Abstract—
Data on the species diversity, morphological variability, genetic structure, phylogeny, and phylogeography of the D. longispina s. l. group from water bodies of southern Siberia are summarized. The integrated approach involves traditional morphological studies, an analysis of body shape variability using geometric morphometrics, and study of the genetic variability based on mitochondrial (12S, 16S, ND2) and nuclear (ITS2) markers. This approach allows us to identify several forms/species within the genus Daphnia that are new and endemic to the fauna of Russia, to describe some distinctive features of their morphology, to reconstruct phylogenetic relationships within the D. longispina s. l. group, and to elucidate the distribution ranges of species, both common and rare. The study of the variability of mitochondrial DNA genes provided the opportunity to propose and substantiate the hypothesis that various forms/species of this cladoceran group could have passed through different evolutionary scenarios across the territory of northern Eurasia.
Similar content being viewed by others
REFERENCES
Adamowicz, S.J., Petrusek, A., Colbourne, J.K., Hebert, P.D.N., and Witt, J.D.S., The scale of divergence: a phylogenetic appraisal of intercontinental allopatric speciation in a passively dispersed freshwater zooplankton genus, Mol. Phylogenet. Evol., 2009, vol. 50, pp. 423–436.
Arzhannikov, S.G., Alekseev, S.V., Glyzin, A.V., Razmakhnina, T.B., and Orlova, L.A., Natural situation in the Holocene in the western part of the Todzha depression as exemplified by the Merzlyi Yar section, in Problemy rekonstruktsii klimata i prirodnoi sredy Golotsena i Pleistotsena Sibiri (Problems of Reconstruction of the Climate and Natural Environment of the Holocene and Pleistocene of Siberia), Novosibirsk: Izd. Inst. Arkheol. Etnogr. Sib. Otd. Ross. Akad. Nauk, 2000, no. 2, pp. 18–29.
Ballinger, M.J., Bruenn, J.A., Kotov, A.A., and Taylor, D.J., Selectively maintained paleoviruses in Holarctic water fleas reveal an ancient origin for phleboviruses, Virology, 2013, vol. 446, pp. 276–282.
Bekker, E.I., Karabanov, D.P., Galimov, Y.R., and Kotov, A.A., DNA barcoding reveals high cryptic diversity in the North Eurasian Moina species (Crustacea: Cladocera), PLoS One, 2016, vol. 11. e0161737. https://doi.org/10.1371/journal.pone.0161737
Bekker, E.I., Karabanov, D.P., Galimov, Y.R., Haag, C.R., Neretina, T.V., and Kotov, A.A., Phylogeography of Daphnia magna Straus (Crustacea: Cladocera) in Northern Eurasia: evidence for a deep longitudinal split between mitochondrial lineages, PLoS One, 2018, vol. 13. e0194045. https://doi.org/10.1371/journal.pone.0194045
Belyaeva, M. and Taylor, D.J., Cryptic species within the Chydorus sphaericus species complex (Crustacea: Cladocera) revealed by molecular markers and sexual stage morphology, Mol. Phylogenet. Evol., 2009 vol. 50, pp. 534–546.
Benzie, J.A.H., The genus Daphnia (including Daphniopsis) (Anomopoda: Daphniidae), in Guides to the Identification of the Microinvertebrates of the Continental Waters of the World, 2005, vol. 21, pp. 1–376.
Bochkarev, N.A., Zuykova, E.I., and Katokhin, A.V., Morphology and mitochondrial dna variation of the Siberian whitefish Coregonus lavaretus pidschian (Gmelin) in the upstream water bodies of the Ob and Yenisei rivers, J. Evol. Ecol., 2011, vol. 25, pp. 557–572.
