Adaptive Evolution of Sperm Bindin Tracks Egg Incompatibility in Neotropical Sea Urchins of the Genus Echinometra

Molecular Biology and Evolution

Volumn 21, Issue 4, 2004, Pages 732-745

  McCartney, Michael A ^a,b   Lessios, H A ^a  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

Bindin; Echinometra; Gamete recognition; Sea urchin; Speciation

Indexed keywords

BINDIN; COMPLEMENTARY DNA; GAMETE RECOGNITION PROTEIN; MITOCHONDRIAL DNA; PROTEIN; RNA; UNCLASSIFIED DRUG;

ADAPTATION; AMINO ACID SEQUENCE; ARTICLE; EGG; GAMETE; GAMETE RECOGNITION; GENETIC POLYMORPHISM; MEMBRANE FUSION; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEA URCHIN; SPECIES DIFFERENTIATION; SPERM;

ADAPTATION, BIOLOGICAL; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; EVOLUTION, MOLECULAR; GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, GENETIC; SEA URCHINS; SEQUENCE ANALYSIS, DNA;

ECHINOIDEA; ECHINOMETRA; ECHINOMETRA LUCUNTER; ECHINOMETRA VANBRUNTI; ECHINOMETRA VIRIDIS; INVERTEBRATA;

EID: 1842557435     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msh071     Document Type: Article

References (78)

1. Aslan, L. M., and T. Uehara. 1997. Hybridization and Fl backcrosses between two closely related tropical species of sea urchins (genus Echinometra) in Okinawa. Invert. Reprod. Dev. 31:319-324.
2. Bermingham, E. B., and H. A. Lessios. 1993. Rate variation of protein and mtDNA evolution as revealed by sea urchins separated by the Isthmus of Panama. Proc. Natl. Acad. Sci. USA 90:2734-2738.
3. Biermann, C. H. 1998. The molecular evolution of sperm bindin in six species of sea urchins (Echinoida: Strongylocentrotidae). Mol. Biol. Evol. 15:1761-1771.
4. Butlin, R. 1989. Reinforcement of premating isolation. Pp. 158-179. in D. Otte and J. A. Endler, eds., Speciation and its consequences. Sinauer Associates, Sunderland, Mass.
5. Denny, M. W., E. K. Nelson, and K. S. Mead. 2002. Revised estimates of the effects of turbulence on fertilization in the purple sea urchin, Strongylocentrotus purpuratus. Biol. Bull. 203:275-277.
6. Dickerson, R. E., and I. Geis. 1983. Hemoglobin: structure, function, evolution and pathology. Benjamin/Cummings, Menlo Park, Calif.
7. Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:368-376.
8. Frohman, M. A., M. K. Dush, and G. R. Martin. 1988. Rapid production of full-length complementary DNA species from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. USA 85:8998-9002.
9. Gao, B., L. E. Klein, R. J. Britten, and E. H. Davidson. 1986. Sequence of mRNA coding for bindin, a species-specific sea urchin sperm protein required for fertilization. Proc. Natl. Acad. Sci. USA 83:8634-8638.
10. Geyer, L. B. and S. R. Palumbi. 2003. Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins. Evolution 57:1049-1060.
11. Glabe, C. G., and V. D. Vacquier. 1977. Species specific agglutination of eggs by bindin isolated from sea urchin sperm. Nature 267:822-824.
12. Goldman, N., and Z. Yang. 1994. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol. Biol. Evol. 11:725-736.
13. Hellberg, M. E., and V. D. Vacquier. 1999. Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Mol. Biol. Evol. 16:839-848.
14. Holland, B., and W. Rice. 1998. Perspective: chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52:1-7.
15. Howard, D. J. 1993. Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis. Pp. 46-69. in R. G. Harrison, ed., Hybrid zones and the evolutionary process. Oxford University Press, New York.
16. Kamei, N., and C. G. Glabe. 2003. The species-specific egg receptor for sea urchin sperm adhesion is EBR1, a novel ADAMTS protein. Genes Dev. 17:2502-2507.
17. Kirkpatrick, M., and V. Ravigne. 2002. Speciation by natural and sexual selection: models and experiments. Am. Nat. 159(Suppl S):S22-S35.
18. Kishino, H., and M. Hasegawa. 1989. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in the Hominoidea. J. Mol. Evol. 29:170-179.
19. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA2: molecular evolutionary genetics analysis. Arizona State University, Tempe, Ariz.
20. Landry, C., L. B. Geyer, Y. Arakaki, T. Uehara, and S. R. Palumbi. 2003. Recent speciation in the Indo-West Pacific: rapid evolution of gamete recognition and sperm morphology in cryptic species of sea urchin. Proc. R. Soc. Ser. B. 270:1839-1847.
21. Lee, Y. H., T. Ota, and V. D. Vacquier. 1995. Positive selection is a general phenomenon in the evolution of abalone sperm lysin. Mol. Biol. Evol. 12:231-238.
22. Lee, Y. H., and V. D. Vacquier. 1992. The divergence of species-specific abalone sperm lysins is promoted by positive Darwinian selection. Biol. Bull. 182:97-104.
23. Lessios, H. A. 1979. Use of Panamanian sea urchins to test the molecular clock. Nature 280:599-601.
24. -. 1981. Reproductive periodicity of the echinoids Diadema and Echinometra on the two coasts of Panama. J. Exp. Mar. Biol. Ecol. 50:47-61.
25. Lessios, H. A., J. D. Cubit, D. R. Robertson, M. J. Shulman, M. R. Parker, S. D. Garrity, and S. C. Levings. 1984. Mass mortality of Diadema antillarum on the Caribbean coast of Panama. Coral Reefs 3:173-182.
26. Lessios, H. A., and C. W. Cunningham. 1990. Gametic incompatibility between species of the sea urchin Echinometra on the two sides of the Isthmus of Panama. Evolution 44:933-941.
27. Levitan, D. R. 1991. Influence of body size and population density on fertilization success and reproductive output in a free-spawning invertebrate. Biol. Bull. 181:261-268.
28. -. 1998. Sperm limitation, gamete competition, and sexual selection in external fertilizers. Pp. 173-215 in T. Birkhead and A. Moller, eds., Sperm competition and sexual selection. Academic Press, New York.
29. -. 2002. The relationship between conspecific fertilization success and reproductive isolation among three congeneric sea urchins. Evolution 56:1599-1609.
30. Lewis, C. A., C. F. Talbot, and V. D. Vacquier. 1982. A protein from abalone Haliotis rufescens sperm dissolves the egg vitelline layer by a nonenzymatic mechanism. Dev. Biol. 92:227-239.
31. Li, W.-H. 1993. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol. Evol. 36:96-99.
32. McCartney, M. A., G. Keller, and H. A. Lessios. 2000. Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol. Ecol. 9:1391-1400.
33. McCartney, M. A., and H. A. Lessios. 2002. Quantitative analysis of gametic incompatibility between closely related species of neotropical sea urchins. Biol. Bull. 202:166-181.
34. McClary, D. J., and M. A. Sewell. 2003. Hybridization in the sea: gametic and developmental constraints on fertilization in sympatric species of Pseudechinus (Echinodermata: Echinoidea). J. Exp. Mar. Biol. Ecol. 284:51-70
35. McDonald, J. H., and M. Kreitman. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654.
36. Metz, E. C., G. Gomez-Gutierrez, and V. D. Vacquier. 1998. Mitochondrial DNA and bindin gene sequence evolution among allopatric species of the sea urchin genus Arbacia. Mol. Biol. and Evolution 15:185-195.
