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A Molecular Genetic Evidence of the Occurrence of the Freshwater Snail Radix Lagotis (Schrank, 1803) (Gastropoda: Lymnaeidae) in Bulgaria

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A Molecular Genetic Evidence of the Occurrence of the Freshwater Snail Radix Lagotis (Schrank, 1803) (Gastropoda: Lymnaeidae) in Bulgaria Research Article ISSN 2336-9744 (online) | ISSN 2337-0173 (print) The journal is available on line at www.biotaxa.org/em A molecular genetic evidence of the occurrence of the freshwater snail Radix lagotis (Schrank, 1803) (Gastropoda: Lymnaeidae) in Bulgaria KATRIN SCHNIEBS1*, DILIAN GEORGIEV2, PETER GLÖER3 & ANNA K. HUNDSDOERFER1 1Senckenberg Natural History Collections Dresden, Museum of Zoology, Königsbrücker Landstraße 159, D-1109 Dresden, Germany. E-mails: [email protected], [email protected] 2Department of Ecology and Environmental Conservation, University of Plovdiv, Tzar Assen Str. 24, BG-4000 Plovdiv, Bulgaria. E-mail: [email protected] 3Biodiversity Research Laboratory, Schulstraße 3, D-25491 Hetlingen, Germany. E-mail: [email protected] *Corresponding author: E-mail: [email protected] Received 5 August 2015 │ Accepted 19 August 2015 │ Published online 21 August 2015. Abstract Radix lagotis (Schrank, 1803) was found in the Dragoman marshes in Bulgaria. By comparison of the mitochondrial cyt-b sequences (fragment of 329 bp) and sequence data obtained from the nuclear ITS-2 spacer these specimens fell into one cluster with sequences from R. lagotis from Germany, Austria and Czech Republic confirming the morphological determination and the first record of this species for Bulgaria. Key words: Radix lagotis, Bulgaria, molecular genetics. Introduction Although Hubendick (1953) gave a very detailed morphological and anatomical description of Radix lagotis (Schrank, 1803), for a long time this species was not accepted as a distinct species by most European malacologists but referred to as forms of R. auricularia (Linnaeus, 1758) and R. peregra (O. F. Müller, 1774). However, it was generally accepted as species by Russian and Ukrainian malacologists (e. g. Kruglov & Starobogatov 1983, 1993; Stadnichenko 2004; Kruglov 2005). Using molecular genetic techniques Bargues et al. (2001) could distinguish R. lagotis from Czech Republic and Austria from the other Radix species occurring in Europe R. auricularia, R. balthica (Linnaeus, 1758), R. labiata (Rossmässler, 1835), and R. ampla (Hartmann, 1821) with certainty, and for the first time. The first evidences of the occurrence of R. lagotis in Germany were published by Oheimb et al. (2007) for Brandenburg, Glöer & Diercking (2009) for Hamburg, Schniebs et al. (2011) for Saxony, and Körnig et al. (2013) for Saxony-Anhalt. Morphological distinguishing characters between R. lagotis and other European Radix species were discussed by Schniebs et al. (2011, 2013) and Huňová et al. (2012). R. lagotis seems to be widely distributed in Europe and Western Siberia (Khokhutkin et al. 2003, 2009; Stadnichenko 2004; Kruglov 2005) as well as in Central Asia (Hubendick 1953; Stadnichenko 2004). But molecular genetically validated records are still published only from Austria (Bargues et al. 2001), Czech Republic (Bargues et al. 2001; Huňová et al. 2012), Germany (Schniebs et al. 2011, 2013; Körnig et al. 2013) and Kyrgyzstan (Glöer et al. 2014). Radix specimens and Radix species with an anatomy similar to Ecol. Mont., 3, 2015, 29-39 MOLECULAR GENETIC EVIDENCE OF RADIX LAGOTIS IN BULGARIA R. lagotis have been described from the Palaearctic [Hubendick 1953: R. peregra from Siberia and R. ovata (Draparnaud, 1805) from the Kola Peninsula; Falniowski 1980: R. peregra from Poland, Figs. 10, 12, 15, 16, 17; R. fontinalis (Studer, 1820), R. intermedia (Lamarck, 1822), R. burnetti (Alder, 1848), R. tenera (Küster, 1862), R. persica (Issel, 1865), R. aberrans (Westerlund, 1897) R. middendorffi (Dybowski, 1903), R. jacutica (Starobogatov et Streletzkaja, 1967), R. amurensis (Kruglov, Moskvicheva et Starobogatov, 1984), R. kafanovi (Kruglov et Starobogatov, 1984), R. nogoonica (Kruglov et Starobogatov, 1983), R. novikovi (Kruglov et Starobogatov, 1983), R. manomaensis (Kruglov, Starobogatov et Zatravkin, 1984)] and it would be very interesting to revise the group using molecular genetic analyses to find out whether the alleged species actually belong to one widely distributed species or they can be validated as several species. For Bulgaria Wohlberedt (1911) reported R. lagotis from Panega River near Vratsa town and Hesse (1913, 1914) from deposits of Maritsa River near Plovdiv city. The species was included in the catalog of Angelov (2000), omitted by Hubenov (2007), and again listed by Georgiev & Hubenov (2013). In April 2011, Radix specimens were collected in the Dragoman marshes in Bulgaria and sent to the Senckenberg Natural History Collections Dresden, Museum of Zoology (SNSD) for molecular genetic