Journal of Molecular Evolution

, Volume 43, Issue 1, pp 58–70

What can 18S rDNA do for bivalve phylogeny?

  • Gerhard Steiner
  • Manfred Müller


Molecular characteristics, especially 18S rDNA sequences, may be of great value for the study of bivalve evolution and its numerous morphological convergencies once the reliability of these data can be evaluated. The analysis of 11 published complete molluscan sequences and two new ones,Arca noae andAtrina pectinata, reveals considerable differences in relative substitution rates. The gastropod and eulamellibranch species have the fastest and Atrina species have the slowest rates. Two methods are used to assess the information contents of the dataset in addition to bootstrap analysis, spectral analysis, and the “pattern of resolved nodes” technique. Tree reconstructions by parsimony, neighbor-joining, and maximum-likelihood differ in regard to the position of the eulamellibranch family Mactridae and ofCrassostrea. Although there is a signal for the monophyly of Bivalvia, Mactridae cluster with Gastropoda in most runs, rendering Bivalvia diphyletic. The position ofCrassostrea was extremely variable, probably due to the high substitution rate of this species.Atrina roots deeper thanArca in all trees, although a corresponding signal in spectral analysis is absent. Phylogenetic signals among the three pectinid species are low but sufficient to resolve the branching pattern. The tree inferred from the 18S rDNA and from morphological data has Bivalvia monophyletic with a basal polytomy of Mactridae,Crassostrea, and the remaining Pteriomorphia, whereArca branches off before Atrina and the Pectinidae.Argopecten is sister group to the other two pectinids; 18S sequence data will have great impact on our understanding of bivalve phylogeny, but only when more sequences of similar substitution rates are available.