Bolotov, I.N., Kondakov, A.V., Konopleva, E.S., Vikhrev, I.V., Aksenova, O.V., Aksenov, A.S., et al., Integrative taxonomy, biogeography and conservation of freshwater mussels (Unionidae) in Russia, Sci. Rep., 2020, vol. 10, p. 3072. https://doi.org/10.1038/s41598-020-59867-7
Di Capua, I., Maffucci, F., Pannone, R., Mazzocchi, M.G., Biffali, E., et al., Molecular phylogeny of Oncaeidae (Copepoda) using nuclear ribosomal internal transcribed spacer (ITS rDNA), PLoS One, 2017, vol. 12, no. 4. e0175662. https://doi.org/10.1371/journal.pone.0175662
Colbourne, J.K. and Hebert, P.D.N., The systematic of North American Daphnia (Crustacea: Anomopoda): a molecular phylogenetic approach, Philos. Trans. R. Soc., B, 1996, vol. 351, pp. 349–360.
Van Damme, K. and Kotov, A.A., The fossil record of the Cladocera (Crustacea: Branchiopoda): evidence and hypotheses, Earth-Sci. Rev., 2016, vol. 163, pp. 162–189.
Darriba, D., Taboada, G.L., Doallo, R., and Posada, D., ModelTest 2: more models, new heuristics and parallel computing, Nat. Methods, 2012, vol. 9, no. 8, p. 772.
Dlouhá, S., Thielsch, A., Kraus, R.H.S., Seda, J., Schwenk, K., et al., Identifying hybridizing taxa within the Daphnia longispina species complex: a comparison of genetic methods and phenotypic approaches, Hydrobiologia, 2010, vol. 643, pp. 107–122.
Francisco, F.O., Nunes-Silva, P., Francoy, T.M., Wittmann, D., Imperatriz-Fonseca, V.L., et al., Morphometrical, biochemical and molecular tools for assessing biodiversity. An example in Plebeia remota (Holmberg, 1903) (Apidae, Meliponini), Insectes Soc., 2008, vol. 55, pp. 231–237.
Frey, D.G., Questions concerning cosmopolitanism in Cladocera, Arch. Hydrobiol., 1982, vol. 93, pp. 484–502.
Frey, D.G., The taxonomy and biogeography of the Cladocera, Hydrobiologia, 1987, vol. 145, pp. 5–17.
Friedrich, J., Dandekar, T., Wolf, M., and Muller, T., ProfDist: a tool for the construction of large phylogenetic trees based on profile distances, Bioinformatics, 2005 vol. 21, pp. 2108–2109.
Garibian, P.G., Neretina, A.N., Klimovsky, A.I., and Kotov, A.A., A new case of west-east differentiation of the freshwater fauna in Northern Eurasia: the Pleuroxus trigonellus species group (Crustacea: Cladocera: Chydoridae), Zootaxa, 2018, vol. 4532, pp. 451–482.
De Gelas, K. and De Meester, L., Phylogeography of Daphnia magna in Europe, Mol. Ecol., 2005, vol. 1, pp. 753–764.
Gießler, S., Morphological differentiation within the Daphnia longispina group, Hydrobiologia, 2001, vol. 442, pp. 55–66.
Gießler, S. and Englbrecht, C.C., Dynamic reticulate evolution in a Daphnia multispecies complex, J. Exp. Zool., A, 2009, vol. 311, pp. 531–549.
Gießler, S., Mader, E., and Schwenk, K., Morphological evolution and genetic differentiation in daphnia species complexes, J. Exp. Biol., 1999, vol. 12, pp. 710–723.
Giri, F. and Collins, P.A., A geometric morphometric analysis of two sympatric species of the family Aeglidae (Crustacea, Decapoda, Anomura) from the La Plata basin, Ital. J. Zool., 2004, vol. 71, pp. 85–88.
Glagolev, S.M., Morphology, taxonomy and geographical distribution of cladocerans of the genus Daphnia of Eurasia, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow: Inst. Evol. Morphol. Ekol. Zhiv. Akad. Nauk SSSR, 1986.
Grandcolas, P., Nattier, R., and Trewick, S., Relict species: a relict concept?, Trends Ecol. Evol., 2014, vol. 29, pp. 655–663.
