Marine Biology

, Volume 124, Issue 2, pp 267–278

Evolution and systematics in Haliotidae (Mollusca: Gastropoda): inferences from DNA sequences of sperm lysin

  • Youn-Ho Lee
  • V. D. Vacquier


Abalone taxonomy and systematics have remained unresolved: neither stable species-level nomenclature nor a cladistic hypothesis of relationships among species have been established. To infer the phylogeny of the genus Haliotis and to identify species using molecular data, we compared complementary DNA (cDNA) sequences of sperm lysin from 27 species-group taxa from California, Japan, Australia, New Zealand, Taiwan, Borneo, Madagascar, South Africa, Greece, France, Italy and the Azores. The lysin cDNA sequences reveal that 22 of the 27 taxa are clearly distinguishable by >20 nucleotide differences. Of the remaining 5, H. coccinea from the Azores may be a subspecies of H. tuberculata, if not a sibling species (10 nucleotide differences). The other four taxa are most probably the same species as one of the 22 taxa: the lysin sequences are almost identical between H. madaka and H. discus hannai, H. conicopora and H. rubra, H. diversicolor supertexta and H. diversicolor aquatilis, and H. tuberculata lamellosa and H. tuberculata tuberculata. The phylogeny of lysin cDNA suggests that there are three groups among the 27 species-group taxa: (1) all California species and 3 Japanese species (H. gigantea, H. discus hannai, and H. madaka): (2) 1 New Zealand species (H. iris); (3) 1 Japanese species (H. diversicolor aquatilis), Indo-West Pacific species and European species. These groups can be assigned to three previously recognized subgenera (Nordotis, Paua and Padollus) in the genus Haliotis. Two historical hypotheses are proposed to explain the biogeography and evolution within these abalone: (1) Tethyan distribution of the ancestral abalone, during the Cretaceous, followed by extinction in most of the habitat, but radiation in California and Southeast Asia which later spread to the other areas; (2) North Pacific rim distribution of the ancestral abalone, followed by dispersal to the other areas during the Paleogene.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anderson FM (1902) Cretaceous deposits of the Pacific coast. Proc Calif Acad Sci 2: 1–154Google Scholar
  2. Brown LD (1993) Biochemical genetics and species relationships within the genus Haliotis (Gastropoda: Haliotidae). J mollusc Stud 59: 429–443Google Scholar
  3. Brown LD, Murray ND (1992) Genetic relationships within the genus Haliotis. In: Shepherd SA, Tegner MJ, Guzmán del Próo SA (eds) Abalone of the world: biology, fisheries and culture. Blackwells Scientific Publishers, London, pp 19–23Google Scholar
  4. Burton RS, Lee B-N (1994) Nuclear and mitochondrial gene genealogies and allozyme polymorphism across a major phylogeographic break in the copepod Tigriopus californicus. Proc natn Acad Sci USA 91: 5197–5201Google Scholar
  5. Chomczynski P, Sacchi N (1987) Single-step method on RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analyt Biochem 162: 156–159Google Scholar
  6. Cox KW (1962) California abalones, family Haliotidae. Fish Bull. Calif 118: 1–131Google Scholar
  7. Dauphin Y, Cuif JP, Mutvei H, Denis A (1989) Mineralogy, chemistry and ultrastructure of the external shell-layer in ten species of Haliotis with reference to H. tuberculata (Mollusca: Archeogastropoda). Bull geol Instn Univ Upsala (NS) 15: 7–38Google Scholar
  8. Durham JW (1979) California Cretaceous Haliotis. Veliger 21: 373–374Google Scholar
  9. Feng D-F, Doolittle RF (1990) Progressive alignment and phylogenetic tree construction of protein sequences. Meth Enzym 183: 375–387Google Scholar
  10. Habe T, Kosuge S (1964) A list of the Indo-Pacific molluses, concerning to the Japanese molluscan fauna. I. Superfamily Pleurotomarioidea. National Science Museum, Ueno Park, Tokyo, JapanGoogle Scholar
  11. Hara M, Fujio Y (1992) Genetic relationship among abalone species. [in Jap] Suisan Ikushu (Mar Aquacult) 17: 55–61Google Scholar
  12. Herbert DG (1990) Designation of lectotype and type locality for Haliotis rugosa Lamarck, 1822 (Mollusca: Gastropoda: Haliotidae). Ann Natal Mus 31: 207–213Google Scholar
  13. Hertlein LG (1937) Haliotis koticki, a new species from the lower Miocene of California. Bull Sth Calif Acad Sci 36: 93–97Google Scholar
  14. Hillis DM, Moritz C (1990) Molecular systematics. Sinauer Associates, Boston, MassachusettsGoogle Scholar
  15. Hughes AL (1992) Avian species described on the basis of DNA only. Trends Ecol Evolut 7: 2–3Google Scholar
  16. Hultman T, Stahl S, Hornes E, Uhlen M (1989) Direct solid phase sequencing of genomic and plasmid DNA using magnetic beads as solid support. Nucleic Acids Res 17: 4937–4945Google Scholar
  17. Ino T (1952) Biological studies on the propagation of Japanese abalone (genus Haliotis). Bull Tokai reg Fish Res Lab 5: 1–102Google Scholar
  18. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132Google Scholar
