Marine Biology

, Volume 125, Issue 4, pp 735–742

Are meiofaunal species cosmopolitan? Morphological and molecular analysis of Xenotrichula intermedia (Gastrotricha: Chaetonotida)

  • M. A. Todaro
  • J. W. Fleeger
  • Y. P. Hu
  • A. W. Hrincevich
  • D. W. Foltz


Many meiofaunal species are reported to be cosmopolitan, but due to uncertainties of identification, the affiliation of specimens from geographically distant areas to the same species-taxon is problematic. In this study, we examined morphological and molecular variation in samples of Xenotrichula intermedia Remane (Gastrotricha: Chaetonotida) from the Mediterranean Sea, the northwestern Atlantic and the northern Gulf of Mexico. Univariate analysis of 16 morphological traits was unable to detect differences among populations, except for the length of the pharynx, which was significantly shorter in the Gulf of Mexico specimens. Canonical discriminant analysis separated the Gulf of Mexico specimens from the other two populations, with pharynx length contributing about half of the total discrimination. Molecular analysis based on restriction-fragment length polymorphisms (RFLPs) in a 710-base pair polymerase chain-reaction (PCR) produet representing roughly half of the mitochondrial cytochrome oxidase I (COI) gene detected four haplotypes: one each from the Mediterranean and the Gulf of Mexico populations and two coexisting within the Atlantic population. The estimated nucleotide-sequence divergence calculated for each pairwise combination of haplotypes (based on the proportion of shared fragments) ranged from 5.3 to 11.5%. The high genetic divergence and the inability to clearly separate populations based on morphology suggest that individuals characterized by different haplotypes are genetically isolated sibling species.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. A Rev Ecol Syst 18: 489–522Google Scholar
  2. Avise JC, Nelson WS, Sigita H (1994) A speciational history of “living fossils”: molecular evolutionary patterns in horseshoe crabs. Evolution 48: 1986–2001Google Scholar
  3. Balsamo M, Manicardi GC (1995) Nuclear DNA content in Gastrotricha. Experientia 51: 356–359Google Scholar
  4. Balsamo M, Todaro MA, Tongiorgi P (1992) Marine gastrotrichs from the Tuscan Archipelago (Tyrrhenian Sea). II. Chaetonotida, with description of three new species. Boll Zool 59: 487–498Google Scholar
  5. Brown WM (1985) The mitochondrial genome of animals. In: McIntyre RJ (ed) Molecular evolutionary genetics. Plenum Press, New York, pp 95–130Google Scholar
  6. Bucklin A, Frost BW, Kocher TD (1995) Molecular systematics of six Calanus and three Metridia species (Calanoida: Copepoda). Mar Biol 121: 655–664Google Scholar
  7. Burton RS (1994) Inferring the genetic structure of marine populations: a case study comparing allozyme and DNA sequence data. Rep Calif coop ocean Fish Invest (CalCOFI) 35: 52–60Google Scholar
  8. Burton RS, Lee BN (1994) Nuclear and mitochondrial gene genealogies and allozyme polymorphism across a major phylogeo-graphic break in the copepod Tigriopus californicus. Proc natn Acad Sci USA 91: 5197–5201Google Scholar
  9. Castagnone-Sereno P, Vanlerberghe-Masutti F, Leroy F (1994) Gentic polymorphism between and within Meloidogyne species detected with RAPD markers. Genome 37: 904–909Google Scholar
  10. Cherry LM, Case SM, Wilson AC (1978) Frog perspective on the morphological difference between humans and chimpanzees. Science, NY 200: 209–211Google Scholar
  11. Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J molec Evolut 22: 252–271Google Scholar
  12. Coull BC (1988) Ecology of the marine meiofauna. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, DC, pp 18–38Google Scholar
  13. Cunningham CW, Blackstone NW, Buss LW (1992) Evolution of king crabs from hermit crab ancestors. Nature, Lond 355: 539–542Google Scholar
  14. Evans WA (1994) Morphological variability in warm-temperate and subtropical populations of Macrodasys (Gastrotricha: Macrodasyida: Macrodasyidae) with description of seven new species. Proc biol Soc Wash 107: 239–255Google Scholar
  15. Fava G, Volkmann B (1975) Tisbe (Copepoda: Harpacticoida) species from the Lagoon of Venice. I. Seasonal fluctuations and ecology. Mar Biol 30: 151–165Google Scholar
  16. 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. Molec mar Biol Biotechnol 3: 294–299Google Scholar
  17. Ganapati PN, Rao GC (1967) On some marine interstitial Gastrotrichs from the beach sands of Waltair coast. Proc Indian Acad Sci (Sect B) 66: 214–225Google Scholar
  18. Gárate T, Robinson MP, Chacón MR, Parkhouse RME (1991) Characterization of species and races of the genus Meloidogyne by DNA restriction enzyme analysis. J Nematol 23: 414–420Google Scholar
  19. Geller JB, Carlton JT, Powers DA (1994) PCR-based detection of mtDNA haplotypes of native and invading mussels on the northeastern Pacific coast: latitudinal pattern of invasion. Mar Biol 119: 243–249Google Scholar
  20. Gerlach SA (1953) Gastrotrichen aus dem Kuestengrundwasser des Mittelmeeres. Zool Anz 150: 203–211Google Scholar
  21. Gerlach SA (1962) Freilebende Meeresnematoden von den Malediven. Kieler Meeresforsch 18: 81–108Google Scholar