Grosswald, M.G., Evraziiskie gidrosistemnye katostrofy i oledeneniya Arktiki (Eurasian Hydrosystem Catastrophies and Glaciations in the Arctic), Moscow: Nauchnyi Mir, 1999.
Grosswald, M.G. and Kotlyakov, V.M., The great periglacial runoff system of Northern Asia and its significance for interregional correlations, in Chetvertichnyi period. Paleografiya i litologiya: Sbornik nauchnykh trudov (Quaternary Period. Paleography and Lithology: Collection of Scientific Works), Chisinau: Shtiinitsa, 1989, pp. 5–13.
Hamrová, E., Krajicek, M., Karanovic, T., Černý, M., and Petrusek, A., Congruent patterns of lineage diversity in two species complexes of planktonic crustaceans, Daphnia longispina (Cladocera) and Eucyclops serrulatus (Copepoda), in East European mountain lakes, Zool. J. Linn. Soc., 2012, vol. 166, pp. 754–757.
Huang, Q., Xu, S.L., Xu, L., and Han, B.P., Haplotype diversity and genetic differentiation of dormant and active populations of Daphnia galeata in Liuxihe Reservoir of Guangdong Province, southern China, J. Lake Sci., 2017, vol. 29, pp. 1209–1216.
Ishida, S. and Taylor, D.J., Mature habitats associated with genetic divergence despite strong dispersal ability in an arthropod, BMC Exp. Biol., 2007, vol. 7, no. 52. https://doi.org/10.1186/1471-2148-7-52
Ishida, S. and Taylor, D.J., Quaternary diversification in a sexual Holarctic zooplankter, Daphnia galeata, Mol. Ecol., 2007a, vol. 16, pp. 569–582.
Ishida, S., Takahashi, A., Matsushima, N., Yokoyama, J., Makino, W., et al., The long-term consequences of hybridization between the two Daphnia species, D. galeata and D. dentifera, in mature habitats, BMC Exp. Biol., 2011, vol. 11, no. 209. https://doi.org/10.1186/1471-2148-11-209
Karabanov, D.P., Bekker, E.I., Shiel, R.J., and Kotov, A.A., Invasion of a Holarctic planktonic cladoceran Daphnia galeata Sars (Crustacea: Cladocera) in the Lower Lakes of South Australia, Zootaxa, 2018, vol. 4402, pp. 136–148.
Kirdyasheva, A.G. and Kotov, A.A., Morphology and age variability of Daphnia galeata Sars (Cladocera: Daphniidae) in two adjacent water bodies of the Kola Peninsula, Biol. Bull. (Moscow), 2013, vol. 40, no. 2, pp. 158–168.
Koetschan, C., Forster, F., Keller, A., Schleicher, T., Ruderisch, B., Schwarz, R., et al., The ITS2 database III—sequences and structures for phylogeny, Nucleic Acids Res., 2010, vol. 38, pp. 275–279.
Korovchinsky, N.M., How many species of Cladocera are there?, Hydrobiologia, 1996, vol. 321, pp. 191–204.
Korovchinsky, N.M., The genus Leptodora Lilljeborg (Crustacea: Branchiopoda: Cladocera) is not monotypic: description of a new species from the Amur River basin (Far East of Russia), Zootaxa, 2009, vol. 2120, pp. 39–52.
Kotov, A.A., Morfologiya i filogeniya Anomopoda (Crustacea: Cladocera) (Morphology and Phylogeny of Anomopoda (Crustacea: Cladocera)), Moscow: Tovarishchestvo nauchnykh izdanii KMK, 2013.
Kotov, A.A., A critical review of the current taxonomy of the genus Daphnia O.F. Muller, 1785 (Anomopoda, Cladocera), Zootaxa, 2015, vol. 3911, pp. 184–200.
Kotov, A.A., Faunistic complexes of Cladocera (Crustacea, Branchiopoda) of Eastern Siberia and the Far East of Russia, Zool. Zh., 2016, vol. 95, pp. 748–768.
