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Molecular Insights Into the Taxonomy of Hypanis (Bivalvia, Cardiidae, Lymnocardiinae) in the Black Sea Lagoons

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Molecular Insights Into the Taxonomy of Hypanis (Bivalvia, Cardiidae, Lymnocardiinae) in the Black Sea Lagoons Helgol Mar Res (2012) 66:153–158 DOI 10.1007/s10152-011-0256-1 ORIGINAL ARTICLE Molecular insights into the taxonomy of Hypanis (Bivalvia, Cardiidae, Lymnocardiinae) in the Black Sea lagoons Luis Popa · Oana Popa · Elena Iorgu · Beatrice Kelemen · Dumitru Murariu Received: 21 October 2010 / Revised: 23 March 2011 / Accepted: 24 March 2011 / Published online: 8 April 2011 © Springer-Verlag and AWI 2011 Abstract In this study, we used data from morphology Introduction and three DNA markers to assess the taxonomic status of the putative bivalve species Hypanis colorata and Hypanis The bivalve subfamily Lymnocardiinae in the family Car- angusticostata in a Black Sea lagoon, the Razelm Lake in diidae includes several fossil genera and two extant gen- Romania. The morphological data (the shape of shell ribs era, Hypanis and Didacna. In the former genus, two and the multivariate analysis of morphometric variance of subgenera have been described, Monodacna and Adacna. three variables constructed as the ratios between the main The subgenus Monodacna comprises about 20 living spe- dimensions of the shell) conWrmed that the two analyzed cies and/or subspecies distributed in the Black, Azov, species are distinct morphological entities. Three molecular and Caspian Seas and the connected brackish lakes markers, one from the nuclear genome (18S rRNA) and (Nabozhenko 2005). The literature on these species is scarce, two from the mitochondrial genome (16S rRNA and COI), and the diagnostic criteria used in species identiWcation showed extremely reduced sequence divergence (0–0.1%) include only a small number of conchological and ana- between the two putative species. Based on these results, tomical features with a great plasticity that leads to confusions we suggest that H. angusticostata and H. colorata are mor- and uncertainties (Borcea 1926; Munasypova-Motyash photypes of a single species. 2006a, b). Borcea (1926) made the Wrst extensive study on the Keywords Monodacna colorata · Monodacna Lymnocardiinae of the Black Sea lagoons and noticed the angusticostata · Genetic distance · Molecular markers presence of two species of Hypanis in the subgenus Mono- dacna, Hypanis pontica (Eichwald, 1838) (presented as Monodacna pseudocardium), and Hypanis colorata (Eichwald, 1829) (presented as Monodacna colorata). He described four varieties of Hypanis colorata, namely Communicated by H.-D. Franke. H. colorata var. ialpugensis, H. colorata var. angusticostata, H. colorata var. razelmiana, and H. colorata var. lucida. L. Popa and O. Popa contributed equally to this work. Thirty years later Zhadin (1952) considered that in the Electronic supplementary material The online version of this USSR Fauna there were three species in the genus Hypanis article (doi:10.1007/s10152-011-0256-1) contains supplementary (subgenus Monodacna): H. pontica (named M. pontica), material, which is available to authorized users. H. colorata (named M. colorata), and H. edentula (Pallas, 1771) (named M. edentula syn. M. caspia (Eichwald, L. Popa (&) · O. Popa · E. Iorgu · D. Murariu Grigore Antipa National Museum of Natural History, 1829)). Sos. Kiseleff Nr. 1, 011341 Bucharest, Romania In Romania, Grossu (1962, 1973), Tudorancea (1972), e-mail: [email protected]; [email protected] Negrea and Negrea (1975), and Sarkany-Kiss (1995) identi- Wed only two Hypanis (subgenus Monodacna) species: B. Kelemen Babes-Bolyai University, Molecular Biology Center, H. pontica (M. pontica) and H. colorata (M. colorata). In a 42 Treboniu Laurian Street, 400271 Cluj-Napoca, Romania monography of the Black and Azov Seas, Scarlato and 123 154 Helgol Mar Res (2012) 66:153–158 Starobogatov (1972) listed Wve species of this subgenus: (SW), and shell height (SH) were used to compute the SW/ H. (M.) pontica, H. (M.) colorata, H. (M.) caspia, H. (M.) SL, SH/SL, and SW/SH ratios. A MANOVA analysis was angusticostata (Borcea, 1926), and H. (M.) ialpugensis performed with the species designation as independent (Borcea, 1926). Munasypova-Motyash (2006a, b) studied variables and the three mentioned ratios as dependent vari- some anatomical features of the soft body and noticed the ables, using the software package PAST (Hammer et al. presence of three species of the subgenus Monodacna in 2001). A discriminant analysis/Hotelling test was per- Ukraine, H. angusticostata, H. colorata, and H. pontica. formed using the same software package. A P value of In the present work, we studied the taxonomic status of ·0.05 was considered statistically signiWcant. the putative species Hypanis colorata and Hypanis angusti- costata in the Razelm-Golovita Lake system in Romania. DNA isolation, ampliWcation, and sequencing First, we examined how diVerent these two putative species are from a morphological point of view, using a multivari- DNA isolation was performed with the NucleoSpin® ate morphometric analysis. Then, we analyzed three