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Population Genetic Analysis of Trematode Parasaccocoelium Mugili Zhukov, 1971 (Haploporidae Nicoll, 1914) from the Russian Far E

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Population Genetic Analysis of Trematode Parasaccocoelium Mugili Zhukov, 1971 (Haploporidae Nicoll, 1914) from the Russian Far E Parasitology Research (2019) 118:2575–2581 https://doi.org/10.1007/s00436-019-06401-y GENETICS, EVOLUTION, AND PHYLOGENY - ORIGINAL PAPER Population genetic analysis of trematode Parasaccocoelium mugili Zhukov, 1971 (Haploporidae Nicoll, 1914) from the Russian Far East and Vietnam based on ribosomal ITS and mitochondrial COI gene partial sequence data Dmitry M. Atopkin1,2 & Karina P. Chalenko3 & Ha V. Nguyen4 Received: 20 November 2018 /Accepted: 16 July 2019 /Published online: 3 August 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Intraspecific variation of Parasaccocoelium mugili collected from mullet fish of the south of Russian Far East and Vietnam has previously been estimated on the basis of two molecular markers: ribosomal internal transcribed spacer 1 (ITS1) rDNA and mitochondrial cytochrome oxidase I (COI) gene sequences. In the present study, molecular identification of this species from the Kievka River, Primorye and from Vietnam was performed by analysis of 28S rDNA sequences. Analysis of ITS1 rDNA sequences variation revealed two highly differentiated main groups, representing trematode specimens from the two regions. Genetic variation within each region was relatively low. Mitochondrial COI gene sequence data analysis revealed fixed nucle- otide and amino acid substitutions, and supported the existence of two genetically different groups associated with geographical origin. Analysis of the COI gene fragments showed extremely high variation within Russian and Vietnamese P. mugili samples. Our results for P. mugili most probably represent a case of initial step of allopotric speciation for this trematode, caused by living strategy of its definitive host at evolutionary scale. Mitochondrial DNA sequence data show that existence of gene flow between local populations of P. mu gi li in the Primorye Region caused by definitive hosts can be proposed. Keywords Mullet fish . P.mugili . Sequence data . Haploporidae . COI Introduction problem at the present time (Besprozvannykh et al. 2017a, 2017b;Blasco-Costaetal.2009; Pulis and Overstreet 2013; The topic of phylogenetic interrelationships of trematodes of Pulis et al. 2013;Andresetal.2014, 2015, 2018;Andresetal. the family Haploporidae Nicoll, 1914 is an actively discussed 2016). Recent studies using complex morphological and mo- lecular approaches have resulted in the identification of sev- eral new species, genera and subfamilies within the family, Section Editor: Christoph G. Grevelding along with leading to some taxonomical rearrangements (Pulis et al. 2013; Besprozvannykh et al. 2015a, 2017a, b; * Dmitry M. Atopkin [email protected] Andres et al. 2015;Curranetal.2018;Andresetal.2018). Most studies of haploporid trematodes have focused on high taxa, thus omitting the micro evolutionary processes which are 1 Federal Scientific Center of East Asia Terrestrial Biodiversity, Far an important factor during speciation. Population genetic stud- Eastern Branch of Russian Academy of Sciences, Vladivostok, Russia 690022 ies are useful for evaluating these processes through the anal- ysis of intraspecific polymorphism and differentiation using 2 Department of Cell Biology and Genetics, Far Eastern Federal University, Ajax-10 str., Vladivostok, Russia 690051 molecular data. The first investigation into these features was performed 3 Saint Petersburg National Research University of Information Technologies, Mechanics and Optics, Kronverksky ave., 49, Saint previously for the haploporid species Parasaccocoelium Petersburg, Russia 197101 mugili Zhukov, 1971. Trematodes of the genus 4 Institute of Ecology and Biological Resources, Vietnamese Academy Parasaccocoelium Zhukov, 1971 (Haploporidae, of Sciences and Technology, Hanoi, Vietnam Waretrematinae) are common intestinal parasites of the redlip 2576 Table 1 List of taxa incorporated into molecular analysis. N, number of sequences (28S/ITS1/COI). P (or C) and V, Primorye and Vietnam, respectively Species N Host Locality Reference № of samples/accession numbers 28S rDNA ITS1 rDNA COI gene, mtDNA Parasaccocoelium 8/53/77 Planiliza Kievka River, Primorye, Present study P01-P08 MK128572- P01-P12,P25,P27 MK128519- P01-P73, MK128586- mugili haematocheila Russian Far East MK128579 -29,P35,P38,P41, MK128563 C01-C04 MK128662 P43-P62,P66-P69, P71-P72 P. mugili 8/8/6 Mugil cephalus Cat Ba, Vietnam Present study V01-V08 MK128564- V01-V06,V08,V10 MK128511- V02-V03, MK128580- MK128571 MK128518- V05-V08 MK128585 P. mugili 3/−/− Planiliza Razdolnaya River, Primorye, Besprozvannykh et al. 2015a P.mug2-2,P. HF548468, –––– haematocheila Russian Far East