Advertisement

Marine Biology

, Volume 149, Issue 3, pp 503–513 | Cite as

Sympatric size variants of the microcopepod Oncaea venusta exhibit distinct lineages in DNA sequences

  • Dirk Elvers
  • Ruth Böttger-Schnack
  • Dietmar Blohm
  • Wilhelm Hagen
Research Article

Abstract

We investigated the phylogenetic relationships among different size groups of the pelagic microcopepod Oncaea venusta Philippi, 1843, by comparing the patterns of genetic variation of specimens collected at five locations of the Indo-West Pacific Ocean. Phylogenetic analyses were based on sequence data obtained from two DNA markers: A 310 bp fragment of the mitochondrial cytochrome b (cyt b) gene and a 480 bp fragment of the nuclear internal transcribed spacer 1 (ITS1). The cyt b sequences showed a much higher level of variation than those from ITS1, but the conclusion from both genes was concordant. Four genetic clades could be differentiated. A small- and a large-size group were unambiguously assigned to two distinct clades or lineages. Unexpectedly, the medium-sized individuals could be divided into another two different genetic clades. All four lineages were supported by high bootstrap values. The high levels of sequence divergence under sympatric conditions indicated that at least the two main groups, the large and the small one, may be assigned to different species. For the medium-size group additional morphological studies and more sensitive nuclear markers are required to clarify their taxonomic status.

Keywords

Codon Position Biological Species Concept Pairwise Sequence Divergence Oncaeid Species Sequence Divergence Rate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We wish to thank Dres. S. Nishida (University of Tokyo), K.C.C. Nair and K. Ramu (National Institute of Oceanography, Cochin), and H. Itoh (Suidosha Co. Ltd., Kawasaki) for providing the copepod material from the Indo-West Pacific Ocean. Thanks are due to Dr. M. Kochzius (Biotechnology and Molecular Genetics, University of Bremen), to Prof. R. Hanel (Leibniz-Institut für Meereswissenschaften, Kiel), to Prof. M. G. Vicker (University of Bremen) and the anonymous reviewers for helpful comments and suggestions on the manuscript. We appreciate the financial support of the Deutsche Forschungsgemeinschaft (DFG) to W. Hagen and D. Blohm (Ha 1706/9-1).

