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The taxonomic position of Asian Holopedium (Crustacea: Cladocera) confirmed by morphological and genetic analyses

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Abstract

The cladoceran Holopedium gibberum Zaddach, 1855 (Ctenopoda: Holopediidae) was once thought to occur broadly in the northern hemisphere, but its cryptic sister species was recently separated from H. gibberum sensu stricto (s.s.) as a new species, Holopedium glacialis. In East Asia, although “H. gibberum” occurrence has been recorded in many water bodies, the identity of the surveyed populations has rarely been confirmed via molecular analyses. Thus, it is unclear whether it is actually H. gibberum s.s. or H. glacialis that is distributed in East Asia. We used DNA-barcoding techniques to check the taxonomic status of Holopedium samples collected in Japan. We sequenced mitochondrial cytochrome c oxidase subunit 1 (mtCOI) and nuclear 18S ribosomal DNA (nr18S) of Japanese Holopedium and compared the results with those of H. gibberum s.s. collected in Norway and H. glacialis collected in Canada. The mtCOI sequence divergences between Norwegian H. gibberum s.s. and Japanese Holopedium were at most 2.4%, which was within the degree of intraspecific differentiation in cladocerans. Norwegian H. gibberum s.s. and Japanese Holopedium shared identical nr18S haplotypes. Individuals of Canadian H. glacialis were genetically different from those of Japanese Holopedium. We therefore concluded that Japanese Holopedium can be identified as H. gibberum s.s.

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References

  • Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA Genes. PLoS One 4:e6372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baloch WA, Maeda H, Saisho T (1998) Seasonal abundance and vertical distribution of zooplankton in Lake Ikeda, southern Japan. Microbes Environ 13:1–8

    Article  Google Scholar 

  • Ban S, Makino W, Sakano H, Haruna H, Ueda H (2013) Annual variation in biomass and the community structure of crustacean zooplankton over 5 years in Lake Toya, Japan. Limnology 14:59–70

    Article  Google Scholar 

  • Belyaeva M, Taylor DJ (2009) Cryptic species within the Chydorus sphaericus species complex (Crustacea: Cladocera) revealed by molecular markers and sexual stage morphology. Mol Phylogenet Evol 50:534–546

    Article  CAS  PubMed  Google Scholar 

  • Costa FO, deWaard JR, Boutillier F, Ratnasingham S, Dooh ST, Hajibabaei M, Hebert PDN (2007) Biological identifications through DNA barcodes: the case of the Crustacea. Can J Fish Aquat Sci 64:272–295

    Article  CAS  Google Scholar 

  • Cox JA, Hebert PDN (2001) Colonization, extinction, and phylogeographic patterning in a freshwater crustacean. Mol Ecol 10:371–386

    Article  CAS  PubMed  Google Scholar 

  • Crease TJ, Colbourne JK (1998) The unusually long small-subunit ribosomal RNA of the Crustacean, Daphnia pulex: sequence and predicted secondary structure. J Mol Evol 46:307–313

    Article  CAS  PubMed  Google Scholar 

  • Crease TJ, Taylor DJ (1998) The origin and evolution of variable-region helices in V4 and V7 of the small-subunit ribosomal RNA of Branchiopod crustaceans. Mol Biol Evol 15:1430–1446

    Article  CAS  PubMed  Google Scholar 

  • Cristescu ME (2014) From barcoding single individuals to metabarcoding biological communities: towards an integrative approach to the study of global biodiversity. Trends Ecol Evol 29:566–571

    Article  PubMed  Google Scholar 

  • De Melo R, Hebert PDN (1994) A taxonomic reevaluation of North American Bosminidae. Can J Zool 72:1808–1825

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Frey DG (1982) Questions concerning cosmopolitanism in Cladocera. Arch Hydrobiol 93:484–502

    Google Scholar 

  • Ha J-Y, Hanazato T, Chang K-H, Jeong K-S, Kim D-K (2015) Assessment of the lake biomanipulation mediated by piscivorous rainbow trout and herbivorous daphnids using a self-organizing map: a case study in Lake Shirakaba, Japan. Ecol Inform 29:182–191

    Article  Google Scholar 

  • Hanazato T, Nohara S (1992) Seasonal succession and vertical distribution of zooplankton in Lake Ozenuma. Jpn J Limnol 53:55–63

    Article  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Hebert PDN, Ratnasingham S, de Waard JR (2003a) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B 270:S96–S99

    CAS  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SF, de Waard JR (2003b) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321

    Article  CAS  Google Scholar 

  • Ishida S, Taylor DJ (2007) Quaternary diversification in a sexual Holarctic zooplankter, Daphnia galeata. Mol Ecol 16:569–582

