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Genetic Divergence of Mussels (Mollusca, Mytilidae) Based on the 28S rRNA, 18S rRNA, and H3 Nuclear Gene Sequences

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Abstract

On the basis of nucleotide sequences of three nuclear genes and using molecular phylogenetic and evolutionary genetic approaches, the phylogeny of the main representatives of one of the largest taxa of bivalve mollusks, the family Mytilidae, was studied, and its system and taxonomy were refined. A phylogenetic system for the family Mytilidae and closely relative taxa of the order Mytilida, which currently has no consensus among specialists on the basis of traditional characters, is presented. Using nucleotide sequences of the 28S rRNA, 18S pRNA, and histone H3 genes, this consensus was established by the study of Mytilidae. Some concerns of mussel systematics were resolved; in particular, the monophyly of the family Mytilidae Rafinesque, 1815 was established with the strongest support for the subfamily Mytilinae Rafinesque, 1815. The data obtained disprove Distel’s conclusion on polyphyly of the subfamily Mytilinae Rafinesque, 1815. Isolation of the taxa in the rank of the Modiolinae G. Termier & H. Termier, 1950 and Bathymodiolinae Kenk & Wilson, 1985 subfamilies in the family Mytilidae and also the family Septiferidae Scarlato et Starobogatov, 1979 was confirmed, although the rank of the later taxon is not universally recognized and it remains to be clarified in an additional study.

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References

  1. Skurikhina, L.A., Kartavtsev, Yu.F., Chichvarkhin, A.Yu., and Pan’kova, M.V., Study of two species of mussels, Mytilus trossulus and Mytilus galloprovincialis (Bivalvia, Mytilidae), and their hybrids in Peter the Great Bay of the Sea of Japan with the use of PCR markers, Russ. J. Genet., 2001, vol. 37, no. 12, pp. 1448–1450.

    CAS  Google Scholar 

  2. Kartavtsev, Y.Ph., Chichvarkhin, A.Y., Kijima, A., et al., Allozyme and morphometric analysis of two common mussel species of Mytilus genus (Mollusca, Mytilidae) in Korea, Japan and Russia waters, Korean J. Genet., 2005, vol. 27, no. 4, pp. 289–306.

    CAS  Google Scholar 

  3. Boss, K.J., How Many Species of Mollusks Are There?, American Malacological Union, Annual Report, 1971.

    Google Scholar 

  4. Huber, M., Compendium of Bivalves: A Full-Color Guide to 3300 of the World’s Marine Bivalves. A Status on Bivalvia after 250 Years of Research, Hackenheim: Conch Books, 2010.

    Google Scholar 

  5. Kafanov, A.I. and Drozdov, A.L., Comparative sperm morphology and phylogenetic classification of recent Mytiloidea (Bivalvia), Malacologia, 1998, vol. 39, pp. 129–139.

    Google Scholar 

  6. Bayne, B.L., Primary and secondary settlement in Mytilus edulis L. (Mollusca), J. Anim. Ecol., 1964, vol. 33, pp. 513–523.

    Article  Google Scholar 

  7. Skarlato, O.A., Dvustvorchatye mollyuski umerennykh shirot zapadnoi chasti Tikhogo Okeana (Bivalve Mollusks of Temperate Latitudes of the Western Pacific Ocean), Leningrad: Nauka, 1981.

    Google Scholar 

  8. Lutz, R.A. and Kennish, M.J., Ecology of deep-sea hydrothermal vent communities: a review, Rev. Geophys., 1993, vol. 31, pp. 211–242.

    Article  Google Scholar 

  9. Distel, D.L., Baco, A.R., Chuang, E., et al., Marine Ecology–do mussels take wooden steps to deep-sea vents, Nature, 2000, vol. 403, no. 6771, pp. 725–726.

    Article  PubMed  CAS  Google Scholar 

  10. Skarlato, O.A. and Starobogatov, A.I., The systematic position and distribution of mussels, Promyslovye dvustvorchatye mollyuski–midii i ikh rol’ v ekosistemakh (Commercial Bivalve Molluscan Mussels and Their Role in the Ecosystem), Scarlato, O.A., Ed., Leningrad: Zool. Inst. Akad. Nauk USSR, 1979, pp. 106–111.

    Google Scholar 

  11. Seed, R., Systematics, evolution and distribution of mussels belonging to the genus Mytilus: an overview, Am. Malacol. Bull., 1992, vol. 9, pp. 123–137.

