Abstract
DNA barcoding, based on sequence diversity in the mitochondrial COI gene, has proven an excellent tool for identifying species in many animal groups. Here, we report the first barcode studies for freshwater zooplankton from Mexico and Guatemala and discuss the taxonomic and biological implications of this work. Our studies examined 61 species of Cladocera and 21 of Copepoda, about 40% of the known fauna in this region. Sequence divergences among conspecific individuals of cladocerans and copepods averaged 0.82% and 0.79%, respectively, while sequence divergences among congeneric taxa were on average 15-20 times as high. Barcodes were successful in discriminating all species in our study, but sequences for Mexican Daphnia exilis overlapped with those of D. spinulata from Argentina. Our barcode data revealed evidence of many species overlooked by current classification systems —for example, based on COI genotypes the Diapahanosoma birgei group appears to include 5 species, while Ceriodaphnia cf. rigaudi, Moina cf. micrura, Mastigodiaptomus albuquerquensis and Mastigodiaptomus reidae all include 2–3 taxa. The barcode results support recent taxonomic revisions, such as recognition of the genus Leberis, and the presence of several species in the D. birgei and Chydorus sphaericus complexes. The present results indicate that DNA barcoding will provide powerful new insights into both the incidence of cryptic species and a better understanding of zooplankton distributions, aiding evaluation of the factors influencing competitive outcomes, and the colonization of aquatic environments.References
Adamowicz, S.J., Hebert, P.D.N. & Marinone, M.C. (2004) Species diversity and endemism in the Daphnia of Argentina: a genetic investigation. Zoological Journal of the Linnean Society, 140(2), 171–205.
Adamowicz, S.J. & Purvis, A. (2005) How many branchiopod crustacean species are there? Quantifying the components of underestimation. Global Ecology and Biogeography, 14(5), 455–468.
Adamowicz, S.J., Menu–Marque, S., Hebert, P.D.N. & Purvis, A. (2007) Molecular systematics and patterns of morphological evolution in the Centropagidae (Copepoda: Calanoida) of Argentina. Biological Journal of the Linnean Society, 90(2), 279–292.
Berner, D.B. (1985) Morphological differentiaton among species in the Ceriodaphnia cornuta complex (Crustacea, Cladocera). Verhandlungen der Internationalen Vereinigung der Limnologie, 22, 3099–3103.
Benzie, J.A.H. (2005) Cladocera: The Genus Daphnia (including Daphniosis). Kenobi Productions & Backhuys Publishers, Ghent, Leiden, 376 pp.
Berner, D.B. (1992) Restricted distribution of Ceriodaphnia quadrangula in North America. Book of Abstracts XXV SIL International Congress, Barcelona, 50.
Boxshall, G.A. & Defaye D. (2008). Global diversity of copepods (Crustacea: Copepoda) in freshwater. Hydrobiologia, 595, 195–207.
Bowman, T.E. (1986) Freshwater Calanoid copepods of the West Indies. Syllogeus, 58, 237–246.
Bucklin, A., Guarnieri, M., Hill, R.S., Bentley, A.M. & Kaartvedt, S. (1999) Taxonomic and systematic assessment of planktonic copepods using mitochondrial COI sequence variation and competitive, species–specific PCR. Hydrobiologia, 401, 239–254.
Bucklin, A., Wiebe, P.H., Smolenack, S.B., Copley, N.J., Beaudet, J.G., Bonner, K.G., Farber–Lorda J. & Pierson, J.J. (2007) DNA barcodes for species identification of euphausiids (Euphausiacea, Crustacea), Journal of Plankton Research 29, 483–493.
Burton, R.S. & Bang–Ning, L. (1994) Nuclear and mitochondrial gene genealogies and allozyme polymorphism across a major phylogeographic break in the copepod Tigriopus californicus. Proceedings of the National Academy of Sciences of the United States of America, 91, 5197–5201.
Cervantes–Martínez, A., Elías–Gutiérrez, M., Gutiérrez–Aguirre, M.A. & Kotov, A.A. (2005) Ecological remarks on Mastigodiaptomus nesus Bowman, 1986 (Copepoda : Calanoida) in a Mexican karstic sinkhole. Hydrobiologia, 542: 95–102.