mug1-1, HF548470, P.mug2-1 HF548473 P. haematochelium 2/−/− Planiliza Razdolnaya River, Primorye, Besprozvannykh et al. 2015a P.sp.n.1-1., HF548461, –––– haematocheila Russian Far East Par7-4 HF548467 P. polyovum 2/−/− Planiliza Razdolnaya River, Primorye, Besprozvannykh et al. 2015a Par4-1, HF548474, –––– haematocheila Russian Far East Par5-3 HF548478 al waters of Cat Ba Island, Vietnam ( of south of the Russian Far East ( ing parasitological field work from the Kievka River in the Besprozvannykh et al. ( RAS. Morphological description ofdepository this of biological sample samples of is FSC given of Biodiversity in FEB Haploporidae family, the genus 1845) in the Russian Far East. Following the revision of the mullet of one representative of Adult trematode specimens were collected from the intestine Material and methods from flukes using a hotSHOT technique96% (Truett ethanol for molecular analysis. Total DNA was extracted Parasaccocoelium mugili microscopy and all of them were identicaltion morphologically and to DNA extraction, all worms were examined with light 28S ribosomal DNA (rDNA) using the primers DIG12request. (5 samples can be obtained from the corresponding author upon ular variation of tochrome oxidase I gene (COI)end, and evaluation estimation of of ribosomal the ITS1, and molec- ferent the geographic mitochondrial cy- regions and definitive host species. To this specific variation of chondrial DNA sequence data ingraphical order origin. to To estimate test the this intra- hypothesis, we analysed mito- 2015b eral fixed nucleotide substitutionsnucleotide sequences, (Besprozvannykh which differed et from each al. othervariants by of sev- 28S rDNASkrjabinolecithum and spasskii internal transcribed spacerisolated (ITS) from mullet from the Russianintestine Far trematode East species and of Vietnam, theCat Waretrematinae subfamily Ba Island, Vietnam.been Molecular detected studies in of the another intestines giant of mullet in coastal waters of proaches (Besprozvannykh et al. ly been restored using morphological and molecular ap- lecular differences may exist in previous studies, we predicted thatiant similar was intraspecific found mo- indetected Vietnam. in Considering trematodes the of results the of Kievka River these and the third var- and (2) to estimate molecular variationIsland, of Vietnam using 28S rRNA gene sequence datain analysis Primorye, south of theP. Russian mugili Far East, and fromHaploporidae. Cat Ba The aims offirst this time study that were such (1) a to study identify has been carried out on Osteomugil cunnesius The polymerase chain reaction (PCR) was used to amplify ; Atopkin et al. Planiliza haematocheila in the intestines of mullet fish of the Kievka River P. mugili P. mugili. 2015 Planiliza haematocheila Vlnine,1836)(Valenciennes, from the coast- 2015a from these regions were carried out. ,Holotype ). Two sequence variants have been Belous, 1954, revealed three main n This is, to our knowledge, the P. mugili Parasaccocoelium ). Trematodes were fixed in = 75), and from one specimen Parasitol Res (2019) 118:2575 2015a (Temminck & Schlegel, n № ). This species has also = 8). Before preserva- ,associatedwithgeo- 50.1-Tr, which is in P. mugili 2006 in 2016 dur- has recent- from dif- ). DNA – 2581 ′ - Parasitol Res (2019) 118:2575–2581 2577 included. The COI gene fragments were amplified and direct- ly sequenced using the primers Trema-cox1/F (5′-TTC GGT CAT CCT GAG GTT TAT GTT-3′) and Trema-cox1/R (5′- CAG CAA ATC ATG ATG CAA AAG GTA-3′)withan annealing temperature of 50 °C (Atopkin et al. 2018). The PCR products were directly sequenced using the ABI Big Dye Terminator v.3.1 Cycle Sequencing Kit (Applied Biosystems, MA, USA), following the manufacturer’sin- structions, with the internal sequencing primers described by Tkach et al. (2003) for 28S rDNA, and those described by Luton et al. (1992) for the ITS2 rDNA fragment. The PCR products were analysed using an ABI 3130xl genetic analyser at the Department of Cell Biology, Far Eastern Federal University. Sequences were submitted to GenBank of the NCBI database with the accession numbers detailed in Table 1. Nucleotide sequences were assembled with SeqScape v. 2.6 software (Applied Biosystems, MA, USA). Alignments, estimation of the number of variable sites and sequence dif- ferences and unweighted pair group method with arithmetic mean (UPGMA) analysis were performed using MEGA 7.0 Fig. 1 UPGMA dendrogram of the genus Parasaccocoelium based on p- (Kumar et al. 2016). The UPGMA phylogenetic relationship distance estimation using 28S rDNA partial sequences. Nodal numbers, values of bootstrap statistics (%); numerals, index number of specimen. P significance was estimated using a bootstrap analysis and V, Primorye and Vietnam, respectively (Felsenstein 1985)with1000replications. Calculation of gene and nucleotide diversity indices (Hd and Pi, respectively), the differentiation index (Fst)
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