    Google Scholar 

  12. Distel, D.L., Phylogenetic relationships among Mytilidae (Bivalvia): 18S RNA data suggest convergence in mytilid body plans, Mol. Phyl. Evol., 2000, vol. 15, no. 1, pp. 25–33.

    Article  CAS  Google Scholar 

  13. Newell, N.D., Classification of Bivalvia, Treatise on Invertebrate Paleontology, Moore, R.C., Ed., vol. 1: Mollusca 6: Bivalvia, Kansas: Geological Society of America, 1969, pp. 205–224.

    Google Scholar 

  14. Chichvarkhin, A., Phylogeny and taxonomy of marine mussels: comments on the paper by Distel (2000), Mol. Phylogenet. Evol., 2002, vol. 22, no. 2, pp. 330–332.

    Article  PubMed  Google Scholar 

  15. Rawson, P.D. and Hilbish, T.J., Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex, Mol. Biol. Evol., 1995, vol. 12, pp. 893–901.

    PubMed  CAS  Google Scholar 

  16. Soot-Ryen, T., Superfamily Mytilacea Rafinesque, 1815, Treatise on Invertebrate Paleontology, Moore, R.C., Ed., vol. 1: Mollusca 6: Bivalvia, Kansas: Geological Society of America, 1969, pp. 271–280.

    Google Scholar 

  17. Soot-Ryen, T., A report on the family Mytilidae (Pelecypoda), Allan Hancock Pacific Expedition, 1955, vol. 20, pp. 1–175.

    Google Scholar 

  18. Bernard, F.R., Catalogue of the living Bivalvia of the Eastern Pacific Ocean: Bering Strait to Cape Horn, Spec. Publ. Can. Fish. Aquat. Sci., 1983, vol. 61, p. 102.

    Google Scholar 

  19. Moore, D.R., The little Bivalvia Planktomya unmasked, Anal. Inst. Invest. Mar. Punta Betin, 1983, vol. 13, pp. 123–132.

    Google Scholar 

  20. Kafanov, A.I., Subfamily Mytilinae Rafinesque, 1815 (Bivalvia, Mytilidae) in the Cenozoic of the Northern Pacific, in Fauna i raspredelenie mollyuskov: Severnaya Patsifika i Polyarnyi bassein (Fauna and Distribution of Mollusks: North Pacific and the Polar Basin), Vladivostok: Dalnevostochnyi Nauchnyi Tsentr Akademii Nauk SSSR, 1987, pp. 65–103.

    Google Scholar 

  21. Habe, T., Systematics of Mollusca in Japan: Bivalvia and Scaphopoda, Tokyo: Hokuryukan, 1977.

    Google Scholar 

  22. Iredale, T., Mollusca, part 1, Great Barrier Reef Expedition: Scientific Report, 1928–1929, London: British Museum of Natural History, 1939, vol. 5, no. 6, pp. 209–425.

    Google Scholar 

  23. Carter, J.G., Altaba, C.R., and Anderson, L.C., Paleontological Contributions: A Synoptical Classification of the Bivalvia (Mollusca), Kansas: Univ. Kansas, 2011. http://paleo.ku.edu/contributions. http://hdl.handle. net/1808/8287.

    Google Scholar 

  24. Starobogatov, A.I., Morphological basis for phylogeny and classification of Bivalvia, Ruthenica, 1992, vol. 2, no. 1, pp. 1–25.

    Google Scholar 

  25. Coan, E.V., Scott, P.V., and Bernard, F.R., Bivalve Seashells of Western North America: Marine Bivalve Mollusks from Arctic Alaska to Baja California, Santa Barbara: Santa Barbara Museum of Natural History, 2000, pp. 153–190.

    Google Scholar 

  26. Morals, L. and Svensen, R.L., Bivalve Seashells of Western North America, Valentich, C. and Bernard., S., Eds., Santa Barbara: Santa Barbara Museum of Natural History, 2001. http://www.sbnature.org/atlas/bivbook.htm or psadeghian@sbnature2.org.

    Google Scholar 

  27. Alasaad, S., Rossi, L., Maione, S., et al., HotSHOT Plus ThermalSHOCK, a new and efficient technique for preparation of PCR-quality mite genomic DNA, Parasitol. Res., 2008, vol. 103, pp. 1455–1457. http://dx.doi.org/10.1007/s00436-008-1127-9.