Chiambeng, G.Y. & Dumont, H.J. (2004) The genus Pleuroxus Baird, 1843 (Crustacea : Anomopoda : Chydoridae) in Cameroon, Central–West Africa. Annales de Limnologie–International Journal of Limnology, 40(3), 211–229.
Costa, F.O., DeWaard, J.R., Boutillier, J., Ratnasingham, S., Dooh, R.T., Hajibabaei, M. & Hebert, P.D.N. (2007) Biological identifications through DNA barcodes: the case of the Crustacea. Canadian Journal of Fisheries and Aquatic Sciences, 64(2), 272–295.
De Melo, R. & Hebert, P.D.N. (1994) A taxonomic reevaluation of North American Bosminidae. Canadian Journal of Zoology, 72, 1808–1825.
Cox, A.J. & Hebert, P.D.N. (2001) Colonization, extinction, and phylogeographic patterning in a freshwater crustacean. Molecular Ecology, 10(2), 371–386.
De Gelas, K. & De Meester, L. (2005) Phylogeography of Daphnia magna in Europe. Molecular Ecology, 14(3), 753–764.
Dumont, H.J. (2006) Morphology and ecology of a group of small, pelagic, tropical Tropocyclops (Crustacea, Copepoda, Cyclopoida), with the description of a new species from South China. Annales de Limnologie–International Journal of Limnology, 42(4), 261–275.
Dumont, H.J. & Pensaert J. (1983) A revision of the Scapholeberinae (Crustacea: Cladocera). Hydrobiologia, 100, 3–45.
Elías–Gutiérrez, M. (1995) Notas sobre los cladóceros de embalses a gran altitud en el Estado de México, México. Anales de la Escuela Nacional de Ciencias Biológicas, 40, 197–214.
Elías–Gutiérrez, M. & Suárez–Morales, E. (2003) Estado actual del conocimiento de los cladoceros de México. In : Barreiro–Güemes, M. T. et al. (Eds.), El Colegio de la Frontera Sur, Universidad Autónoma Metropolitana, Estado de Veracruz, Mexico, 171–183.
Elías–Gutiérrez, M. & Valdez–Moreno, M. (2008) A new cryptic species of Leberis Smirnov, 1989 (Crustacea, Cladocera, Chydoridae) from the Mexican semi–desert region, highlighted by DNA barcoding. Hidrobiologica, 18(1), 63–74.
Elías–Gutiérrez, M., Ciros–Pérez, J., Suárez–Morales, E. & Silva–Briano, M. (1999) The freshwater Cladocera (Orders Ctenopoda & Anomopoda) of Mexico, with comments on selected taxa. Crustaceana, 72(2), 171–186.
Elías–Gutiérrez, M., Kotov, A.A. & Garfias–Espejo, T. (2006) Cladocera (Crustacea: Ctenopoda, Anomopoda) from southern Mexico, Belize and northern Guatemala, with some biogeographical notes. Zootaxa, 1119, 1–27.
Fiers, F., Ghenne, V. & Suárez–Morales, E. (2000) New species of continental cyclopoid copepods (Crustacea, Cyclopoida) from the Yucatan Peninsula, Mexico. Studies on Neotropical Fauna & Environment, 35, 209–251.
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. Molecular Marine Biology and Biotechnology, 3, 294–299.
Forró, L., Korovchinsky, N.M., Kotov, A.A. & Petrusek, A. (2008) Global diversity of cladocerans (Cladocera; Crustacea) in freshwater. Hydrobiologia, 595, 177–184.
Frey, D.G. (1980) On the plurality of Chydorus sphaericus (O.F. Müller) Cladocera, Chydoridae), and designation of a neotype from Sjaelso, Denmark. Hydrobiologia, 69(1–2), 83–123.
Frey, D.G. (1982) Questions concerning cosmopolitanism in Cladocera. Archiv für Hydrobiologie, 93(4), 484–502.
Ganz, H.H. & Burton, R.S. (1995) Genetic diferentiation and reproductive incompatibility among Baja California populations of the copepod Tigriopus californicus. Marine Biology, 123(4), 821–827.
Goulden, C.E. (1968) The systematics and evolution of the Moinidae. Transactions of the American Microscopical Society, 58, 1–101.