Key words

Mollusca Bivalvia Phylogeny 18S rDNA Spectral analysis Atrina pectinata Arca noae 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adamkewicz LS, Harasewych MG (1994) Use of random amplified polymorphic DNA (RAPD) markers to assess relationships among beach clams of the genusDonax. Nautilus (Suppl) 2:51–60Google Scholar
  2. Adoutte A, Philippe H (1993) The major lines of metazoan evolution: summary of traditional evidence and lessons from ribosomal RNA sequence analysis. In: Pichon Y (ed) Comparative molecular neurobiology. Birkhäuser, Basel, pp 1–30Google Scholar
  3. Backeljau T, Winnepenninckx B, De Bruyn L (1993) Cladistic analysis of metazoan relationships: a reappraisal. Cladistics 9:167–181CrossRefGoogle Scholar
  4. Boore JL, Brown WM (1994) Mitochondrial genomes and the phylogeny of mollusks. Nautilus (suppl) 2:61–78Google Scholar
  5. Boss KJ (1982) Mollusca. In: Parker SP (ed) Synopsis and classification of living organisms, vol 1. McGraw-Hill, New York, pp 945–1166Google Scholar
  6. Carter JG, Tevesz MJS (1978) The shell structure ofPtychodesma (Cyrtodontidae; Bivalvia) and its bearing on the evolution of the Pteriomorphia. Philos Trans R Soc Lond Biol 284:367–374Google Scholar
  7. Conway Morris S (1993) The fossil record and the early evolution of the Metazoa. Nature 361:219–225Google Scholar
  8. De Rijk P, De Wachter R (1993) DOSE, an interactive tool for sequence alignment and secondary structure research. Cabios 9:735–740PubMedGoogle Scholar
  9. Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–410Google Scholar
  10. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376CrossRefPubMedGoogle Scholar
  11. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791Google Scholar
  12. Felsenstein J (1993) PHYLIP: phylogenetic inference package, version 3.5c. Distributed by the author, Department of Genetics, University of Washington, SeattleGoogle Scholar
  13. Ghiselin MT, Degens ET, Spencer DW, Parker RH (1967) A phylogenetic survey of molluscan shell matrix proteins. Brevoria 262:1–35Google Scholar
  14. Goodman M, Pedwaydon J, Czelusniak J, Suzuki T, Gotoh T, Moens L, Shishikura F, Walz D, Vinogradov S (1988) An evolutionary tree for invertebrate globin sequences. J Mol Evol 27:236–249CrossRefPubMedGoogle Scholar
  15. Harte ME (1992) A new approach to the study of bivalve evolution. Am Malacol Bull 9:199–206Google Scholar
  16. Healy JM (1988) Sperm morphology and its systematic importance in the Gastropoda. Malacol Rev (suppl)4:251–266Google Scholar
  17. Healy JM (1989) Spermiogenesis and spermatozoa in the relict bivalve genusNeotrigonia: relevance to trigonoid relationships, particularly Unionidea. Mar Biol 103:75–85CrossRefGoogle Scholar
  18. Healy JM (1995) Molluscan sperm ultrastructure: correlation with taxonomic units within the Gastropoda, Cephalopoda and Bivalvia. In: Taylor J (ed) Origin and evolutionary radiation of the mollusca. Oxford University Press, Oxford, pp 99–113Google Scholar
  19. Hendy MD, Penny D (1993) Spectral analysis of phylogenetic data. J Classif 10:5–24Google Scholar
  20. Kenchington EL, Roddick DL, Singh KR, Bird CJ (1994) Analysis of small-subunit rRNA gene sequences from six families of molluscs. J Mar Biotechnol 1:215–217Google Scholar
  21. Kilias R (1982) Mollusca, Bivalvia. In: Gruner H-J (ed) Lehrbuch der Speziellen Zoologie. Gustav Fischer Verlag, Stuttgart, pp 152–202Google Scholar
  22. Kojima S, Segawa R, Kobayashi T, Hashimoto T, Fujikura K, Hashimoto J, Otha S (1995) Phylogenetic relationships among species ofCalyptogena (Bivalvia: Vesicomyidae) collected around Japan revealed by nucleotide sequences of mitochondrial genes. Mar Biol 122:401–407CrossRefGoogle Scholar
  23. Lake JA (1987) Rate-independent technique for analysis of nucleic acid sequences: evolutionary parsimony. Mol Biol Evol 4:167–191PubMedGoogle Scholar
  24. Lecointre G, Philippe H, Lê LHV, Le Guyader H (1993) Species sampling has a major impact on phylogenetic inference. Mol Phyl Evol 2:205–224Google Scholar
  25. Lecointre G, Philippe H, Lê LHV, Le Guyader H (1994) How many nucleotides are required to resolve a phylogenetic problem? The use of a new statistical method applicable to available sequences. Mol Phyl Evol 3:292–309Google Scholar
  26. Lento GM, Hickson RE, Chambers GK, Penny D (1995) Use of spectral analysis to test hypotheses on the origin of pinnipeds. Mol Biol Evol 12:28–52PubMedGoogle Scholar
  27. Littlewood DTJ (1994) Molecular phylogenetics of cupped oysters based on partial 28s rRNA gene sequences. Mol Phyl Evol 3:221–229Google Scholar
  28. Littlewood DTJ, Ford SE, Fong D (1991) Small subunit rDNA gene sequence ofCrassostrea virginica (Gmelin) and a comparison with similar sequences from other bivalve molluscs. Nuclei Acids Res 19:6048Google Scholar
  29. Morton B (1995) The evolutionary history of the Bivalvia. In: Taylor J (ed) Origin and evolutionary radiation of the Mollusca. Oxford University Press, Oxford, pp 337–360Google Scholar