Kotov, A.A. and Korovchinsky, N.M., First record of fossil Mesozoic ctenopoda (Crustacea, Cladocera), Zool. J. Linn. Soc., 2006, vol. 146, pp. 269–274.
Kotov, A.A. and Sinev, A.Yu., Cladocera (Crustacea, Branchiopoda) of the Zeya River basin (Amur region, Russian Federation). 2. Descriptions of new taxa, Zool. Zh., 2011, vol. 90, pp. 272–284.
Kotov, A.A. and Taylor, D.J., Contrasting endemism in pond-dwelling cyclic parthenogens: the Daphnia curvirostris species group (Crustacea: Cladocera), Sci. Rep., 2019, vol. 9, p. 6812. https://doi.org/10.1038/s41598-019-43281-9
Kotov, A.A., Ishida, S., and Taylor, D.J., A new species in the Daphnia curvirostris (Crustacea: Cladocera) complex from the eastern palearctic with molecular phylogenetic evidence for the independent origin of neckteeth, J. Plankton Res., 2006, vol. 28, pp. 1067–1079.
Kotov, A.A., Karabanov, D.P., Bekker, E.I., Neretina, T.V., and Taylor, D.J., Phylogeography of the chydorus sphaericus group (cladocera: chydoridae) in the northern palearctic, PLoS One, 2016, vol. 11. e0168711. https://doi.org/10.1371/journal.pone.0168711
Kumar, S., Stecher, G., and Tamura, K., MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 2016, vol. 33, pp. 1870–1874.
Ma, X., Petrusek, A., Wolinska, J., Gieβler, S., Zhong, Y., et al., Diversity of the Daphnia longispina species complex in Chinese lakes: a DNA taxonomy approach, J. Plankton Res., 2015, vol. 37, pp. 55–65.
Ma, X., Hu, W., Smilauer, P., Yin, M., and Wolinska, J., Daphnia galeata and D. dentifera are geographically and ecologically separated whereas their hybrids occur in intermediate habitats: a survey of 44 Chinese lakes, Mol. Ecol., 2019, vol. 28, pp. 785–802.
Mangerud, J., Jakobsson, M., Alexanderson, H., Astakhov, V., Clarke, G.K.C., et al., Ice-dammed lakes and rerouting of the drainage of northern Eurasia during the last glaciation, Quat. Sci. Rev., 2004, vol. 23, pp. 1313–1332.
De Meester, L., Gómez, A., Okamura, B., and Schwenk, K., The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms, Acta Oecol., 2002, vol. 23, pp. 121–135.
Möst, M., Petrusek, A., Sommaruga, R., Juracka, P.J., Slusarczyk, M., et al., At the edge and on the top: molecular identification and ecology of Daphnia dentifera and D. longispina in high-altitude Asian lakes, Hydrobiologia, 2012, vol. 715, pp. 51–62.
Nei, M. and Kumar, S., Molecular Evolution and Phylogenetics, New York: Oxford Univ. Press, 2000.
Nilssen, J.P., Hobaek, A., Petrusek, A., and Skage, M., Restoring Daphnia lacustris G.O. Sars, 1862 (Crustacea, Anomopoda): a cryptic species in the Daphnia longispina group, Hydrobiologia, 2007, vol. 594, pp. 5–17.
Perrière, G. and Gouy, M., WWW-Query: an on-line retrieval system for biological sequence banks, Biochimie, 1996, vol. 78, pp. 364–369.
Petrusek, A., Černý, M., Mergeay, J., and Schwenk, K., Daphnia in the Tatra Mountain lakes: multiple colonization and hidden species diversity revealed by molecular markers, Fundam. Appl. Limnol., Arch. Hydrobiol., 2007, vol. 169, pp. 279–291.