Grimaldo–Ortega, D., Elías–Gutiérrez, M. & Camacho–Lemus, M. (1998) Additions to Mexican freshwater copepods with the description of the female Leptodiaptomus mexicanus (Marsh). Journal of Marine Systems, 15, 381–390.
Gutiérrez–Aguirre, M. & Suárez–Morales, E. (2000) New range extension of the Diaptomid copepod Prionodiaptomus colombiensis Thiébaud, 1912 (Copepoda, Calanoida) with complementary description of this species. Zoosystema, 22(3), 507–516.
Hajibabaei, M., DeWaard, J.R., Ivanova, N.V., Ratnasingham, S., Dooh, R., Kirk, S.L., Mackie, P.M. & Hebert, P.D.N. (2005) Critical factors for assembling a high volume of DNA barcodes. Philosophical Transactions of the Royal Society of London Series B–Biological Sciences, 360, 1959–1967.
Havel, J.E., Colbourne, J.K. & Hebert, P.D.N. (2000) Reconstructing the history of intercontinental dispersal in Daphnia lumholtzi by use of genetic markers. Limnology and Oceanography, 45(6), 1414–1419.
Hebert, P.D.N. & Finston, T.L. (1996) A taxonomic reevaluation of North American Daphnia (Crustacea: Cladocera) II. New species in the Daphnia pulex group from the south–central United States and Mexico. Canadian Journal of Zoology, 74(4), 632–653.
Hebert, P.D.N., Cywinska, A., Ball, S.L. & DeWaard, J.R. (2003a) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B–Biological Sciences, 270(1512), 313–321.
Hebert, P.D.N., Witt, J.D.S. & Adamowicz, S.J. (2003b) Phylogeographical patterning in Daphnia ambigua: Regional divergence and intercontinental cohesion. Limnology and Oceanography, 48(1), 261–268.
Hebert, P.D.N., Stoeckle, M.Y., Zemlak, T.S. & Francis, C.M. (2004) Identification of birds through DNA barcodes. PLoS Biology, 2(10), 1657–1663.
Hogg, I.D. & Hebert, P.D.N. (2004) Biological identification of springtails (Hexapoda: Collembola) from the Canadian Arctic, using mitochondrial DNA barcodes. Canadian Journal of Zoology, 82(5), 749–754.
Ivanova, N.V., DeWaard, J.R. & Hebert, P.D.N. (2006) An inexpensive, automation–friendly protocol for recovering high–quality DNA. Molecular Ecology Notes, 6, 998–1002.
Kiefer, F. (1938) Ruderfubkrebse (Crust. Cop.) aus Mexico. Zoologischer Anzeiger, 115(9), 274–279.
Kimura, M. (1980) A simple method of estimating evolutionary rate of base substitutions through comparative studies. Journal of Molecular Evolution, 16, 111–120.
Korinek, V. (1981) Diaphanosoma birgei n. sp. (crustacea, Cladocera). A new species from America and its widely distributed subspecies Diaphanosoma birgei ssp. lacustris n.ssp. Canadian Journal of Zoology, 59, 1115–1121.
Korovchinsky, N.M. (1992) Sididae and Holopediidae. SPB Academic Publishing, Amsterdam, 82 p.
Korovchinsky, N.M. (2002) Description of two new species of Diaphanosoma Fischer, 1850 (Crustacea, Branchiopoda, Sididae) from the United States and Canada and species richness of the genus in North America. Hydrobiologia, 489(1–3), 45–54.
Korovchinsky, N.M. (2005) Two new species of Diaphanosoma Fischer, 1850 (Crustacea: Branchiopoda: Cladocera) from the United States. International Review of Hydrobiology, 90(2), 201–208.
Kotov, A.A., Garfias–Espejo, T. & Elías–Gutiérrez, M. (2004) Separation of two Neotropical species: Macrothrix superaculeata (Smirnov, 1982) versus M. elegans Sars, 1901 (Macrothricidae, Anomopoda, Cladocera). Hydrobiologia, 517(1–3), 61–88.
Kumar, S., Tamura, K. & Masatoshi, N. (2004) MEGA3: Integrated Software for Molecular Evolutionary Genetics Analysis and Sequence Alignment. Briefings in Bioinformatics, 5, 150–163.
