. 1 Chapeco, Santa Catarina, Brazil KM489501 Sao Paulo, Sao Paulo, Brazil KM489446 Pinhalzinho, Sao Paulo, Brazil KM489448 S. sp. 2 Jatai, Goias, Brazil KM489452 Jatai, Goias, Brazil KM489454 Jatai, Goias, Brazil KM489456 Semperula wallacei Sabah, Malaysia DQ897673 Tutuila, American Samoa JX532109 Vaginulus taunaisii Brazil HQ660056 Veronicella cubensis Hawaii, USA HQ660057 St. Paul Parish, Antigua and Barbuda JX532112 Winfried Gibbons Nature Reserve, Devonshire Parish, South Road Bermuda KC206184 Outgroups Onchidella floridana HQ660035 Onchidium vaigiense HQ660040 Hirano et al. (2019), BioInvasions Records 8(2): 258–265, https://doi.org/10.3391/bir.2019.8.2.07 261 First record of Semperula wallacei in Japan Figure 2. Map of the veronicellid sampling sites. Site 1–5 are in the Ryukyu Islands, and 6 is in the Ogasawara Islands. The numbers correspond to the site number in
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