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 nucleotide 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. mugili in the Primorye Region caused by definitive hosts can be proposed.
Similar content being viewed by others
References
Andres MJ, Pulis EE, Cribb TH, Overstreet RM (2014) Erection of the haploporid genus Litosaccus n.g. and its phylogenetic relationship within the Haploporidae Nicoll, 1914. Syst Parasitol 89:185–194. https://doi.org/10.1007/s11230-014-9521-4
Andres MJ, Curran SS, Fayton TJ, Pulis EE, Overstreet RM (2015) An additional genus and two additional species of Forticulcitinae (Digenea: Haploporidae). Folia Parasitol 62:025. https://doi.org/10.14411/fp.2015.025
Andres MJ, Pulis EE, Overstreet RM (2016) Description of three species of Isorchis (Digenea: Atractotrematidae) from Australia. Acta Parasitol 61:590–601
Andres MJ, Pulis EP, Curran SS, Overstreet RM (2018) On the systematic of some marine haploporids (Trematoda) with the description of a new species of Megasolena Linton, 1910. Par Int 67:805–815. https://doi.org/10.1016/j.parint.2018.08.002
Atopkin DM, Beloded AY, Ngo HD (2015) Molecular genetic characterization of the far eastern trematode Skrjabinolecithum spasskii Belous, 1954, (Digenea, Haploporidae), a parasite of mullets. Rus J Mol Biol 49:373–379. https://doi.org/10.1134/S0026893315030024
Atopkin DM, Nakao M, Besprozvannykh VV, Ha ND, Nguyen HV, Sasaki M (2018) Morphological and molecular data for species of Lecithaster Lühe, 1901 and Hysterolecithoides Yamaguti, 1934 (Digenea: Lecithasteridae) from fish of East Asia and phylogenetic relationships within the Hemiuroidea Looss, 1899. J Helminthol. In press
Besprozvannykh VV, .Atopkin DM, Ermolenko, AV, Nikitenko AYu (2015a) Restoration of the genus Parasaccocoelium Zhukov, 1971 (Digenea: Haploporidae) and a description of two new species from mugilid fish in the Far East of Russia. J Helminthol 89:565–576. https://doi.org/10.1017/S0022149X14000443
Besprozvannykh VV, Atopkin DM, Ngo HD, Beloded АY, Ermolenko АV, Ha NV, Tang NV (2015b) Skrjabinolecithum spasskii Belous, 1954 (Digenea: Haploporidae), parasite of mullets (Mugilidae) from Primorsky Region (Far East of Russia) and Tonkin Bay (North Vietnam): morphology and molecular data. Rus J Mar Biol 41:267–275. https://doi.org/10.1134/S1063074015040021
Besprozvannykh VV, Atopkin DM, Ermolenko АV Beloded АY (2017a) Morphometric and molecular analyses for a new species Skrjabinolecithum pyriforme n. sp. (Digenea: Haploporidae) in mullet fish from the Primorsky Region, Russia. J Helminthol 91:625–632. https://doi.org/10.1017/S0022149X16000626
Besprozvannykh VV, Atopkin DM, Ngo HD, Ha NV, Tang NV, Beloded АY (2017b) Morphometric and molecular analyses of two digenean species from the mullet: Skrjabinolecithum spinosum n. sp. from the Russian southern Far East and Unisaccus tonkini n. sp. from Vietnam. J Helminthol 92:713–724. https://doi.org/10.1017/S0022149X17000943
Blair D, Agatsuma T, Watanobe T, Okamoto M, Ito A (1997) Geographical genetic structure within the human lung fluke, Paragonimus westermanii, detected from DNA sequences. Parasitology 115:411–417
Blasco-Costa I, Balbuena JA, Kostadinova A, Olson PD (2009) Interrelationships of the Haploporinae (Digenea: Haploporidae): a molecular test of the taxonomic framework based on morphology. Parasitol Int 58:263–269. https://doi.org/10.1016/j.parint.2009.03.006
Curran SS, Pulis EE, Andres MJ, Overstreet RM (2018) Two new species of Saccocoelioides (Digenea: Haploporidae) with phylogenetic analysis of the family, including species of Saccocoelioides from North, Middle and South America. J Parasitol 104:221–239. https://doi.org/10.1645/17-189
Felsenstein J (1985) Confidence limits on phylogenies: an approach using bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589
Iwagami M, Ho LY, Su K, Lai PF, Fukushima M, Nakano M, Blair D, Kawashima K, Agatsuma T (2000) Molecular phylogeographic studies on Pragonimus westermanii in Asia. J Helminthol 74:315–322. https://doi.org/10.1017/S0022149X00000469
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Luton K, Walker D, Blair D (1992) Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Mol Biochem Parasitol 56:323–327. https://doi.org/10.1016/0166-6851(92)90181-I
Pulis E, Overstreet R (2013) Review of haploporid (Trematoda) genera with ornate muscularisation in the region of the oral sucker, including four new species and a new genus. Syst Parasitol 84:167–191. https://doi.org/10.1007/s11230-012-9401-8
Pulis E, Fayton T, Curran S, Overstreet R (2013) A new species of Intromugil (Digenea: Haploporidae) and redescription of Intromugil mugilicolus. J Parasitol 99:501–508. https://doi.org/10.1645/12-106.1
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Tkach VV, Littlewood DTJ, Olson PD, Kinsella JM, Swiderski Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst Parasitol 56:1–15
Truett GE (2006) Preparation of genomic DNA from animal tissues. In: Kieleczawa J (ed) The DNA book: protocols and procedures for the modern molecular biology. Jones & Bartlett Publisher, MA, pp 33–46
Acknowledgements
Authors of the present study deeply thanks to collaborators of the laboratory of parasitology of FSC Biodiversity FEB RAS, namely Vladimir V. Besprozvannykh (Ph.D., Head) and Alexey V. Ermolenko (Ph.D., senior researcher) for help with material collection and trematode species identification.
Funding
This study was supported by Grant of Russian Scientific Foundation, № 17-74-20074.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Christoph G. Grevelding
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Atopkin, D.M., Chalenko, K.P. & Nguyen, H.V. 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. Parasitol Res 118, 2575–2581 (2019). https://doi.org/10.1007/s00436-019-06401-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06401-y