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Characterization of the Sperm Molecule Bindin in the Sea Urchin Genus Paracentrotus

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Abstract

Bindin is a sea urchin gamete-recognition protein that plays an essential role in the specificity of egg–sperm interactions and thus may be evolving under sexual selection and be related to speciation. Bindin has been found to evolve under strong selection in some sea urchin genera and neutrally in others. In this study, we characterized bindin in the two extant species of the genus Paracentrotus: P. lividus from the Atlanto-Mediterranean region and P. gaimardi from Brazil. The structure of the bindin molecule in Paracentrotus is similar to that of other genera studied thus far, consisting of a conserved core flanked by two variable regions and an intron of variable length located at the same conserved position as in other genera. Polymorphism in P. lividus is caused mainly by point substitutions and insertions/deletions, and length variations are caused mainly by the number of repeated motifs in the flanking regions. There is no evidence of recombination. Positive selection is acting on amino acid sites located in two regions flanking the conserved core.

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References

  • Biermann CH (1998) The molecular evolution of sperm bindin in six species of sea urchins (Echinoidea: Strongylocentrotidae). Mol Biol Evol 15:1761–1771

    PubMed  CAS  Google Scholar 

  • Boudouresque CF, Verlaque M (2001) Ecology of Paracentrotus lividus. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, The Netherlands, pp 177–216

    Chapter  Google Scholar 

  • Brendel V, Bucher P, Nourbakhsh I, Blaisdell BE, Karlin S (1992) Methods and algorithms for statistical analysis of protein sequences. Proc Natl Acad Sci USA 89:2002–2006

    Article  PubMed  CAS  Google Scholar 

  • Calderón I, Giribet G, Turon X (2008) Two markers and one history: phylogeography of the edible common sea urchin Paracentrotus lividus in the Lusitanian region. Mar Biol 154:137–151

    Article  Google Scholar 

  • Calderón I, Turon X, Pascual M (2009) Isolation of 9 nuclear microsatellites in the common Mediterranean sea urchin Paracentrotus lividus (Lamarck). Mol Ecol Resour. doi:10.111/j.1577.0998.2009.02585.x

  • Civetta A, Singh RS (1998) Sex-related genes, directional sexual selection, and speciation. Mol Biol Evol 15:901–909

    PubMed  CAS  Google Scholar 

  • Coyne JA (1992) Genetics and speciation. Nature 35:511–515

    Article  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland, MA

    Google Scholar 

  • Coyne KJ, Qin XX, Waite JH (1997) Extensible collagen in mussel byssus—a natural block copolymer. Science 277:1830–1832

    Article  PubMed  CAS  Google Scholar 

  • Crandall KA, Kelsey CR, Imamichi H, Lane HC, Salzman NP (1999) Parallel evolution of drug resistance in HIV: failure of nonsynonymous/synonymous substitution rate ratio to detect selection. Mol Biol Evol 16:372–382

    PubMed  CAS  Google Scholar 

  • Duran S, Palacín C, Becerro MA, Turon X, Giribet G (2004) Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Mol Ecol 13:3317–3328

    Article  PubMed  CAS  Google Scholar 

  • Ferris PJ, Armbrust EV, Goodenough EH (2002) Genetic structure of the mating-type locus of Chlamydomonas reinhardtii. Genetics 160:181–200

    PubMed  CAS  Google Scholar 

  • Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998–9002

    Article  PubMed  CAS  Google Scholar 

  • Gao B, Klein LE, Britten RJ, Davidson EH (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

    Article  PubMed  CAS  Google Scholar 

  • Geyer LB, Palumbi SR (2003) Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins. Evolution 57:1049–1060

    PubMed  Google Scholar 

  • Glabe CG, Lennarz WJ (1979) Species-specific sperm adhesion in sea urchins: a quantitative investigation of bindin-mediated egg agglutination. J Cell Biol 83:595–604

    Article  PubMed  CAS  Google Scholar 

  • Glabe CG, Vacquier VD (1977) Species specific agglutination of eggs of bindin isolated from sea urchin sperm. Nature 267:822–824

    Article  Google Scholar 

  • Guerette PA, Ginzinger DG, Weber BH, Gosline JM (1996) Silk properties determined by gland-specific expression of a spider fibroin gene family. Science 272:112–115

    Article  PubMed  CAS  Google Scholar 

  • Hellberg ME, Vacquier VD (1999) Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Mol Biol Evol 16:839–848

    PubMed  CAS  Google Scholar 

  • Howard DJ (1999) Conspecific sperm and pollen precedence and speciation. Annu Rev Ecol Syst 30:109–133