    Article  PubMed  Google Scholar 

  • Ishida S, Kotov AA, Taylor DJ (2006) A new divergent lineage of Daphnia (Cladocera: Anomopoda) and its morphological and genetical differentiation from Daphnia curvirostris Eylmann, 1887. Zool J Linn Soc 146:385–405

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Korovchinsky NM (1992) Sididae and Holopedidae (Crustacea: Daphniiformes). SPB Academic Publishing, Amsterdam

    Google Scholar 

  • Korovchinsky NM (2005) New species of Holopedium Zaddach, 1855 (Crustacea: Claocera: Ctenopoda) from Greenland. J Limnol 64:103–112

    Article  Google Scholar 

  • Korovchinsky NM (2006) The Cladocera (Crustacea: Branchiopoda) as a relict group. Zool J Linnean Soc 147:109–124

    Article  Google Scholar 

  • Korovchinsky NM (2009) The genus Leptodora Lillijeborg (Crustacea: Branchiopoida: Cladocera) is not monotypic: description of a new species from the Amur River basin (Far East of Russia). Zootaxa 2120:39–52

    Article  Google Scholar 

  • Kotov AA, Taylor DJ (2019) Contrasting endemism in pond-dwelling cyclic parthenogenesis: the Daphnia curvirostris species group (Crustacea: Cladocera). Sci Rep 9:6812

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kotov AA, Ishida S, Taylor DJ (2006) An assessment of species diversity in the Daphnia curvirostris (Crustacea: Cladocera) complex with phylogenetic evidence for the independent origin of neckteeth. J Plankton Res 28:1067–1079

    Article  Google Scholar 

  • Kotov AA, Ishida S, Taylor DJ (2009) Revision of the genus Bosmina Baird, 1845 (Cladocera: Bosminidae), based on evidence from male morphological characters and molecular phylogenies. Zool J Linn Soc 156:1–51

    Article  Google Scholar 

  • Kotov AA, Karabanov DP, Bekker EI, Neterina TV, Taylor DJ (2016) Phylogeography of the Chydorus sphaericus group (Cladocera: Chydoridae) in the Northern Palearctic. PLoS One 11:e0168711

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lakatos C, Urabe J, Makino W (2015) Cryptic diversity of Japanese Diaphanosoma (Crustacea: Cladocera) revealed by morphological and molecular assessments. Inland Waters 5:253–262

    Article  Google Scholar 

  • Makino W, Tanabe AS (2009) Extreme population genetic differentiation and secondary contact in the freshwater copepod Acanthodiaptomus pacificus in the Japanese Archipelago. Mol Ecol 18:3699–3713

    Article  CAS  PubMed  Google Scholar 

  • Makino W, Ohtsuki H, Urabe J (2013) Finding copepod footprints: a protocol for molecular identification of diapausing eggs in lake sediments. Limnology 14:269–282

    Article  Google Scholar 

  • Makino W, Maruoka N, Nakagawa M, Takamura N (2017) DNA barcoding of freshwater zooplankton in Lake Kasumigaura, Japan. Ecol Res 32:481–493

    Article  CAS  Google Scholar 

  • Makino W, Tanabe AS, Urabe J (2018) The fauna of freshwater calanoid copepods in Japan in the early decades of the 21st Century: implications for the assessment and conservation of biodiversity. Limnol Oceanogr 63:758–772

    Article  Google Scholar 

  • Mills S, Alcántara-Rodríguez JA, Ciros-Pérez J, Gómez A, Hagiwara A, Galindo KH, Walsh EJ et al (2017) Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) trough DNA taxonomy. Hydrobiologia 796:39–58

    Article  CAS  Google Scholar 

  • Mizuno T, Takahashi E (eds) (2000) An illustrated guide to freshwater zooplankton in Japan (in Japanese). Tokai University Press, Tokyo

    Google Scholar 

  • Pace ML (1986) An empirical analysis of zooplankton community size structure across lake trophic gradients. Limnol Oceanogr 31:45–55

    Article  Google Scholar 

  • Petrusek A, Černý M, Audenaert E (2004) Large intercontinental differentiation of Moina micrura (Crustacea: Anomopoda): one less cosmopolitan cladoceran? Hydrobiologia 526:73–81

    Article  Google Scholar 

  • Porter TM, Hajibabaei M (2018) Automated high throughput animal CO1 metabarcode classification. Sci Rep 8:4226

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org/

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rowe CD, Adamovicz SJ, Hebert PDN (2007) Three new cryptic species of the freshwater zooplankton genus Holopedium (Crustacea: Branchiopoda: Ctenopoda), revealed by genetic methods. Zootaxa 1656:1–49