Kurz, W. (1874) Dodekas neuer Cladoceren nebst einer kurzen Üebersicht der Cladocerenfauna Bühmens. Sitzungsberichte der Akademie der Wissenschaften der ddr. Mathematik–Naturwissenschaften: Technik, 70, 7–88.
Lefebure, T., Douady, C. J., Gouy, M. & Gibert, J. (2006) Relationship between morphological taxonomy and molecular divergence within Crustacea: Proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution, 40(2), 435–447.
Limp, R.P. & Fernando, C.H. (1978) Production of Cladocera inhabiting the vegetated littoral of Pinehurst Lake, Ontario, Canada. Verhandlungen der Internationalen Vereinigung der Limnologie, 1, 225–231.
Marsh, C.D. (1907) A revision on the North American species of Diaptomidae. Transactions of the Wisconsin Academy of Sciences, Arts and Letters, 15, 381–516.
Megard, R.O. (1967) Three new species of Alona (Cladocera, Chydoridae) from the United States. Internationale Revue der Gesamten Hydrobiologie, 52(1), 37–50.
Montiel-Martínez A., Ciros-Pérez J., Ortega-Mayagoitia E. & Elías-Gutiérrez M. (2008). Morphological, ecological, reproductive and molecular evidence for Leptodiaptomus garciai (Osorio-Tafall 1942) as a valid endemic species. Journal of Plankton Research, doi, 10.1093/plankt/fbn067.
Moline, A.B., Shuster, S.M., Hendrickson, D.A. & Marks, J.C. (2004) Genetic variation in a desert aquatic snail (Nymphophilus minckleyi) from Cuatro Cienegas, Coahuila, Mexico. Hydrobiologia, 522(1–3), 179–192.
Naiman, R.J. (2008) Freshwater animal diversity assessment – Foreword. Hydrobiologia, 595, 1–2.
Osorio–Tafall, B.F. (1942) Un nuevo Diaptomus del México central (Copepoda, Diaptomidae). Revista Brasileira de Zoologia, 2(2), 147–154.
Padial, J.M. & de la Riva I. (2007) Integrative taxonomists should use and produce DNA barcodes. Zootaxa, 1586, 67–68.
Paggi, J.C. (1979) Revision de las especies argentinas del género Bosmina, Baird agrupadas en el subgénero Neobosmina Lieder. (Crustacea: Cladocera). Acta Zoologica Lilloana, 35, 137–162.
Paggi, J.C. (1986) Aportes al conocimiento de la fauna Argentina de cladóceros, V: Ceriodaphnia laticaudata Müller 1867 y C. pulchella Sars 1862. Revista de la Asociación de Ciencias Naturales del Litoral, 17(1), 39–49.
Paggi, J.C. & da Rocha, C.E.F. (1999) Neodiaphanosoma a new genus of Sididae (Branchiopoda, Ctenopoda); with description of N. bergamini sp n. and comments on N. volzi (Stingelin 1905). Hydrobiologia, 397, 5–19.
Pearse, A. S. (1904) A new species of Diaptomus from Mexico. American Naturalist, 38, 889–891.
Penton, E.H., Hebert, P.D.N. & Crease, T.J. (2004) Mitochondrial DNA variation in North American populations of Daphnia obtusa: continentalism or cryptic endemism? Molecular Ecology, 13(1), 97–107.
Petrusek, A., Cerny M. & Audenaert E. (2004) Large intercontinental differentiation of Moina micrura (Crustacea : Anomopoda): one less cosmopolitan cladoceran? Hydrobiologia, 526, 73–81.
Ratnasingham, S. & Hebert, P.D.N. (2007) BOLD: The Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes, 7(3), 355–364
Richard, J. (1894a) Entomostracés recueillis dans lac Toba (Sumatra). Annali del Museo Civico di Storia Naturale Giacomo Doria, 14, 565–578.
Richard, J. (1894b) Sur quelques animaux intérieurs des eaux douces du Tonkin (Protozoaires, Rotifères, Entomostraces). Mémoires de la Société Zoologique de France, 7(2–3), 237–243.
Sacherova, V. & Hebert, P.D.N. (2003) The evolutionary history of the Chydoridae (Crustacea : Cladocera). Biological Journal of the Linnean Society, 79(4), 629–643.
Saitou, N. & Nei, M. (1987) The Neighbor–Joining Method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406–425.