References

  1. Andersen NM, Cheng L, Damgaard J, Sperling FAH (2000) Mitochondrial DNA sequence variation and phylogeography of oceanic insects (Hemiptera: Gerridae: Halobates spp.). Mar Biol 136:421–430CrossRefGoogle Scholar
  2. Arbogast BS, Edwards SV, Wakeley J, Beerli P, Slowinski JB (2002) Estimating divergence times from molecular data on phylogenetic and population genetic timescales. Ann Rev Syst 33:707–740CrossRefGoogle Scholar
  3. Bensasson D, Zhang De-X, hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16:314–321CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bermingham E, Lessios HA (1993) Rate variation of protein and mitochondrial DNA evolution as revealed by sea urchins separated by the Isthmus of Panama. Proc Natl Acad Sci 90:2734–2738CrossRefPubMedPubMedCentralGoogle Scholar
  5. Böttger R (1987) The vertical distribution of micro- and small mesozooplankton in the central Red Sea. Biol Oceanogr 4:383–402Google Scholar
  6. Böttger-Schnack R (1995) Summer distribution of micro- and small mesozooplankton in the Red Sea and Gulf of Aden, with special reference to non-calanoid copepods. Mar Ecol Prog Ser 118:81–102CrossRefGoogle Scholar
  7. Böttger-Schnack R (2001) Taxonomy of Oncaeidae (Copepoda, Poecilostomatoida) from the Red Sea. II. Seven species of Oncaea s.str. Bull Natl Hist Mus Lond (Zool) 67:25–84Google Scholar
  8. Böttger-Schnack R, Hagen W, Schnack-Schiel SB (2001) The microcopepod fauna in the Gulf of Aqaba, northern Red Sea: species diversity and distribution of Oncaeidae (Poecilostomatoida). J Plankton Res 23:1029–1235CrossRefGoogle Scholar
  9. Böttger-Schnack R, Huys R (2004) Size polymorphism in Oncaea venusta Philippi, 1843 and the validity of O. frosti Heron, 2002: a commentary. Hydrobiologia 513:1–5CrossRefGoogle Scholar
  10. Böttger-Schnack R, Lenz J, Weikert H (2004) Are taxonomic details of relevance to ecologists? An example from oncaeid microcopepods of the Red Sea. Mar Biol 144:1127–1140CrossRefGoogle Scholar
  11. Brower AVZ (1994) Rapid morphological radiation and convergence among races of the butterfly Helicornius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA 91:6491–6495CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bucklin A, Frost BW, Bradford-Grieve JM, Allen LD, Copley NJ (2003) Molecular systematic and phylogenetic assessment of 34 calanoid copepod species of the Calanidae and Clausocalanidae. Mar Biol 142:333–343CrossRefGoogle Scholar
  13. Chu KH, Li CP, Ho HY (2001) The first transcribed spacer (ITS-1) of ribosomal DNA as a molecular marker for phylogenetic and population analyses in Crustacea. Mar Biotechnol 3:355–361CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cracraft J (1989) Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer Ass, Sunderland, pp 28–59Google Scholar
  15. Crofts A, Robinson H, Andrews K, Van Doren S, Berry E (1987) Catalytic sites for reduction and oxidation of quinones. In: Papa S, Chance B, Ernster L (eds) Cytochrome systems. Molecular biology and bioenergetics. Plenum, New York, pp 617–624CrossRefGoogle Scholar
  16. Edmands S, Harrison JS (2003) Molecular and quantitative trait variation within and among populations of the intertidal copepod Tigriopus californicus. Evolution 57:2277–2285CrossRefPubMedPubMedCentralGoogle Scholar
  17. Farran G (1929) Crustacea. Part X.-Copepoda. Natural history reports. British Antarctic (‘Terra Nova’) Expedition, 1910, Zoology 8:203–306Google Scholar
  18. Farris JS, Källersjö A, Kuge G, Bult C (1995) Constructing a significance test for incongruence. Syst Biol 44:570–572CrossRefGoogle Scholar
  19. Felsenstein J (1981) Evolutionary trees from DNA-sequences: a maximum likelihood approach. J Mol Evol 32:79–81Google Scholar
  20. Felsenstein J (1985) Confidence limits on phylogenies: an approach using bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  21. Feral J-P (2002) How useful are the genetic markers in attempts to understand and manage marine biodiversity? J Exp Mar Biol Ecol 268:121–145CrossRefGoogle Scholar
  22. Gantenbein B, Largiader C (2003) The phylogeographic importance of the Strait of Gibraltar as a gene flow barrier in terrestrial arthropods: a case study with the scorpion Buthus occitanus as model organism. Mol Phylogenet Evol 28:119–130CrossRefPubMedPubMedCentralGoogle Scholar
  23. Goetze E (2003) Cryptic speciation on the high seas, global phylogenetics of the copepod family Eucalanidae. Proc R Soc Lond B 270:2321–2331CrossRefGoogle Scholar
  24. Good DA, Wake DB (1992) Geographic variation and speciation in the torrent salamanders of the genus Rhyacotriton (Caudata: Rhyacotritonidae). Uni Calif Pub Zool 126:1–91Google Scholar
  25. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98 Google Scholar