    Article  Google Scholar 

  • Somervo P, Yu DW, Xu CCY, Ji Y, Hultman J, Wirta H, Ovaskainen O (2017) Quantifying uncertainty of taxonomic placement in DNA barcoding and metabarcoding. Methods Ecol Evol 8:397–408

    Google Scholar 

  • Stefanni S, Stankovic D, Borme D, de Olazabal A, Juretic T, Pallavicini A, Tirelli V (2018) Multi-marker metabarcording approach to study mesozooplankton at basin scale. Sci Rep 8:12085

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanabe AS (2007) KAKUSAN: a computer program to automate the selection of a nucleotide substitution model and the configuration of a mixed model on multilocus data. Mol Ecol Notes 7:962–964

    Article  CAS  Google Scholar 

  • Tanabe AS, Nagai S, Hida K, Yasuike M, Fujiwara A, Nakamura Y, Katakura S et al (2016) Comparative study of the validity of three regions of the18S-rRNA gene for massively parallel sequencing-based monitoring of the planktonic eukaryote community. Mol Ecol Res 16:402–414

    Article  CAS  Google Scholar 

  • Tanaka M (1992) Nihon kosho-shi (Records of Japanese lakes). Nagoya University Press, Nagoya (in Japanese)

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urabe J, Ishida S, Nishimoto M, Weider LW (2003) Daphnia pulicaria, a zooplankton species that suddenly appeared in 1999 in the offshore zone of Lake Biwa. Limnology 4:35–41

    Article  Google Scholar 

  • Weider LJ, Hobaek A, Colbourne J, Crease TJ, Dufresne F, Hebert PDN (1999) Holarctic phylogeography of an asexual species complex. I. Mitochondrial DNA variation in Arctic Daphnia. Evolution 53:777–792

    Article  PubMed  Google Scholar 

  • Xu S, Hebert PDN, Kotov AA, Cristescu ME (2009) The noncosmopolitanism paradigm of freshwater zooplankton: insights from the global phylogeography of the predatory cladoceran Polyphemus pediculus (Linnaeus, 1761) (Crustacea, Onychopoda). Mol Ecol 18:5161–5179

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Han B-P, Van Damme K, Vierstaete A, Vanfleteren JR, Dumont HJ (2011) Biogeography and evolution of the Holarctic zooplankton genus Leptodora (Crustacea: Branchiopoda: Haplopoda). J Biogeogr 38:359–370

    Article  Google Scholar 

  • Yang J, Zhang X, Xie Y, Song C, Zhang Y, Yu H, Burton GA (2017) Zooplankton community profiling in a eutrophic freshwater ecosystem-Lake Tai basin by DNA metabarcoding. Sci Rep 7:1773

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zuykova EI, Simonov EP, Bochkarev NA, Taylor DJ, Kotov AA (2018a) Resolution of the Daphnia umbra problems (Crustacea: Cladocera) using an integrated taxonomic approach. Zool J Linn Soc 184:969–998

    Google Scholar 

  • Zuykova EI, Simonov EP, Bochkarev NA, Abramov SA, Sheveleva NG, Kotov AA (2018b) Contrasting phylogeographic patterns and demographic history in closely related species of Daphnia longispina group (Crustacea: Cladocera) with focus on North-Eastern Eurasia. PLoS One 13:e0207347

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

Marcia Kyle (Norwegian University of Life Sciences) and Tom Andersen (University of Oslo) collected Norwegian Holopedium specimens, and Paul Frost, Andrea Conine, and Clay Prater (Trenton University) collected Canadian Holopedium specimens. We are truly grateful for their very kind support. The present study was also supported by grants from the Japan Society for the Promotion of Science (16770011, 19770010, 23570015, 15H02380, 15K07211, and 18K06407); by funds from the Ministry of the Environment, Japan (the Environment Research and Technology Development Fund, 4-1602); by funds from the Water Resources Environment Technology Center (2008-06, and 2018-03) to WM; and by grants from the Japan Society for the Promotion of Science (25291094 and 16H02522) and the Ministry of the Environment, Japan (the Environment Research and Technology Development Fund, D-1002) to JU.

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  1. Graduate School of Life Sciences, Tohoku University, 6-3 Aramaki Aza Aoba, Sendai, Miyagi, 980-8578, Japan

    Ayaka Yamamoto, Wataru Makino & Jotaro Urabe

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  1. Ayaka Yamamoto
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Correspondence to Wataru Makino.

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Yamamoto, A., Makino, W. & Urabe, J. The taxonomic position of Asian Holopedium (Crustacea: Cladocera) confirmed by morphological and genetic analyses. Limnology 21, 97–106 (2020). https://doi.org/10.1007/s10201-019-00585-z

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