  30. Nevesskaya LA, Scarlato OA, Starobogatov YI, Eberzin AG (1971) New ideas on bivalve systematics. Paleontol J 5:141–155Google Scholar
  31. Newell ND, Boyd DW (1978) A paleontologist's view of bivalve phylogeny. Philos Trans R Soc Lond Biol 284:203–215Google Scholar
  32. Patterson C (1987) Introduction. In: Patterson C (ed) Molecules and morphology in evolution: conflict or compromise? Cambridge University Press, Cambridge, pp 1–22Google Scholar
  33. Penny D, Watson EE, Hickson RE, Lockhard PJ (1993) Recent progress with methods for evolutionary trees. N Z J Bot 31:275–288Google Scholar
  34. Philippe H, Chenuil A, Adoutte A (1994) Can the cambrian explosion be inferred through molecular phylogeny? Development (suppl): 15–25Google Scholar
  35. Powell JR (1994) Molecular techniques in population genetics: a brief history. In: Schierwater B, Streit B, Wagner GP (eds) Molecular ecology and evolution: approaches and applications. Birkhäuser Verlag, Basel, pp 132–156Google Scholar
  36. Purchon RD (1990) Stomach structure, classification and evolution of the Bivalvia. In: Morton B (ed) The Bivalvia—Proceedings of a Memorial Symposium in Honour of Sir Charles Maurice Yonge (1899–1986), Edinburgh. Hong Kong University Press, Hong Kong, pp 73–82Google Scholar
  37. Purchon RD (1959) Phylogenetic classification of the Lamellibranchia, with special reference to the Protobranchia. Proc Malacol Soc Lond 33:224–230Google Scholar
  38. Rice EL (1990) Nucleotide sequence of the 18S ribosomal RNA gene from the Atlantic sea scallopPlacopecten magellanicus. Nucleic Acids Res 18:5551PubMedGoogle Scholar
  39. Rice EL, Roddick D, Singh RK (1993) A comparison of molluscan (Bivalvia) phylogenies based on palaeontological and molecular data. Mol Mar Biol Biotechnol 2:137–146PubMedGoogle Scholar
  40. Ridewood WG (1903) On the structure and the gills of the Lamellibranchia. Philos Trans R Soc Lond Biol 195:147–284Google Scholar
  41. Rosenberg G, Kuncio GS, Davis GM, Harasewych MG (1994) Preliminary ribosomal RNA phylogeny of gastropod and unionidean bivalve mollusks. Nautilus (Suppl)2:111–121Google Scholar
  42. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  43. Salvini-Plawen L, Steiner G (1995) Synapomorphies and plesiomorphies in higher classification of Mollusca. In: Taylor J (ed) Origin and evolutionary radiation of the mollusca. Oxford University Press, Oxford, pp 29–51Google Scholar
  44. Scarlato OA, Starobogatov YI (1978) Phylogenetic relations and the early evolution of the class Bivalvia. Philos Trans R Soc Lond Biol 284:217–224Google Scholar
  45. Swofford DL (1993) PAUP 3.1 user's manual. Illinois Natural History Survey, Champaign, p 272Google Scholar
  46. Swofford DL, Olsen GJ (1990) Phylogenetic reconstruction. In: Hillis DM, Moritz C (eds) Molecular systematics. Sinauer, Sunderland, MA pp 411–501Google Scholar
  47. Tillier S, Masselot M, Guerdoux J, Tillier A (1994) Monophyly of major gastropod taxa tested from partial 28S rRNA sequences, with emphasis on Euthyneura and hot-vent limpetsPeltospira. Nautilus (Suppl)2:122–140Google Scholar
  48. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighing, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedGoogle Scholar
  49. Waller TR (1978) Morphology, morphoclines and a new classification of the Pteriomorphia. Philos Trans R Soc Lond Biol 284:345–365Google Scholar
  50. Waller TR (1990) The evolution of ligament systems in the Bivalvia. In: Morton B (ed) The Bivalvia. Hong Kong University Press, Hong Kong, pp 49–71Google Scholar
  51. Waller TR (1991) Evolutionary relationships among commercial scallops (Mollusca: Bivalvia: Pectinidae). In: Shumway SE (ed) Scallops: biology, ecology and aquaculture. Elsevier, New York, pp 1–73Google Scholar
  52. Winnepenninckx B, Van de Peer Y, Peeters K, de Baere I, Moens L (1992) Study of invertebrate and plant globins: templates and evolutionary trees. Belge J Bot 125:191–200Google Scholar
  53. Winnepenninckx B, Backeljau T, De Wachter R (1994) Small ribosomal subunit RNA and the phylogeny of Mollusca. Nautilus (Suppl)2:98–110Google Scholar
  54. Yonge CM (1953) The monomyarian condition in the Lamellibranchia. Trans R Soc Edinburgh 62:443–478Google Scholar
  55. Yonge CM (1957) Mantle fusion in the Lamellibranchia. Pubbl Stan Zool Napoli 29:151–171Google Scholar
  56. Yonge CM (1982) Mantle margins with a revision of siphonal types in the Bivalvia. J Mol Stud 48:102–103Google Scholar
  57. Yonge CM, Campbell JI (1968) On the heteromyarian condition in the Bivalvia with special reference toDreissena polymorpha and certain Mytilacea. Trans R Soc Edinburgh 68:21–42Google Scholar

Copyright information

© Springer-Verlag New York Inc 1996

Authors and Affiliations

  • Gerhard Steiner
    • 1
  • Manfred Müller
    • 2
  1. 1.Institute of ZoologyUniversity of ViennaViennaAustria
  2. 2.Institute of GeneticsUniversity of ViennaViennaAustria

Personalised recommendations