  26. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 21:160–174CrossRefGoogle Scholar
  27. Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321CrossRefGoogle Scholar
  28. Hebert PDN, Remigio EA, Colbourne JK, Taylor DJ, Wilson CC (2002) Accelerated molecular evolution in halophilic crustaceans. Evolution 56:909–926CrossRefPubMedPubMedCentralGoogle Scholar
  29. Heron GA (2002) Oncaea frosti, a new species (Copepoda: Poecilostomatoida) from the Liberian coast and the Gulf of Mexico. Hydrobiologia 480:145–154CrossRefGoogle Scholar
  30. Hey J (2001) The mind of the species problem. Trends Ecol Evol 17:326–329CrossRefGoogle Scholar
  31. Hickerson MJ, Gilchrist MA, Takebayashi N (2003) Calibrating a molecular clock from phylogeographic data: moments and likelihood estimators. Evolution 57:2216–2225CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hillis DM (1991) Discriminating between phylogenetic signal and random noise in DNA sequences. In: Miyamoto MM, Cracraft J (eds) Phylogenetic analysis of DNA sequences. Oxford University Press, New York, pp 278–294Google Scholar
  33. Hillis DM, Huelsenbeck JP (1992) Signal, noise and reliability in molecular phylogenetic analyses. J Hered 83:189–195CrossRefPubMedPubMedCentralGoogle Scholar
  34. Hopcroft RR, Roff JC, Chavez FP (2001) Size paradigms in copepod communities: a re-examination. Hydrobiologia 453/454:133–141CrossRefGoogle Scholar
  35. Howell N, Gilbert K (1988) Mutational analysis of the mouse mitochondrial cytochrome b gene. J Mol Biol 203:607–617CrossRefPubMedPubMedCentralGoogle Scholar
  36. Huelsenbeck JP, Rannala B (1997) Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276 :227–232CrossRefPubMedPubMedCentralGoogle Scholar
  37. Johannesson K (2001) Parallel speciation: a key to sympatric divergence. Trends Ecol Evol 16:148–153CrossRefPubMedPubMedCentralGoogle Scholar
  38. Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90CrossRefGoogle Scholar
  39. Knowlton N, Weigt LA (1997) Species of marine invertebrates: a comparison of the biological and phylogenetic species concepts. In: Claridge MF, Dawah HA, Wilson MR (eds) Species: the units of biodiversity. Chapman & Hall, London, pp 199–219Google Scholar
  40. Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc Lond B 265:2257–2263CrossRefGoogle Scholar
  41. Knowlton N, Weigt LA, Solorzano LA, Mills DK, Bermingham E (1993) Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science 260:1629–1631CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: Molecular Evolutionary Genetics Analysis software. Bioinf Applicat Note 17:1244–1245CrossRefGoogle Scholar
  43. Lee CE (2000) Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate “populations”. Evolution 54:2014–2027CrossRefGoogle Scholar
  44. Malt SJ (1983a) Studies on the taxonomy and ecology of the marine copepod genus Oncaea Philippi. PhD Thesis, University. London, pp 500Google Scholar
  45. Malt SJ (1983b) Polymorphism and pore signature patterns in the copepod genus Oncaea (Cyclopoida). J mar biol Ass UK 63:449–466CrossRefGoogle Scholar
  46. Marko PB (2002) Fossil calibration of molecular clocks and the divergence times of germinate species pairs separated by the Isthmus of Panama. Mol Biol Evol 19:2005–2021CrossRefGoogle Scholar
  47. Marko PB, Moran AL (2002) Correlated evolutionary divergence of egg size and a mitochondrial protein across the Isthmus of Panama. Evolution 56:1303–1309CrossRefPubMedPubMedCentralGoogle Scholar
  48. Mayr E (1963) Animal species and evolution. Harvard University Press, CambridgeCrossRefGoogle Scholar
  49. Merritt TJS, Shi L, Chase MC, Rex MA, Etter RJ, Quattro JM (1998) “Universal” cytochrome b primers facilitate intraspecific studies in molluscan taxa. Molec Mar Biol Biotechnol 7:7–11Google Scholar
  50. Miller KJ, Bradford-Grieve JM, Jillett JB (1999) Genetic relationship between winter deep-dwelling and spring surface-dwelling female Neocalanus tonsus in the Southern Ocean. Mar Biol 134:99–106CrossRefGoogle Scholar
  51. Paffenhöfer G-A (1993) On the ecology of marine cyclopoid copepods (Crustacea, Copepoda). J Plankton Res 15 :37–55CrossRefGoogle Scholar
  52. Pagal M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884CrossRefGoogle Scholar
  53. Paskewitz SM, Wesson DM, Collins FH (1993) The internal transcribed spacers of ribosomal DNA in five members of the Anopheles gambiae species complex. Insect Mol Biol 2:247–257CrossRefPubMedPubMedCentralGoogle Scholar
  54. Posada D, Crandall K (1998) MODELTEST: testing the model of DNA substitution. Bioinf Applicat Note 14:817–818CrossRefGoogle Scholar
  55. Proudlove G, Wood PJ (2003) The blind leading the blind: cryptic subterranean species and DNA taxonomy. Trends Ecol Evol 18:272–273CrossRefGoogle Scholar