    Article  Google Scholar 

  • Hughes AL (1993) Coevolution of immunogenic proteins of Plasmodium falciparum and the host’s immune system. In: Takahata N, Clark AG (eds) Mechanisms of molecular evolution. Sinauer, Sunderland, MA, pp 109–127

    Google Scholar 

  • Jobb G (2007) TREEFINDER February 2007 version. Munich, Germany. Available at: http://www.treefinder.de. Accessed June 2008

  • Lee Y, Vacquier VD (1992) The divergence of species-specific abalone sperm lysins is promoted by positive Darwinian selection. Biol Bull 182:97–104

    Article  CAS  Google Scholar 

  • Lee Y, Ota T, Vacquier VD (1995) Positive selection is a general phenomenon in the evolution of abalone sperm lysin. Mol Biol Evol 12:231–238

    PubMed  CAS  Google Scholar 

  • Lessios HA (2007) Reproductive isolation between species of sea urchins. Bull Mar Sci 81:191–208

    Google Scholar 

  • Lessios HA (2008) The Great American schism: divergence of marine organisms after the rise of the Central American Isthmus. Annu Rev Ecol Evol Syst 39:63–91

    Article  Google Scholar 

  • Levitan DR, Farrell DL (2006) Selection on gamete recognition proteins depends on sex, density and genotype frequency. Science 312:267–269

    Article  PubMed  CAS  Google Scholar 

  • Li WH (1993) Unbiased estimation of the rates of synonymous and nonsynonymous substitutions. J Mol Evol 36:96–99

    Article  PubMed  CAS  Google Scholar 

  • Lopez A, Miraglia SJ, Glabe CG (1993) Structure/function analysis of the sea urchin sperm adhesive protein bindin. Dev Biol 156:24–33

    Article  PubMed  CAS  Google Scholar 

  • Martin DP, Williamson C, Posada D (2005) RDP2: Recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262

    Article  PubMed  CAS  Google Scholar 

  • McCartney MA, Lessios HA (2004) Adaptive evolution of sperm bindin tracks egg incompatibility in neotropical sea urchins of the genus Echinometra. Mol Biol Evol 21:732–745

    Article  PubMed  CAS  Google Scholar 

  • McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654

    Article  PubMed  CAS  Google Scholar 

  • Metz EC, Palumbi SR (1996) Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol Biol Evol 13:397–406

    PubMed  CAS  Google Scholar 

  • Metz EC, Kane RE, Yanagamachi 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 187:23–34

    Article  Google Scholar 

  • Metz EC, Gómez-Gutiérrez G, Vacquier VD (1998) Mitochondrial DNA and bindin gene sequence evolution among allopatric species of the sea urchin genus Arbacia. Mol Biol Evol 15:185–195

    PubMed  CAS  Google Scholar 

  • Minor JE, Fromson DR, Britten RJ, Davidson EH (1991) Comparison of bindin proteins of Strongylocentrotus franciscanus, S. purpuratus and Lytechinus variegatus: Sequences involved in the species-specificity of fertilization. Mol Biol Evol 8:681–795

    Google Scholar 

  • Mortensen T (1943) A monograph of the Echinoidea. Camarodonta, vol. III. C. A. Reitzel, Copenhagen, Denmark

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, NY

    Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous substitutions. Mol Biol Evol 3:418–426

    PubMed  CAS  Google Scholar 

  • Nielsen R, Yang Z (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929–936

    PubMed  CAS  Google Scholar 

  • Palacín C, Turon X, Ballesteros M, Giribet G, López S (1998) Stock evaluation of three littoral echinoid species on the Catalan Coast (North-Western Mediterranean). Pubblicazione della Stazione Zoologica di Napoli: Mar Ecol 19:163–177

    Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Palumbi SR (1998) Species formation and the evolution of gamete recognition loci. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, Oxford, UK, pp 271–278

    Google Scholar 

  • Palumbi SR (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

    Article  PubMed  CAS  Google Scholar 

  • Pamilo P, Bianchi O (1993) Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol Biol Evol 10:271–281

    PubMed  CAS  Google Scholar 

  • Park DJ, Pask AJ, Renfree MB, Graves JA (2003) 3′ RACE walking along a large cDNA employing tiered suppression PCR. Biotechniques 34(750–752):754–756

    Google Scholar 

  • Posada D (2006) ModelTest Server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucl Ac Res 34:700–703

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez del Barrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Swanson WJ, Vacquier VD (1995) Extraordinary divergence and positive Darwinian selection in a fusagenic protein coating the acrosomal process of abalone spermatozoa. Proc Natl Acad Sci USA 92:4957–4961

    Article  PubMed  CAS  Google Scholar 

  • Swanson WJ, Vacquier VD (1997) The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule. Proc Natl Acad Sci USA 94:6724–6729