    Article  PubMed  CAS  Google Scholar 

  28. Giribet, G., Carranza, S., Baguna, J., et al., First molecular evidence for the existence of a Tardigrada C Arthropoda clade, Mol. Biol. Evol., 1996, vol. 13, p. 7684.

    Article  Google Scholar 

  29. Colgan, D., Mclauchlan, A., Wilson, G.D.F., et al., Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution, Aust. J. Zool., 1998, vol. 46, pp. 419–437.

    Article  Google Scholar 

  30. Bellocq, J.G., Ferte, H., Depaqiut, J., et al., Phylogeny of the Trichostrongylina (Nematoda) inferred from 28S rDNA sequences, Mol. Phylogenet. Evol., 2001, vol. 19, pp. 430–442.

    Article  CAS  Google Scholar 

  31. Sonnenberg, R., Nolte, A.W., and Tauts, D., An evaluation of LSU rDNA D1-D2 sequences for their use in species identification, Front. Zool., 2007, vol. 4, p. 6. doi 10.1186/1742-9994-4-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Hall, T.A., BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows95/98/NT, Nucleic Acids Symp. Ser., 1999, vol. 41, pp. 95–98.

    CAS  Google Scholar 

  33. Tamura, K., Stecher, G., Peterson, D., et al., MEGA6: molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol., 2013, vol. 30, pp. 2725–2729. doi 10.1093/molbev/mst197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Hall, B., Phylogenetic Trees Made Easy: A How-To Manual for Molecular Biologists, Sunderland: Sinauer, 2001.

    Google Scholar 

  35. Kartavtsev, Y.Ph., Sharina, S.N., Saitoh, K., et al., Phylogenetic relationships of Russian far eastern flatfish (Pleuronectiformes, Pleuronectidae) based on two mitochondrial gene sequences, Co-1 and Cyt-b, with inferences in order phylogeny using complete mitogenome data, Mitochondrial DNA, 2014, vol. 27, no. 1, pp. 667–678.

    Google Scholar 

  36. Kartavtsev, Yu.Ph., Batishcheva, N., Bogutskaya, N.G., et al., Molecular systematics research, DNA barcoding of Altai Osmans, Oreoleuciscus (Pisces, Cyprinidae, Leuciscinae), and nearest relatives, inferred from sequences of cytochrome b (Cyt-b), cytochrome oxidase c (Co-1), and complete mitochondrial genome, Mitochondrial DNA, 2016. http://dx.doi.org/10.3109/24701394.2016.1149822.

    Google Scholar 

  37. Ronquist, F., Teslenko, M., Mark, P.V.D., et al., MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space, Syst. Biol., 2012, vol. 61, no. 3, pp. 539–542. doi 10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  38. STATISTICA for Windows (Data Analysis Software System), Version 6, Tulsa: StatSoft, 2006. www.statstsoft. com.

  39. Kafanov, A.I., System of subfamily Mytilinae (Bivalvia, Mytilidae), in Morfologiya, sistematika, filogeniya i ekogenez dvustvorchatykh mollyuskov (Morphology, Taxonomy, Phylogeny and Ecogenesis of Bivalve Molluscs), Moscow: Nauka, 1984, pp. 43–45.

    Google Scholar 

  40. Bieler, R., Carter, J.G., and Coan, E.V., Classification of bivalve families, Malacologia, 2010, vol. 52, no. 2, pp. 113–133.

    Google Scholar 

  41. Chichvarkhin, A.Yu., Kartavtsev, Yu.F., and Kafanov, A.I., Genetic relationships among some species of Mytilidae (Mollusca: Bivalvia) from the Northern Pacific Ocean, Russ. J. Genet., 2000, vol. 36, no. 9, pp. 1003–1016.

    CAS  Google Scholar 

  42. Vainola, R. and Strelkov, P., Mytilus trossulus in northern Europe, Mar. Biol., 2011, vol. 158, no. 4, pp. 817–833.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Katolikova, M., Khaitov, V., and Väinölä, R., Genetic, ecological and morphological distinctness of the blue mussels Mytilus trossulus Gould and M. edulis L. in the White Sea, PLoS One, 2016, vol. 11, no. 4, pp. 1–25.

