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

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Characterization of the Sperm Molecule Bindin in the Sea Urchin Genus Paracentrotus J Mol Evol (2009) 68:366–376 DOI 10.1007/s00239-009-9219-4 Characterization of the Sperm Molecule Bindin in the Sea Urchin Genus Paracentrotus Isabel Caldero´n Æ Xavier Turon Æ H. A. Lessios Received: 29 October 2008 / Accepted: 19 February 2009 / Published online: 28 March 2009 Ó Springer Science+Business Media, LLC 2009 Abstract Bindin is a sea urchin gamete-recognition Introduction protein that plays an essential role in the specificity of egg– sperm interactions and thus may be evolving under sexual Proteins involved in reproduction and, more specifically, in selection and be related to speciation. Bindin has been gamete recognition—which control the binding and fusion found to evolve under strong selection in some sea urchin of gametes—may play an essential role in reproductive genera and neutrally in others. In this study, we charac- isolation and speciation in marine organisms (reviewed in terized bindin in the two extant species of the genus Palumbi 1994, 1998; Vacquier et al. 1995; Swanson and Paracentrotus: P. lividus from the Atlanto-Mediterranean Vacquier 2002; Lessios 2007). Reproductive isolation in region and P. gaimardi from Brazil. The structure of the broadcast spawners may be caused by a number of factors, bindin molecule in Paracentrotus is similar to that of other such as nonoverlapping spawning times, chemical genera studied thus far, consisting of a conserved core communication, or species-specific gamete interactions. flanked by two variable regions and an intron of variable Although evolutionary theory suggests that traits closely length located at the same conserved position as in other related to fitness are under purifying selection (Nei 1987), genera. Polymorphism in P. lividus is caused mainly by reproductive proteins often show high rates of diversifica- point substitutions and insertions/deletions, and length tion (Civetta and Singh 1998; Swanson and Vacquier variations are caused mainly by the number of repeated 2002). Evolutionary patterns of proteins directly implicated motifs in the flanking regions. There is no evidence of in reproductive isolation can provide important information recombination. Positive selection is acting on amino acid on speciation processes (Coyne 1992; Palumbi 1994; sites located in two regions flanking the conserved core. Coyne and Orr 2004). Marine invertebrates often possess gamete-recognition Keywords Bindin Á PAML Á Paracentrotus Á proteins that are subject to positive selection. In abalones Positive selection Á Sea urchins Á Speciation and teguline gastropods, several studies have identified the role of positively selected amino acid sites scattered over the entire length of the protein lysin (Lee and Vacquier 1992; Lee et al. 1995; Swanson and Vacquier 1997) that I. Caldero´n(&) affect secondary structure of the protein (Hellberg and Department of Animal Biology, Faculty of Biology, University Vacquier 1999). The abalone lysin changes under positive of Barcelona, 08028 Barcelona, Spain selection to adapt to variations of the receptor molecule, e-mail: [email protected] VERL, located on the egg’s surface (Swanson and Vac- X. