Journal of Molecular Evolution

, Volume 44, Supplement 1, pp S15–S22

Positive darwinian selection on two homologous fertilization proteins: what is the selective pressure driving their divergence?

  • Victor D. Vacquier
  • Willie J. Swanson
  • Youn-Ho Lee
Molecular population genetic

Abstract

Most examples of positive selection inferred from nucleotide sequence data involve host-pathogen interactions. However, positive selection also promotes the divergence of proteins mediating spermegg recognition in marine invertebrates. The abalone spermatozoon has a large acrosomal vesicle containing two proteins of 16 kDa and 18 kDa. Lysin, the 16-kDa protein, exhibits species-specificity in dissolving a hole in the egg vitelline envelope through which the sperm swims to reach the egg plasma membrane. The 18-kDa protein coats the sperm acrosomal process and probably mediates fusion of the two gametes. In this review, we compare sequences of both proteins from five species of California abalones. Both proteins show extensive divergence which has been promoted by positive Darwinian selection. The ratios of nonsynonymous to synonymous nucleotide substitutions may be the highest yet discovered for full-length sequences. Although extensive divergence has occurred, there is conservation of the shape and polarity of residues in both proteins. The two acrosomal proteins arose by a gene duplication followed by their extensive divergence. Five hypotheses are presented which attempt to explain the nature of the unknown selective force responsible for the robust positive selection. The positive selection may, in some unknown way, be related to the establishment of prezygotic barriers to reproduction. Because positive selection promotes the divergence of unrelated, species-specific gamete recognition proteins in both abalones and sea urchins, we predict that positive selection may be a general phenomenon in the evolution of gamete recognition systems in marine invertebrates.