Petrusek, A., Hobaek, A., Nilssen, J.P., Skage, M., Cérný, M., et al., A taxonomic reappraisal of the European Daphnia longispina complex (Crustacea, Cladocera, Anomopoda), Zool. Scr., 2008, vol. 37, pp. 507–519.
Petrusek, A., Thielsch, A., and Schwenk, K., Mitochondrial sequence variation suggests extensive cryptic diversity within the Western Palearctic Daphnia longispina complex, Limnol. Oceanogr., 2012, vol. 57, pp. 1838–1845.
Popova, E.V., Petrusek, A., Korinek, V., Mergeay, J., Bekker, E.I., et al., Revision of the Old World Daphnia (Ctenodaphnia) similis group (Cladocera: Daphniidae), Zootaxa, 2016, vol. 161, pp. 1–40.
Rogers, D.C., Kotov, A.A., Sinev, A.Y., Glagolev, S.M., Korovchinsky, N.M., et al., Keys to Palaearctic fauna, chapter 16.2: Arthropoda: class Branchiopoda, in Thorp and Covich’s Freshwater Invertebrates, Thorp, J.H. and Rogers, D.C., Eds., London: Academic, 2019, vol. 4, 4th ed., pp. 643‒724.
Saitou, N. and Nei, M., The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mol. Biol. Evol., 1987, vol. 4, pp. 6–25.
Santamaria, C.A., Mateos, M., DeWitt, T.J., and Hurtado, L.A., Constrained body shape among highly genetically divergent allopatric lineages of the supralittoral isopod Ligia occidentalis (Oniscidea), Ecol. Evol., 1987, vol. 6, pp. 1537–1554.
Schultz, J. and Wolf, M., ITS2 sequence-structure analysis in phylogenetics: a how-to manual for molecular systematics, Mol. Phylogenet. Evol., 2009, vol. 52, pp. 520–523.
Schwenk, K., Junttila, P., Rautio, M., Bastiansen, F., Knapp, J., et al., Ecological, morphological, and genetic differentiation of Daphnia (Hyalodaphnia) from the Finnish and Russian Subarctic, Limnol. Oceanogr., 2004, vol. 49, pp. 532–539.
Schwenk, K., Posada, D., and Hebert, P.D.N., Molecular systematics of European Hyalodaphnia: the role of contemporary hybridization in ancient species, Proc. R. Soc. London, Ser. B, 2000, vol. 267, pp. 1833–1842.
Seibel, P.N., Muller, T., Dandekar, T., and Wolf, M., Synchronous visual analysis and editing of RNA sequence and secondary structure alignments using 4SALE, BMC Res. Notes, 2008, vol. 1, p. 91.
Silva, I.C., Mesquita, N., and Paula, J., Genetic and morphological differentiation of the mangrove crab Perisesarma guttatum (Brachyura: Sesarmidae) along an East African latitudinal gradient, Biol. J. Linn. Soc., 2010, vol. 99, pp. 28–46.
Smirnov, N.N. and Sheveleva, N.G., Chydorus irinae sp. n. (Anomopoda, Chydoridae, Chydorinae) from the Tom River (Amur River basin, Russia), Zool. Zh., 2010, vol. 89, no. 5, pp. 635–638.
Smirnov, N.N., Physiology of the Cladocera, London: Academic, 2017, 2nd ed.
Smirnov, N.N. and Kotov, A.A., On morphological radiation of Cladocera (Crustacea), Invertebr. Zool., 2018, vol. 15, pp. 231–248.
Tamura, K. and Nei, M., Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees, Mol. Biol. Evol., 1993, vol. 10, pp. 512–526.
Taylor, D.J., Hebert, P.D.N., and Colbourne, J.K., Phylogenetics and evolution of the Daphnia longispina group (Crustacea) based on 12S rDNA sequence and allozyme variation, Mol. Phylogenet. Evol., 1996 vol. 5, pp. 495–510.
Taylor, D.J., Sprenger, H.L., and Ishida, S., Geographic and phylogenetic evidence for dispersed nuclear introgression in a daphniid with sexual propagules, Mol. Ecol., 2005, vol. 14, pp. 525–537.