molec- Tissue kit (Macherey–Nagel GmbH & Co. KG, Düren, ular markers (18S rRNA, 16S rRNA, and COI) in order to Germany), according to the producer’s speciWcations. The see whether morphometric and genetic Wndings are in primers used for the ampliWcation of all three markers were agreement. We also compared the genetic divergence designed with M13 tails to facilitate the DNA sequencing between these two putative species with that between other process. The sequences of the six primers were as follows congeneric species belonging to the family Cardiidae, using (with the M13 tails in brackets): 16S rRNA, 16SF_M13f DNA sequences available in GenBank. (5Ј-CACGACGTTGTAAAACGACcgcctgtttatcaaaaacat-3Ј) and 16SR_M13r (5Ј-GGATAACAATTTCACACAGGcc gctctgaactcagatcacgt-3Ј) (Palumbi et al. 1991); 18S rRNA, Materials and methods 18SF_M13f (5Ј-CACGACGTTGTAAAACGACccgaggc cccgtgattggaatgag-3Ј) and 18SR_M13r (5Ј-GGATAACA Sample collection ATTTCACACAGGctctgtcgccgcagtacgaatgcc-3Ј) (Crease and Colbourne 1998); COI, CoxAF_M13f (5Ј-CACGACGTT Several hundred specimens of Hypanis were collected with GTAAAACGACcwaatcayaaagatattggaac-3Ј) and CoxAR_ a bottom dredge from the Razelm-Golovita Lake Complex M13r (5Ј-GGATAACAATTTCACACAGGaatatawacttcw (44°19Ј23.56ЈЈ–44°58Ј55.89ЈЈN; 28°47Ј11.47ЈЈ–29°06Ј30. gggtgacc-3Ј) (Colgan et al. 2003). 53ЈЈE) in July 2007, July 2009, and August 2009, at a depth For all the markers, the ampliWcation was performed in of 2–3 m. Upon collection, the samples were preserved in 25 l of a solution containing 10 mM Tris–HCl (pH 8.8 at 96% ethanol and transported to the laboratory for further 25°C), 50 mM KCl, 0.08% (v/v) Nonidet P40, 2.5 mM W processing. Morphological identi cation of the collected MgCl2, each dNTP at 0.1 mM, each primer at 0.08 M individuals was performed according to the shape of the (0.1 M for the COI primers), 1 unit of Taq DNA polymer- ribs (higher or more Xattened), the density of the ribs, the ase (Fermentas UAB, Vilnius, Lithuania), and approxi- dentition of the cardinal platform, and the thickness of mately 10 ng of DNA template. The temperature proWle of the valves according to Scarlato and Starobogatov (1972) and the polymerase chain reaction for the 16S rRNA and 18S Munasypova-Motyash (2006a, b). The specimens analyzed rRNA markers consisted of initial denaturation at 94°C for were deposited in the collections of the “Grigore Antipa” 30 s, followed by 2 cycles at 94°C for 30 s, 60°C for 45 s, National Museum of Natural History (Bucharest, Romania). 72°C for 45 s, followed by 5 cycles at 93°C for 30 s, 55°C for 45 s, 72°C for 45 s, followed by 29 cycles at 93°C for Morphometric analysis 30 s, 50°C for 1 min, 72°C for 1 min, and a Wnal extension step performed at 72° for 8 min. For the COI marker, the The following three morphometric variables were mea- temperature proWle of the ampliWcation reaction consisted sured in 114 specimens of H. colorata and H. angusticos- of initial denaturation at 94°C for 2 min, followed by 5 tata: shell length (SL: the maximum antero-posterior cycles at 94°C for 30 s, 45°C for 30 s, 72°C for 30 s, fol- dimension of the shell), shell width (SW: the maximum lowed by 35 cycles at 94°C for 30 s, 54°C for 30 s, 72°C left–right dimension with both valves appressed), and shell for 30 s, and a Wnal extension step performed at 72° for height (SH: the maximum dorsal–ventral dimension of the 5 min. The PCR products were separated on 1% agarose gel, shell measured perpendicular to the length). Bivalves were and the fragments of interest were excised and extracted measured with a digital caliper, to the nearest 0.01 mm. In using the GeneJET™ Gel Extraction Kit (Fermentas UAB, order to maximize the correct identiWcation of the speci- Vilnius, Lithuania). mens, all the analyzed individuals had a shell length larger The sequencing reaction was performed on a LICOR than 20 mm. The measured shell length (SL), shell width 4300L system, with the DNA Cycle Sequencing Kit (Jenna 123 Helgol Mar Res (2012) 66:153–158 155 Bioscience GmbH, Jena, Germany) with M13-labeled Table 1 Genetic markers analyzed in the two Hypanis species primers, according to manufacturer’s speciWcations, on 9 Nseq/hap/shared samples for the COI marker, 30 samples for the 16S rRNA marker, and 14 samples for the 18S rRNA marker. COI 16S 18S H. colorata 5/2/yes 24/2/yes 11/1/yes Sequences analysis Accession HQ420301, HQ420295, HQ420299 numbers HQ420303 HQ420298 The COI, 16S rRNA, and 18S rRNA sequences were H. angusticostata 4/2/yes 6/2/yes 3/1/yes aligned using the ClustalX program (Larkin et al. 2007). Accession HQ420302, HQ420296, HQ420300 Uncorrected genetic distances (p) were estimated for all numbers HQ420304 HQ420297 pairwise comparisons as the proportion of nucleotide sites Nseq number of analyzed sequences, Hap number of observed haplo- that are diVerent, as implemented in MEGA version 4 types, Shared presence/absence of the observed haplotypes in both (Tamura et al. 2007). In order to asses the genetic distance species among congeneric species as well as among individuals of the same species, we used 335 DNA sequences from the family Cardiidae available in GenBank from 11 genera for 430 bp from 24 specimens of H.
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