  56. Prüser F, Mossakowski D (1998) Low substitution rates in mitochondrial DNA in Mediterranean carabid species. Insect Mol Biol 7:121–128CrossRefPubMedPubMedCentralGoogle Scholar
  57. Puorto G, da Graca salomao M, Theakston RDG, Thorpe RS, Warrell DA, Wüsters W (2001) Combining mitochondrial DNA sequences and morphological data to infer species bounderies: phylogeography of lanceheaded pitvipers in the Brazilian Atlantic forest, and the status of Bothrops pradoi (Squamata: Serpentes: Viperidae). J Evol Biol 14:527–538CrossRefGoogle Scholar
  58. Quattro JM, Chase MR, Rex MA, Greig TW, Etter RJ (2001) Extreme mitochondrial DNA divergence within populations of deep-sea gastropod Frigidalvania brychia. Mar Biol 139:1107–1113CrossRefGoogle Scholar
  59. Riccardi N, Mariotto L (2000) Seasonal variations in copepod body length: a comparison between different species in the Lagoon of Venice. Aquat Ecol 34:243–252CrossRefGoogle Scholar
  60. Rocha-Olivares A, Fleeger JW, Foltz DW (2001) Decoupling of molecular and morphological evolution in deep lineages of a meiobenthic copepod. Mol Biol Evol 18:1088–1102CrossRefGoogle Scholar
  61. Rodriguez-Trelles F, Tarrio R, Ayala FJ (2001) Erratic overdispersion of three molecular clocks: GPDH, SOD, and XDH. Proc Natl Acad Sci USA 98:11405–11410CrossRefPubMedGoogle Scholar
  62. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Ehrlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491CrossRefPubMedGoogle Scholar
  63. Schizas NV, Coull BC, Chandler GT, Quattro JM (2002) Sympatry of distinct mitochondrial DNA lineages in a copepod inhabiting estuarine creeks in the southwestern USA. Mar Biol 140:585–594CrossRefGoogle Scholar
  64. Schizas NV, Street GT, Coull BC, Chandler GT, Quattro JM (1997) An efficient DNA extraction method for small metazoans. Mol Mar Biol Biotechnol 6:381–383PubMedGoogle Scholar
  65. Schubart CD, Neigel JE, Felder DL (2000) Molecular phylogeny of mud crabs (Brachyura: Panopeidae) from the northwestern Atlantic and the role of morphological stasis and convergence. Mar Biol 137:11–18CrossRefGoogle Scholar
  66. Shank TM, Lutz RA, Vrijenhoek RC (1998) Molecular systematics of shrimp (Decapoda: Bresiliidae) from deep-sea hydrothermal vents, I: enigmatic “small orange” shrimp from the Mid-Atlantic Ridge are juvenile Rimicaris exoculata. Mol Mar Biol Biotechnol 7:88–96PubMedPubMedCentralGoogle Scholar
  67. Simmons RB, Weller SJ (2001) Utility and evolution of cytochrome b in insects. Mol Phylogenet Evol 20:196–210CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sites JW, Marshall JC (2003) Delimiting species: a renaissance issue in systematic biology. Trends Ecol Evol 18:462–470CrossRefGoogle Scholar
  69. Söller R, Warnke K, Saint-Paul U, Blohm D (2000) Sequence divergence of mitochondrial DNA indicates cryptic biodiversity in Octopus vulgaris and supports the taxonomic distinctiveness of Octopus mimus (Cephalopoda:Octopodidae). Mar Biol 136:29–35CrossRefGoogle Scholar
  70. Strauss E (1999) Can mitochondrial clocks keep time? Science 283:1435–1438CrossRefPubMedPubMedCentralGoogle Scholar
  71. Swofford DL (1998) PAUP*. Phylogenetic analysis using Parsimony (*and other methods). Version 4. Sinauer Ass, Sunderland, Mass (http://www.paup.csit.fsu.edu/)
  72. Tarjuelo I, Posada D, Crandall KA, Pascual M, Turon X (2001) Cryptic species of Clavelina (Ascidiacea) in two different habitats: harbors and rocky littoral zones in the northwestern Mediterranean. Mar Biol 139:455–462CrossRefGoogle Scholar
  73. Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2003) A plea for DNA taxonomy. Trends Ecol Evol 18:70–74CrossRefGoogle Scholar
  74. Taylor DJ, Hebert PDN, Colbourne JK (1996) Phylogenetics and evolution of the Daphnia longispina group (Crustacea) based on 12s rDNA sequence and allozyme variation. Mol Phylogenet Evol 5:495–510CrossRefPubMedPubMedCentralGoogle Scholar
  75. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acid Res 24:4876–4882CrossRefGoogle Scholar
  76. Wu C-I (2001) The genic view of the process of speciation. J Evol Biol 14:851–865CrossRefGoogle Scholar
  77. Yamauchi MM, Miya MU, Nishida M (2003) Complete mitochondrial DNA sequence of the swimming crab, Portunus trituberculatus (Crustacea: Decapoda: Brachyura). Gene 311:129–135CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Dirk Elvers
    • 1
  • Ruth Böttger-Schnack
    • 2
  • Dietmar Blohm
    • 3
  • Wilhelm Hagen
    • 1
  1. 1.Marine ZoologyUniversity of Bremen BremenGermany
  2. 2.Moorsehdener Weg 8Rastorf-RosenfeldGermany
  3. 3.Dept. of Biotechnology and Molecular GeneticsUniversity of BremenBremenGermany

Personalised recommendations