37. Metz, E. C., R. E. Kane, H. Yanagimachi, and S. R. Palumbi. 1994. Fertilization between closely related sea urchins is blocked by incompatibilities during sperm-egg attachment and early stages of fusion. Biol. Bull. 187:23-34.
38. Metz, E. C., and S. R. Palumbi. 1996. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol. Biol. Evol. 13:397-406.
39. Metz, E. C., R. Robles-Sikisaka, and V. D. Vacquier. 1998. Nonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA. Proc. Natl. Acad. Sci. USA 95:10676-10681.
40. Minor, J. E., D. R. Fromson, R. J. Britten, and E. H. Davidson. 1991. Comparison of the bindin proteins of Strongylocentrotus franciscanus, S. purpuratus, and Lytechinus variegatus: sequences involved in the species specificity of fertilization. Mol. Biol. Evol. 8:781-795.
41. Moy, G. W., and V. D. Vacquier. 1979. Immunoperoxidase localization of bindin during the adhesion of sperm to sea urchin eggs. Curr. Topics Dev. Biol. 13:31-44.
42. Noor, M. A. F. 1999. Reinforcement and other consequences of sympatry. Heredity 83:503-508.
43. Ohta, T. 2000. Mechanisms of molecular evolution. Phil. Trans. R. Soc. Lond. Ser. B Biol. Sci. 355:1623-1626.
44. Palumbi, S. R. 1992. Marine speciation on a small planet. Trends Ecol. Evol. 7:114-118.
45. -. 1994. Genetic divergence, reproductive isolation, and marine speciation. Annu. Rev. Ecol. Syst. 25:547-572.
46. -. 1999. All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc. Natl. Acad. Sci. USA 96:12632-12637.
47. Palumbi, S. R., and E. C. Metz. 1991. Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol. Biol. Evol. 8:227-239.
48. Pamilo, P., and O. Bianchi. 1993. Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol. Biol. Evol. 10:271-281.
49. Pennington, J. T. 1985. The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol. Bull. 169:417-430.
50. Posada, D., and K. A. Crandall. 1998. ModelTest: testing the model of DNA substitution. Bioinformatics 14:817-818.
51. Rice, W. R. 1998. Intergenomic conflict, interlocus antagonistic coevolution, and evolution of reproductive isolation. Pp. 261-270 in D. J. Howard and S. H. Berlocher. eds., Endless forms. Species and speciation. Oxford University Press, New York.
52. Rice, W. R., and B. Holland. 1997. The enemies within: intergenomic conflict, interlocus contest evolution (ICE) and the intraspecific Red Queen. Behav. Ecol. Sociobiol. 41:1-10.
53. Rozas, J., and R. Rozas. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175.
54. Sambrook, E., F. Fritsch, and T. Maniatis. 1989. Molecular cloning. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
55. Shaw, A., Y.-H. Lee, D. Stout, and V. D. Vacquier. 1994. The species-specificity and structure of abalone sperm lysin. Semin. Dev. Biol. 5:209-215.
56. Shimodaira, H., and M. Hasegawa. 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16:1114-1116.
57. Sokal, R. R., and F. J. Rohlf. 1981. Biometry. W. H. Freeman, New York.
58. Strathmann, R. R. 1981. On barriers to hybridization between Strongylocentrotus droebachiensis (O.F. Muller) and S. pallidus (G.O. Sars). J. Exp. Mar. Biol. Ecol. 55:39-47
59. Summers, R. G., and B. L. Hylander. 1975. Species-specificity of acrosome reaction and primary gamete binding in echinoids. Exp. Cell Res. 96:63-68.
60. Swanson, W. J., and V. D. Vacquier. 1997. The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule. Proc. Natl. Acad. Sci. USA 94:6724-6729.
61. -. 2002. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3:137-144.
62. Swofford, D. L. 2002. Phylogenetic analysis using parsimony (PAUP*), beta version. Sinauer Associates, Sunderland, Mass.
63. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
64. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
65. Ulrich, A. S., M. Otter, C. G. Glabe, and D. Hoekstra. 1998. Membrane fusion is induced by a distinct peptide sequence of the sea urchin fertilization protein bindin. J. Biol. Chem. 273:16748-16755.
66. Vacquier, V. D. 1998. Evolution of gamete recognition proteins. Science 281:1995-1998.
67. Vacquier, V. D., K. R. Carner, and C. D. Stout. 1990. Species-specific sequences of abalone lysin, the sperm protein that creates a hole in the egg envelope. Proc. Natl. Acad. Sci. 87:5792-5796.
68. Vacquier, V. D., and G. W. Moy. 1977. Isolation of bindin: the protein responsible for adhesion of sperm to sea urchin eggs. Proc. Natl. Acad. Sci. 74:2456-2460.
69. Vacquier, V. D., W. J. Swanson, and M. E. Hellberg. 1995. What have we learned about sea urchin sperm bindin? Dev. Growth Differ. 37:1-10.
70. Van Doom, G. S., P. C. Luttikhuizen, and F. J. Weissing. 2001. Sexual selection at the protein level drives the extraordinary divergence of sex-related genes during sympatric speciation. Proc. R. Soc. Lond. Ser. B 268:2155-2161.
71. West-Eberhard, M. J. 1983. Sexual selection, social competition, and speciation. Q. Rev. Biol. 58:155-183.
72. Yang, Z. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15:568-573.
73. -. 2000. PAML: phylogenetic analysis by maximum likelihood. University College London, London, U.K.
74. Yang, Z., and R. Nielsen. 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol. 19:908-917.
75. Yang, Z., R. Nielsen, N. Goldman, and A. M. K. Pedersen. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431-449.
76. Zigler, K., and H. A. Lessios. 2003a. Evolution of bindin in the pantropical sea urchin Tripneustes: comparisons to bindin of other genera. Mol. Biol. Evol. 20:220-231.
77. -. 2003b. Evolution of the gamete recognition protein bindin across six orders of sea urchins. Biol. Bull. 205:8-15.
78. Zigler, K. S., E. C. Raff, E. Popodi, R. A. Raff, and H. A. Lessios. 2003. Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57:2293-2302.