Thielsch, A., Brede, N., Petrusek, A., De Meester, L., and Schwenk, K., Contribution of cyclic parthenogenesis and colonization history to population structure in Daphnia, Mol. Ecol., 2009, vol. 18, pp. 1616–1628.
Thielsch, A., Knell, A., Mohammadyari, A., Petrusek, A., and Schwenk, K., Divergent clades or cryptic species? Mitonuclear discordance in a Daphnia species complex, BMC Exp. Biol., 2017, vol. 17, no. 227. https://doi.org/10.1186/s12862-017-1070-4
Ventura, M., Petrusek, A., Miró, A., Hamrová, E., Buňay, D., et al., Local and regional founder effects in lake zooplankton persist after thousands of years despite high dispersal potential, Mol. Ecol., 2014, vol. 23, pp. 1014–1027.
Vinarski, M.V., Bolotov, I.N., Schniebs, K., Nekhaev, I.O., and Hundsdoerfer, A.K., Endemics or strangers? The integrative re-appraisal of taxonomy and phylogeny of the Greenland Lymnaeidae (Mollusca: Gastropoda), C. R. Biol., 2017, vol. 340, pp. 541–557.
Volkov, I.A. and Kaz’min, S.P., Water runoff of the last glaciation of the north of Eurasia, Geogr. Prir. Resur., 2007, no. 4, pp. 7–10.
Vysotskiy, E.M., Geomorphology of the basin of Teletskoe Lake, in Physical and Geological Environment of Lake Teletskoe, Selegei, V., Dehandschutter, B., Klerkx, J., and Vysotsky, E., Eds., Tervuren: Musee Royal de I Afrigue Centrale Tervuren, 2001, pp. 164–181.
Wiemers, M., Keller, A., and Wolf, M., ITS2 secondary structure improves phylogeny estimation in a radiation of blue butterflies of the subgenus Agrodiaetus (Lepidoptera: Lycaenidae: Polyommatus), BMC Exp. Biol., 2009, vol. 9, no. 300. https://doi.org/10.1186/1471-2148-9-300
Wolf, M., Ruderisch, B., Dandekar, T., and Muller, T., ProfDistS: (Profile-) Distance based phylogeny on sequence-structure alignments, Bioinformatics, 2008, vol. 24, pp. 2401–2402.
Xu, S., Hebert, P.D.N., Kotov, A.A., and Cristescu, M.E., The non-cosmopolitanism paradigm of freshwater zooplankton: insights from the global phylogeography of the predatory cladoceran Polyphemus pediculus (Crustacea, Onychopoda), Mol. Ecol., 2009, vol. 18, pp. 5161–5179.
Xu, L., Lin, Q., Xu, S., Gu, Y., Hou, J., et al., Daphnia diversity on the Tibetan Plateau measured by DNA taxonomy, Ecol. Evol., 2018, vol. 8, pp. 5069–5078.
Yin, M., Wolinska, J., and Gießler, S., Clonal diversity, clonal persistence and rapid taxon replacement in natural populations of species and hybrids of the Daphnia longispina complex, Mol. Ecol., 2010, vol. 19, pp. 4168–4178.
Zuykova, E.I., Identification and phylogeny of cryptic species of the Daphnia longispina complex (Anomopoda, Daphniidae) using ITS2 secondary structure, Russ. J. Genet., 2019, vol. 55, pp. 604–621.
Zuykova, E.I. and Bochkarev, N.A., Population and interspecific morphological variability of species of the genus Daphnia O.F. Müller, 1785 (Cladocera, Daphniidae), Zool. Zh., 2016, vol. 95, pp. 805–814.
Zuykova, E.I., Bochkarev, N.A., Semenova, A.S., and Katokhin, A.V., Morphological differentiation, mitochondrial and nuclear DNA variability between geographically distant populations of Daphnia galeata and Daphnia cucullata (Anomopoda, Daphniidae), J. Sib. Fed. Univ., Biol., 2010, vol. 4, no. 3, pp. 434–453.