analyses. Anatomical examinations showed that they are very similar to R. lagotis found in Germany. The aim of this study was to elucidate whether these individuals indeed belong to this species. Material and Methods Snails were fixed in 70-80% ethanol or isopropyl alcohol. Shell morphology, mantle pigmentation and anatomy were documented from the specimens studied. Dissections and measurements of genital organs were carried out using stereo microscope (Nikon SMZ18). Photographs were taken with a digital camera system (Nikon DS-Fi2). All specimens used for morphological and molecular genetic studies are listed in Table 1. They are stored in the mollusc collection of the Senckenberg Natural History Collections Dresden, Museum of Zoology (SNSD). For the taxonomy we followed the current European checklists (Falkner et al. 2001; Bank 2011). Molecular techniques and phylogenetic analyses of sequences For outgroup comparison in the molecular genetic analyses we used Palaearctic specimens of the species Aplexa hypnorum (Linnaeus, 1758) from the freshwater gastropod family Physidae and from the lymnaeid species Lymnaea stagnalis (Linnaeus, 1758) and Stagnicola corvus (Gmelin, 1791). We included sequences of Radix auricularia (Linnaeus, 1758), R. balthica (Linnaeus, 1758), R. ampla (Hartmann, 1821) and R. labiata (Rossmässler, 1835) in the ingroup. In addition we used ITS-2 sequences of R. lagotis available from GenBank. Tissue samples taken from the foot were fixed in 100% ethanol. They were registered in the tissue collection of the SNSD with a tissue voucher number and the corresponding collection number in the mollusc collection of SNSD and stored at -80°C. All DNA-sequences have been placed in the European Nucleotide Archive (ENA, see http://www.ebi.ac.uk/ena/). For the molecular genetic analyses we obtained the sequence of the nuclear ITS-2 spacer (280 bp in A. hypnorum, up to 495 bp in L. stagnalis) and a 329 bp fragment of the cyt-b gene as a mitochondrial marker. For primers and protocols of DNA extraction, Polymerase Chain Reaction (PCR), purification of PCR products and DNA sequencing see Schniebs et al. (2011). Alignments were assembled using the sequence alignment editor BioEdit (Hall 1999). The ITS-2 alignment was obtained using the Clustal algorithm of MEGA version 4 (Tamura et al. 2007) and improved by eye. Phylogenetic analyses under the maximum parsimony (MP) criterion for the ITS-2 spacer and cyt-b fragment were carried out using PAUP (version 4.0b10; Swofford 2002; settings: gapmode = NewState, addseq = closest, the maximal number of trees with the setting of maxtree = 10000 did not have to be increased, since the number of best trees remained below 5000; number of bootstrap replicates = 10000). For presentation of the MP results for ITS-2 and cyt-b, one of the 4360 and 592 best trees respectively was chosen to be able to illustrate branch lengths (one showing the same overall topology as the majority rule consensus tree was chosen). 30 SCHNIEBS ET AL. For maximum-likelihood analyses, including bootstrap support, we used RAxML (raxmlGUI 0.9 beta 2, Silvestro & Michalak 2010; Stamatakis et al. 2005). The settings were “ML+thorough bootstrap” with 100 (replicate) runs and 1000 (bootstrap) repetitions. All DNA-sequences have been placed in the European Nucleotide Archive (ENA, see http://www.ebi.ac.uk/ena/). Table 1. Material used for the molecular genetic and morphological analyses. ENA=European Nucleotide Archive. Code Collection No. Locality ENA No. SNSD cyt-b ITS-2 Aplexa hypnorum (Linnaeus, 1758) Aplexa hypnorum 1 Moll S348 Germany, Mecklenburg-Western Pomerania, lake Nebel N 53°15'32" FR797882 FR797832 E 12°42'02" Aplexa hypnorum 2 Moll S350 Germany, Mecklenburg-Western Pomerania, lake Nebel N 53°15'32" FR7978823 FR797833 E 12°42'02" Lymnaea stagnalis (Linnaeus, 1758) Lymnaea stagnalis 1 Moll 49239 Germany, Saxony, Dresden, old branch of River Elbe, N LN874260 HE573064 50°59’50.80" E 13°52’29.39" Lymnaea stagnalis 2 Moll 49835 Germany, Saxony, Niederspree, small pond, N 51°24'28" E 14°54'03" HE573103 HE573065 Lymnaea stagnalis 3 Moll 53108 Germany, Baden-Württemberg, Konstanz- Egg, ditch Hockgraben, N FR797894 FR797834 47°40'57.3" E 9°11'34.2" Lymnaea stagnalis 4 Moll 53109 Germany, Baden-Württemberg, Konstanz- Egg, ditch Hockgraben, N FR797895 FR797835 47°40'57.3" E 9°11'34.2" Lymnaea stagnalis 5 Moll S1760 Ukraine: province Zaporozhye, Zarechnoe village, Yushanly River HG932145 HG931962 Lymnaea stagnalis 6 Moll S2311 Bulgaria: Plovdiv, floodplain of the Mariza River, N 42° 09' 13.5'' E HG932147 HG931965 24° 43' 34.8'' Stagnicola corvus (Gmelin, 1791) Stagnicola corvus 1 Moll 49821 Germany, Saxony, Niederspree, pond Großer Tiefzug, N 51°24'20" E HE577659 HE577638 14°53'38" Stagnicola corvus 2 Moll 49872 Germany, Saxony, pond Vierteich near Freitelsdorf, N 51°15'43" E HE577660 HE577639 13°41'57" Stagnicola corvus 3 Moll 52830 Germany, Saxony,
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