Sars, G.O. (1885) On some Australian Cladocera, raised from dried mud. Forhandlinger i Videnskabs–Selskabei Christiania, 8, 1–46.
Sars, G.O. (1901) Contributions to the knowledge of the fresh–water Entomostraca of South America, as shown by artificial hatching from the dried material. Archiv for Mathematik og Naturvidenskab, 23, 1–102.
Sinev, A.Y., Kotov, A.A. & Van Damme, K. (2004) Morphology of a Neotropical cladoceran Alona dentifera (Sars, 1901), and its position within the Chydoridae Stebbing, 1902 (Branchiopoda: Anomopoda). Arthropoda Selecta, 13(3), 99–107.
Sinev, A.Y., Van Damme, K. & Kotov, A.A. (2006) Redescription of tropical–temperate cladocerans Alona diaphana King, 1853 and Alona davidi Richard, 1895 and their translocation to Leberis Smirnov, 1989 (Branchiopoda: Anomopoda; Chydoridae). Arthropoda Selecta, 14(3), 183–205.
Smirnov, N. N. (1989). Tropical cladocera. 2. New species of the families Chydoridae, Macrothricidae and Moinidae from tropical Australia. Zoologische Zhurnal, 68(7), 51-58.
Smirnov, N.N. (1996) Cladocera: The Chydorinae and Sayciinae (Chydoridae) of the World. SPB Academic Publishing, Amsterdam, 197 p.
Smirnov, N.N., Kotov, A.A. & Coronel, J.S. (2006) Partial revision of the aduncus–like species of Pleuroxus Baird, 1843 (Chydoridae, Cladocera) from the southern hemisphere with comments on subgeneric differentiation within the genus. Journal of Natural History, 40(27–28), 1617–1639.
Smith, M.A., Fisher, B.L. & Hebert, P.D.N. (2005) DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: the ants of Madagascar. Philosophical Transactions of the Royal Society B–Biological Sciences, 360(1462), 1825–1834.
Suárez–Morales, E. & Elías–Gutiérrez, M. (2000) Two new Mastigodiaptomus (Copepoda, Diaptomidae) from Southeastern Mexico with a key for the identification of the known species of the genus. Journal of Natural History, 34(5), 693–708.
Suárez–Morales, E. & Elías–Gutiérrez, M. (2001) On the taxonomical status of Arctodiaptomus dampfi Brehm (Crustacea: Copepoda: Diaptomidae) with comments on A. dorsalis (Marsh). Journal of Limnology, 60, 11–18.
Suárez–Morales, E. & Elías–Gutiérrez, M. (2003) Estado actual del conocimiento de los copépodos de aguas continentales de México. In : Barreiro–Güemes, M. T. et al. (Eds), El Colegio de la Frontera Sur, Universidad Autónoma Metropolitana, Estado de Veracruz, Mexico, pp. 157–169.
Suárez–Morales, E., Reid, J.W. & Elías–Gutiérrez, M. (2005) Diversity and distributional patterns of neotropical freshwater copepods (Calanoida: Diaptomidae). International Review of Hydrobiology, 90(1), 71–83.
Taylor, D.J., Ishikane, C.R. & Haney, R.A. (2002) The systematics of Holarctic Bosminids and a revision that reconciles molecular and morphological evolution. Limnology and Oceanography, 47(5), 1486–1495.
Trapani, J. (2003) Morphological variability in the Cuatro Cienegas cichlid, Cichlasoma minckleyi. Journal of Fish Biology, 62(2), 276–298.
U.S. Environmental Protection Agency. (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. 5th ed. U. S. Environmental Protection Agency, Office of Water (4303T). 1200 Pennsylvania Av. NW, Washington, DC 20460. EPA–821–R–02–012, viii, 266 p.
Ward, R.D., Zemlak, T.S., Innes, B.H., Last, P.R. & Hebert, P.D.N. (2005) DNA barcoding Australia´s fish species. Philosophical Transactions of the Royal Society of London Series B–Biological Sciences, 360(1462), 1847–1857.
Wilson, M.S. (1959) Free–living Copepoda Calanoida. In: Ward and Whipple's Freshwater Biology, 2nd ed., W. T. Edmonson, ed., Wiley, New York, pp. 738–794.