Zuykova, E.I., Bochkarev, N.A., and Katokhin, A.V., Molecular genetic identification and phylogeny of Daphnia Species (Crustacea, Cladocera) from water bodies of the Lake Chany basin, Russ. J. Genet., 2013a, vol. 49, pp. 206–213.
Zuykova, E.I., Bochkarev, N.A., and Katokhin, A.V., Identification of the Daphnia species (Crustacea: Cladocera) in the lakes of the Ob and Yenisei river basins: morphological and molecular phylogenetic approaches, Hydrobiologia, 2013b, vol. 715, pp. 135–150.
Zuykova, E.I., Bochkarev, N.A., and Sheveleva, N.G., Genetic polymorphism, distribution of haplotypes, and phylogeny of species of the genus Daphnia (Cladocera: Anomopoda) from some water bodies of Russia based on the results of 16S gene sequencing of mitochondrial DNA, Russ. J. Genet., 2016, vol. 52, pp. 1–13.
Zuykova, E.I., Simonov, E.P., and Bochkarev, N.A., Comparative morphological and genetic analysis of populations and species of the genus Daphnia O.F. Müller, 1785 (Crustacea; Daphniidae) from Lake Glubokoe and Lake Chany, Biol. Bull. (Moscow), 2017, vol. 44, no. 3, pp. 277–289.
Zuykova, E.I., Simonov, E.P., Bochkarev, N.A., Talor, D.J., and Kotov, A.A., Resolution of the Daphnia umbra problem (Crustacea: Cladocera) using an integrated taxonomic approach, Zool. J. Linn. Soc., 2018a, vol. 184, pp. 969–998.
Zuykova, E.I., Simonov, E.P., Bochkarev, N.A., Abramov, S.A., Sheveleva, N.G., and Kotov, A.A., Contrasting phylogeographic patterns and demographic history in closely related species of Daphnia longispina group (Crustacea: Cladocera) with focus on North-Eastern Eurasia, PLoS One, 2018b, vol. 13. e0207347. https://doi.org/10.1371/journal.pone.0207347
Zuykova, E.I., Sheveleva, N.G., and Kotov, A.A., Redescription of Daphnia turbinata Sars, 1903 (Crustacea: Cladocera: Daphniidae), Zootaxa, 2019a, vol. 4658, pp. 317–330.
Zuykova, E.I., Bochkarev, N.A., Talor, D.J., and Kotov, A.A., Unexpected endemism in the Daphnia longispina complex (Crustacea: Cladocera) in Southern Siberia, PLoS One, 2019b, vol. 14. e0221527. https://doi.org/10.1371/journal.pone.0221527
ACKNOWLEDGMENTS
This paper is dedicated to the memory of Nikolai Nikolaevich Smirnov (1928–2019), one of the leaders of the study of crustaceans in the 20th century. We are grateful to the numerous colleagues who provided the zooplankton samples used in these studies.
Funding
This study was supported by the Russian Foundation for Basic Research (project no. 20-04-00610-a). The sequencing of the ITS2 fragment was carried out within the framework of the Program of Basic Scientific Research (FNI) of the State Academies of Sciences for 2013–2020 (project no. VI.51.1.9. AAAA-A16-116121410119-4). Data analysis was carried out with partial support of the state program to improve the competitiveness of the Kazan (Volga Region) Federal University among the world’s leading research and educational centers.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
Additional information
Translated by S. Nikolaeva
Rights and permissions
About this article
Cite this article
Zuykova, E.I., Bochkarev, N.A. & Kotov, A.A. Specific and Genetic Structure of the Daphnia longispina s. l. Complex (Cladocera, Daphniidae) in Water Bodies of Southern Siberia. Biol Bull Russ Acad Sci 48, 880–891 (2021). https://doi.org/10.1134/S1062359021070323
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1062359021070323