  22. Gerlach S (1977) Means of meiofauna dispersal. Mikrofauna Meeresbod 61: 89–103Google Scholar
  23. Giere O (1993) Meiobenthology. The microscopic fauna in aquatic sediments. Springer-Verlag, BerlinGoogle Scholar
  24. Harris TS, Sandall LJ, Powers TO (1990) Identification of single Meloidogyne juveniles by polymerase chain reaction amplification of mitochondrial DNA. J Nematol 22: 518–524Google Scholar
  25. Hulings NC (1971) Summary and current status of the taxonomy and ecology of benthic Ostracoda including interstitial forms. Smithson Contr Zool 76: 91–96Google Scholar
  26. Hummon WD (1994) Trans- and cis-Atlantic distributions of three marine heterotardigrades. Trans Am microsc Soc 113: 333–342Google Scholar
  27. Hummon WD, Hummon MR, Mostafa HM (1994) Marine Gastrotricha of Mediterranean Egypt. Am Zool 34: p. 10A (Abstract)Google Scholar
  28. Jouk PEH, Hummon WD, Hummon MR, Roidou E (1992) Marine Gastrotricha from the Belgian coast: species list and distribution. Bull Inst Sci nat Belg (Biol) 62: 87–90Google Scholar
  29. Karl SA, Avise JC (1993) PCR-based assay of Mendelian polymorphism from anonymous single-copy nuclear DNA: techniques and applications for population genetics. Molec Biol Evolut 10: 342–361Google Scholar
  30. Knowlton N (1993) Sibling species in the sea. A Rev Ecol Syst 24: 189–216Google Scholar
  31. Knowlton N, Weigt LA, Solórzano LA, Mills DK, Bermingham E (1993) Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science, NY 260: 1629–1632Google Scholar
  32. Levi C (1950) Contribution a l'étude des gastrotriches de la region de Roscoff. Archs Zool exp gén 87: 31–42Google Scholar
  33. Litvaitis MK, Nunn G, Thomas WK, Kocher TD (1994) A molecular approach for the identification of meiofaunal turbellarians (Platyhelminthes, Turbellaria). Mar Biol 120: 437–442Google Scholar
  34. Luporini P, Magagnini G, Tongiorgi P (1973) Chaetonotoid gastrotrichs of the Tuscan Coast. Boll Zool 40: 31–40Google Scholar
  35. Mayr E (1948) The bearing of the new systematics on genetical problems. The nature of species. Adv Genet 2: 205–237Google Scholar
  36. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  37. Nei M Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc natn Acad Sci USA 76: 5269–5273Google Scholar
  38. Palmer MA (1988) Dispersal of marine meiofauna: a review and conceptual model explaining passive transport and active emergence with implication for recruitment. Mar Ecol Prog Ser 48: 81–91Google Scholar
  39. Palumbi SR, Benzie J (1991) Large mitochondrial DNA differences between morphologically similar penaeid shrimp. Molec mar Biol Biotechnol 1: 27–34Google Scholar
  40. Pfannkuche O, Thiel H (1988) Sample processing. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp 134–145Google Scholar
  41. Rao GC, Ganapati PN (1968) The interstitial fauna inhabiting the beach sands of Waltair coast. Proc natn Inst Sci India (Ser B) 34: 82–125Google Scholar
  42. Renaud-Mornant J, Pollock LW (1971) A review of the systematics and ecology of marine Tardigrada. Smithson Contr Zool 76: 109–117Google Scholar
  43. Ruppert EE (1977) Zoogeography and speciation in marine Gastrotricha. Mikrofauna Meeresbod 61: 231–251Google Scholar
  44. Ruppert EE (1979) Morphology and systematics of the Xenotrichulidae (Gastrotricha, Chaetonotida). Mikrofauna Meeresbod 76: 1–56Google Scholar
  45. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HE (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science, NY 239: 487–491Google Scholar
  46. SAS Institute Inc. (1990) SAS user's guide: statistics. Version 6 edn. SAS Institute Inc. Cary, North CarolinaGoogle Scholar
  47. Sterrer W (1973) Plate tectonics as a mechanism for dispersal and speciation in interstitial sand fauna. Neth J Sea Res 7: 200–222Google Scholar
  48. Todaro MA, Fleeger JW, Hummon WD (1995) Marine gastrotrichs from the sand beaches of the northern Gulf of Mexico: species list and distribution. Hydrobiologia 310: 107–117Google Scholar
  49. Volkmann-Rocco B (1972) Species of Tisbe (Copepoda: Harpacticoida) from Beaufort, North Carolina. Archo Oceanogr Limnol 17: 223–258Google Scholar
  50. Wallace DG, Maxson LR, Wilson AC (1971) Albumin evolution in frogs: a test of the evolutionary clock hypothesis. Proc natn Acad Sci USA 68: 3127–3129Google Scholar
  51. Wells JBJ (1986) Biogeography of benthic harpacticoid copepods of the marine littoral and continental shelf. Syllogeus (Nat Mus Can) 58: 126–135 [Proc 2nd int Conf Copepoda (Schriever G, Schminke HK, Shih C-t, eds). Ottawa, Can]Google Scholar
  52. Westheide W (1971) Interstitial Polychaeta (excluding Archianellida). Smithson Contr Zool 76: 57–70Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • M. A. Todaro
    • 1
  • J. W. Fleeger
    • 1
  • Y. P. Hu
    • 1
  • A. W. Hrincevich
    • 1
  • D. W. Foltz
    • 1
  1. 1.Department of Zoology and PhysiologyLouisiana State UniversityBaton RougeUSA
  2. 2.Dipartimento di Biologia AnimaleUniversità di ModenaModenaItaly
  3. 3.Center for Theoretical and Applied GeneticsCook College of Rutgers UniversityNew BrunswickUSA

Personalised recommendations