    Article  PubMed  CAS  Google Scholar 

  • Swanson WJ, Vacquier VD (2002) Rapid evolution of reproductive proteins. Nature Rev Genet 3:137–144

    Article  CAS  Google Scholar 

  • Swanson WJ, Yang Z, Wolfner MF, Aquadro CF (2001) Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc Natl Acad Sci USA 98:2509–2514

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Ulrich AS, Otter M, Glabe CG, Hoekstra D (1998) Membrane fusion is induced by a distinct peptide sequence of the sea urchin fertilization protein bindin. J Biol Chem 273:16748–16755

    Article  PubMed  CAS  Google Scholar 

  • Ulrich AS, Tichelaar W, Forster G, Zschornig O, Weinkauf S, Meyer HW (1999) Ultrastructural characterization of peptide-induced membrane fusion and peptide self-assembly in the lipid bilayer. Biophys J 77:829–841

    Article  PubMed  CAS  Google Scholar 

  • Vacquier VD (1998) Evolution of gamete recognition proteins. Science 281:1995–1998

    Article  PubMed  CAS  Google Scholar 

  • Vacquier VD, Moy GW (1977) Isolation of bindin: the protein responsible for adhesion of sperm to sea urchin eggs. Proc Nat Acad Sci USA 74:2456–2460

    Article  PubMed  CAS  Google Scholar 

  • Vacquier VD, Swanson WJ, Hellberg ME (1995) What have we learned about sea urchin sperm bindin? Dev Growth Differ 37:1–10

    Article  CAS  Google Scholar 

  • Vacquier VD, Swanson WJ, Lee Y (1997) Positive Darwinian selection on two homologous fertilization proteins: what is the selective pressure driving their divergence? J Mol Evol 44(Suppl 1):S15–S22

    Article  PubMed  CAS  Google Scholar 

  • Villablanca FX, Roderick GK, Palumbi SR (1998) Invasion genetics of the Mediterranean fruit fly: variation in multiple nuclear introns. Mol Ecol 7:547–560

    Article  PubMed  CAS  Google Scholar 

  • Wright F (1990) The “effective number of codons” used in a gene. Gene 87:23–29

    Article  PubMed  CAS  Google Scholar 

  • Yang Z (2007) PAML4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Nielsen R, Goldman N, Krabbe Pedersen AM (2000) Codon substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    PubMed  CAS  Google Scholar 

  • Yang Z, Wong WSW, Nielsen R (2005) Bayes Empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Kumar S, Nei M (1997) Small-sample tests of episodic evolution: a case study of primate lysozymes. Mol Biol Evol 14:1335–1338

    PubMed  CAS  Google Scholar 

  • Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22:2472–2479

    Article  PubMed  CAS  Google Scholar 

  • Zigler KS, Lessios HA (2003a) 250 million years of bindin evolution. Biol Bull 205:8–15

    Article  PubMed  CAS  Google Scholar 

  • Zigler KS, Lessios HA (2003b) Evolution of bindin in the pantropical sea urchin Tripneustes: Comparisons to bindin of other genera. Mol Biol Evol 20:220–231

    Article  PubMed  CAS  Google Scholar 

  • Zigler KS, Lessios HA (2004) Speciation on the coasts of the new world: Phylogeography and the evolution of bindin in the sea urchin genus Lytechinus. Evolution 56:1225–1241

    Google Scholar 

  • Zigler KS, Raff EC, Popodi E, Raff RA, Lessios HA (2003) Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57:2293–2302

    PubMed  CAS  Google Scholar 

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Acknowledgements

Special thanks to Axel and Ligia Calderón of STRI-Naos for their help in the laboratory. Thanks to Laura Geyer for providing useful comments on the manuscript. This research was funded by Project No. CTM2007-66635 of the Spanish Government and by general research funds from the Smithsonian Tropical Research Institute.

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Authors and Affiliations

  1. Department of Animal Biology, Faculty of Biology, University of Barcelona, 08028, Barcelona, Spain

    Isabel Calderón

  2. Center for Advanced Studies of Blanes (CEAB, CSIC), Blanes, Girona, Spain

    Xavier Turon

  3. Smithsonian Tropical Research Institute, Balboa, Republic of Panama

    H. A. Lessios

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  1. Isabel Calderón
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  2. Xavier Turon
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  3. H. A. Lessios
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Correspondence to Isabel Calderón.

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Calderón, I., Turon, X. & Lessios, H.A. Characterization of the Sperm Molecule Bindin in the Sea Urchin Genus Paracentrotus . J Mol Evol 68, 366–376 (2009). https://doi.org/10.1007/s00239-009-9219-4

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