  19. Karl SA, Avise JC (1992) Balancing selection at allozyme loci in oysters: implications from unclear RFLPs. Science NY 256: 100–102Google Scholar
  20. Kimura M (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotude sequences. J molec Evolut 16: 111–120Google Scholar
  21. Kumar S, Tamura K, Nei M (1993) MEGA: Molecular evolutionary genetics analysis. version 1.01. The Pennsylvania State University, University Park, PennsylvaniaGoogle Scholar
  22. Lee Y-H, Ota T, Vacquier VD (1995) Positive selection is a general phenomenon in the evolution of abalone sperm lysin. Molec Biol Evolut 12: 231–238Google Scholar
  23. Lee Y-H, Vacquier VD (1992a) The divergence of species-specific abalone sperm lysins is promoted by positive Darwinian selection. Biol Bull mar biol Lab, Woods Hole 182: 97–104Google Scholar
  24. Lee Y-H, Vacquier VD (1992b) Reusable cDNA libraries coupled to magnetic beads. Analyt Biochem 206: 206–207Google Scholar
  25. Lee Y-H, Vacquier VD (1993) A method for obtaining high-quality sequences from the non-biotinylated, free ssDNA remaining after solid-phase sequencing BioTechniques 14: 191–192Google Scholar
  26. Lews CA, Talbot CF, Vacquier VD (1982) A protein from abalone sperm dissolves the egg vitelline layer by a nonenzymatic mechanism. Devl Biol 92: 227–239Google Scholar
  27. Lewontin RC (1991) Twenty-five years ago in genetics: electrophoresis in the development of evolutionary genetics: milestone or millstone? Genetics, Austin, Tex 128: 657–662Google Scholar
  28. Lindberg DR (1992) Evolution, distribution and systematics of Haliotidae. In: Shepherd SA, Tegner MJ, Guzmán del Próo SA (eds) Abalone of the world: biology, fisheries and culture. Blackwells Scientific Publishers, London, pp 3–18Google Scholar
  29. Muller S (1984) Taxonomy of the genus Haliotis in South Africa. Trans R Soc S Afr 44: 69–77Google Scholar
  30. Nakamura HK (1986) Chromosomes of Archeogastropoda (Mollusca: Prosobranchia), with some remarks on their cytotaxonomy and phylogeny. Publ Seto mar biol Lab 31: 191–267Google Scholar
  31. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Molec Biol Evolut. 3: 418–426Google Scholar
  32. Newman WA (1991) Origins of Southern Hemisphere endemism, especially among marine Crustacea. Mem Qd Mus 31: 51–76Google Scholar
  33. Owen B, McLean JH, Meyer RJ (1971) Hybridization in the eastern Pacific abalones. Sci Bull nat Hist Mus Los Ang Cty 9: 1–37Google Scholar
  34. Pickery R (1991) Chronological list of the references to the original descriptions of recent subgenera and species belonging to the family Haliotidae. Gloria Maris (Bull belg Soc Conch, Antwerpen) 29: 105–118Google Scholar
  35. Pilsbry HA (1890) Manual of conchology. Vol XII. Academy of Natural Sciences, PhiladelphiaGoogle Scholar
  36. Reeve L (1846) Monograph of the genus Haliotis. Conchologia Iconica. 3. (Publication details not known)Google Scholar
  37. Shepherd SA (1975) Distribution, habitat and feeding habits of abalone. Aust Fish 34: 12–15Google Scholar
  38. Smith EFG, Arctander P, Fjeldsa J, Amir OG (1991) Distribution and taxonomy of birds of the world. Yale University Press, New Haven, ConnecticutGoogle Scholar
  39. Sogin ML, Elwood HJ, Gunderson JH (1986) Evolutionary diversity of the eukaryotic small subunit rRNA genes. Proc natn Acad Sci USA 83: 1383–1387Google Scholar
  40. Sohl NF (1992) Upper Cretaceous gastropods (Fissurelidae, Haliotidae, Scisurellidae) from Puerto Rico and Jamaica. J Paleont 66: 81–85Google Scholar
  41. Swofford D (1993) PAUP: Phylogenetic analysis using parsimony. Version 3.1.1. (Computer program). Illinois Natural History Survey, Champaign, IllinoisGoogle Scholar
  42. Talmadge RR (1963) Insular haliotids in the western Pacific (Mollusca: Gastropoda). Veliger 5: 129–139Google Scholar
  43. Ubaldi R (1987) The Haliotis in the Atlantic-Mediterranean area (1). Argonauta 3: 268–290Google Scholar
  44. Vacquier VD, Lee Y-H (1983) Abalone sperm lysin: unusual mode of evolution of a gamete recognition protein. Zygote 1: 181–196Google Scholar
  45. Vermeij GJ (1989) Geographical restriction as a guide to the causes of extinction: the case of the cold northern oceans during the Neogene. Paleobiology 15: 335–356Google Scholar
  46. Weber A (1928) Haliotis diversicolor Rve., Hal. tayloriana Rve., Hal. gruneri Phil. und Hal. supertexta Lischke sind artlich nicht verschieden, sondern identisch. Arch Molluskenk 60: 150–153Google Scholar
  47. Woodring WP (1931) A Miocene Haliotis from southern California. J Paleont 5: 34–39Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Youn-Ho Lee
    • 1
    • 2
  • V. D. Vacquier
    • 2
  1. 1.Division of Biology, 156-29California Institute of TechnologyPasadenaUSA
  2. 2.Marine Biology Research Division and Center for Marine Biomedicine and Biotechnology, Scripps Institution of OceanographyUniversity of California at San DiegoLa JollaUSA

Personalised recommendations