Key words

Selective pressure Darwinian selection Homologous fertilization proteins 

References

  1. Andersson MB (1994) Sexual selection. Princeton University Press, Princeton, NJGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 21:403–410Google Scholar
  3. Bayne CJ (1990) Phagocytosis and non-self recognition in invertebrates. Bioscience 40:723–731CrossRefGoogle Scholar
  4. Biosym Profiles 3D users guide (1993) Version 2.3.0, Biosym Technologies, San DiegoGoogle Scholar
  5. Bowie JU, Luthy R, Eisenberg D (1991) A method to identify protein sequences that fold into a known three-dimensional structure. Science 253:164–170PubMedCrossRefGoogle Scholar
  6. Darwin C (1871) The descent of man and selection in relationship to sex. John Murray, LondonGoogle Scholar
  7. Dobzhansky Th (1940) Speciation as a stage in evolutionary divergence. Am Nat 74:312–321CrossRefGoogle Scholar
  8. Endo T, Ikeo K, Gojobori T (1996) Large-scale search for genes on which positive selection may operate. Mol Biol Evol 13:685–690PubMedGoogle Scholar
  9. Foltz KR (1995) Sperm-binding proteins. Int Rev Cytol 163:249–303PubMedCrossRefGoogle Scholar
  10. Genetics Computer Group (1991) Program manual for the GCG package, Version 7, University of Wisconsin, MadisonGoogle Scholar
  11. Gribskov M, Luthy R, Eisenberg D (1990) Profile analysis. Methods Enzymol 183:146–159PubMedCrossRefGoogle Scholar
  12. Haino-Fukushima K, Usui N (1986) Purification and immunocytochemical localization of the vitelline coat lysin of abalone spermatozoa. Dev Biol 115:27–34CrossRefGoogle Scholar
  13. Haino-Fukushima K, Kasai H, Isobe T, Kimura M, Okuyama T (1986) The complete amino acid sequence of vitelline coat lysin. Eur J Biochem 154:503–510PubMedCrossRefGoogle Scholar
  14. Howard DJ (1993) Reinforcement: origins, dynamics and fate of an evolutionary hypothesis. In: Harrison RG (ed) Hybrid zones and the evolutionary hypothesis. Oxford University Press, Oxford, pp 46–69Google Scholar
  15. Hughes AL (1994) The evolution of functionally novel proteins after gene duplication. Proc R Soc Lond [Biol] 256:119–124CrossRefGoogle Scholar
  16. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex loci reveals overdominant selection. Nature 35:167–170CrossRefGoogle Scholar
  17. Hughes AL, Ota T, Nei M (1990) Positive-Darwinian selection promotes charge profile diversity in the antigen binding cleft of Class I major histocompatibility complex molecules. Mol Biol Evol 7: 515–524PubMedGoogle Scholar
  18. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, p 21Google Scholar
  19. Kumar S, Tamura K, Nei M (1993) MEGA: molecular evolutionary genetics analysis, version 1.01. The Pennsylvania State University, University Park, PA 16802Google Scholar
  20. Lee Y-H (1994) Abalone sperm lysin: molecular evolution of a fertilization protein, implications concerning the species-specificity of fertilization and speciation in marine invertebrates. PhD Thesis, University of California, San DiegoGoogle Scholar
  21. Lee Y-H, Vacquier VD (1992) The divergence of species-specific abalone sperm lysins is promoted by positive Darwinian selection. Biol Bull 182:97–104CrossRefGoogle Scholar
  22. Lee Y-H, Vacquier VD (1995) Evolution and systematics in Haliotidae (mollusca: gastropoda): inference from DNA sequences of sperm lysin. Marine Biol 124:267–278CrossRefGoogle Scholar
  23. Lee Y-H, Ota T, Vacquier VD (1995) Positive selection is a general phenomenon in the evolution of abalone sperm lysin. Mol Biol Evol 12:231–238PubMedGoogle Scholar
  24. Lindberg DR (1991) 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, London, p3Google Scholar
  25. Liou LW, Price TD (1994) Speciation by reinforcement of premating isolation. Evolution 48:1451–1459CrossRefGoogle Scholar
  26. Metz EC, Palumbi SR (1996) Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol Biol Evol 13:397–406PubMedGoogle Scholar
  27. Metz EC, Kane RE, Yanagimachi H, Palumbi SR (1994) Fertilization between closely related sea urchins is blocked by incompatibilities during sperm-egg attachment and early stages of fusion. Biol Bull 187:23–34CrossRefGoogle Scholar
  28. Miraglia SJ, Glabe CG (1993) Characterization of the membrane-associating domain of the sperm adhesive protein, bindin. Biochim Biophys Acta 1145:191–198PubMedCrossRefGoogle Scholar
  29. Miyata T, Miyazawa S, Yasunaga T (1979) Two types of amino acid substitutions in protein evolution. J Mol Evol 12:219–236PubMedCrossRefGoogle Scholar
  30. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  31. Nei M, Chakraborty R, Fuerst PA (1976) Infinite allele model with varying mutational rate. Proc Natl Acad Sci USA 73:4164–4168PubMedCrossRefGoogle Scholar
  32. Noor MA (1995) Speciation driven by natural selection in Drosophila. Nature 375:674–675PubMedCrossRefGoogle Scholar
  33. Palumbi SR (1994) Genetic divergence, reproductive isolation and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  34. Palumbi SR, Metz EC (1991) Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol Biol Evol 8:227–239PubMedGoogle Scholar
  35. Pearson WR, Lipman DJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85:2444–2448PubMedCrossRefGoogle Scholar
  36. Rice WR (1996) Sexual antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232–234PubMedCrossRefGoogle Scholar
  37. Rice WR, Hostert EE (1993) Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47:1637–1653CrossRefGoogle Scholar
  38. Rost B, Sander C (1994) Combining evolutionary information and neural networks to predict protein secondary structure. Proteins 19:55–72PubMedCrossRefGoogle Scholar
  39. Shaw A, McRee DE, Vacquier VD, Stout CD (1993) The crystal structure of abalone sperm lysin. Science 262:1864–1867PubMedCrossRefGoogle Scholar
  40. Shaw A, Fortes PGA, Stout CD, Vacquier VD (1995) Crystal structure and subunit dynamics of the abalone sperm lysin dimer: egg envelopes dissociate dimers, the monomer is the active species. J Cell Biol 130:1117–1125PubMedCrossRefGoogle Scholar
  41. Smith DW (1988) A complete, yet flexible, system for DNA/protein sequence analysis using VAX/VMS computers. Comput Appl Biosci 4:212PubMedGoogle Scholar
  42. Swanson WJ, Vacquier VD (1995a) Liposome fusion induced by a Mr 18,000 protein localized to the acrosomal region of acrosome-reactive abalone spermatozoa. Biochemistry 34:14202–14208PubMedCrossRefGoogle Scholar
  43. Swanson WJ, Vacquier VD (1995b) Extraordinary divergence and positive Darwinian selection in a fusagenic protein coating the acrosomal process of abalone spermatozoa. Proc Natl Acad Sci USA 92:4957–4961CrossRefGoogle Scholar
  44. Uzzell T, Corbin KW (1971) Fitting discrete probability distributions to evolutionary events. Science 172:1089–1096PubMedCrossRefGoogle Scholar
  45. Vacquier VD, Lee Y-H(1993) Abalone sperm lysin: unusual mode of evolution of a gamete recognition protein. Zygote 1:181–196PubMedCrossRefGoogle Scholar
  46. Vacquier VD, Carner KR, Stout CD (1990) Species-specific sequences of abalone sperm lysin, the sperm protein that creates a hole in the egg envelope. Proc Natl Acad Sci USA 87:5792–5796PubMedCrossRefGoogle Scholar
  47. Vacquier VD, Swanson WJ, Hellberg ME (1995) What have we learned about sea urchin sperm bindin? Dev Growth Differ 37:1–10CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1997

Authors and Affiliations

  • Victor D. Vacquier
    • 1
  • Willie J. Swanson
    • 1
  • Youn-Ho Lee
    • 1
  1. 1.Marine Biology Research Division, Scripps Institution of OceanographyUniversity of CaliforniaSan Diego, La JollaUSA
  2. 2.Division of BiologyCalifornia Institute of TechnologyPasadenaUSA

Personalised recommendations