    Article  CAS  Google Scholar 

  44. Zbawicka, M., Burzynґski, A., Skibinski, D., and Wenne, R., Scottish Mytilus trossulus mussels retain ancestral mitochondrial DNA: complete sequences of male and female mtDNA genomes, Gene, 2010, vol. 456, pp. 45–53.

    Article  PubMed  CAS  Google Scholar 

  45. Zbawicka, M., Wenne, R., and Burzyński, A., Mitogenomics of recombinant mitochondrial genomes of Baltic Sea Mytilus mussels, Mol. Genet. Genomics, 2014, vol. 289, pp. 1275–1287.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Goto, T., Tamate, H., and Hanzawa, N., Phylogenetic characterization of three morphs of mussels (Bivalvia, Mytilidae) inhabiting isolated marine environments in Palau Islands, Zool. Sci., 2011, vol. 28, no. 8, pp. 568–579.

    PubMed  CAS  Google Scholar 

  47. Kartavtsev, Yu.F., Katolikova, M.V., Sharina, S.N., et al., A population genetic study of the hybrid zone of Mytilus trossulus Gould, 1850 and an introduced species, M. galloprovincialis Lamarck, 1819, (Bivalvia: Mytilidae) in Peter the Great Bay in the Sea of Japan, Russ. J. Mar. Biol., 2014, vol. 40, no. 3, pp. 208–216. https://doi.org/10.1134/S1063074014030055.

    Google Scholar 

  48. Kartavtsev, Y.P. and Lee, J.-S., Analysis of nucleotide diversity at genes Cyt-b and Co-1 on population, species, and genera levels, Russ. J. Genet., 2006, vol. 42, no. 4, pp. 341–362.

    Article  CAS  Google Scholar 

  49. Kartavtsev, Yu.F., Genetic divergence of species and other taxa: geographic species-formation and genetic paradigma of Neo-Darwinism at work, Usp. Sovrem. Biol., 2013, no. 5, pp. 419–451.

    Google Scholar 

  50. Kartavtsev, Y.Ph., Sequence divergence at mitochondrial genes in animals: applicability of DNA data in genetics of speciation and molecular phylogenetics, Mar. Genomics, 2011, vol. 49, pp. 71–81.

    Article  Google Scholar 

  51. Kartavtsev, Y.Ph., Sequence divergence at Co-1 and Cyt-b mtDNA on different taxonomic levels and genetics of speciation in animals, Mitochondrial DNA, 2011, vol. 2, no. 3, pp. 55–65.

    Article  CAS  Google Scholar 

  52. Kartavtsev, Y.Ph., Sequence diversity at Cyt-b and Co-1 mtDNA genes in animal taxa proved Neo-Darwinism, J. Phylogenet. Evol. Biol., 2013, vol. 1, no. 4, pp. 1–5.

    Article  CAS  Google Scholar 

  53. Hedges, S.B., Marin, J., Suleski, M., et al., Tree of life reveals clock-like speciation and diversification, Mol. Biol. Evol., 2015, vol. 32, pp. 835–845.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Nei, M., Molecular Evolutionary Genetics, New York: Columbia University Press, 1987.

    Google Scholar 

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Authors and Affiliations

  1. National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, 690041, Russia

    Yu. Ph. Kartavtsev, S. N. Sharina, A. Yu. Chichvarkhin, O. V. Chichvarkhina, N. A. Masalkova & K. A. Lutaenko

  2. Far Eastern Federal University, Vladivostok, 690095, Russia

    Yu. Ph. Kartavtsev & S. N. Sharina

  3. State University of São Paulo, São Paulo, Brazil

    C. Oliveira

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  1. Yu. Ph. Kartavtsev
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  2. S. N. Sharina
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  3. A. Yu. Chichvarkhin
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Correspondence to Yu. Ph. Kartavtsev.

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Original Russian Text © Yu.Ph. Kartavtsev, S.N. Sharina, A.Yu. Chichvarkhin, O.V. Chichvarkhina, N.A. Masalkova, K.A. Lutaenko, C. Oliveira, 2018, published in Genetika, 2018, Vol. 54, No. 6, pp. 639–660.

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Kartavtsev, Y.P., Sharina, S.N., Chichvarkhin, A.Y. et al. Genetic Divergence of Mussels (Mollusca, Mytilidae) Based on the 28S rRNA, 18S rRNA, and H3 Nuclear Gene Sequences. Russ J Genet 54, 652–669 (2018). https://doi.org/10.1134/S1022795418060078

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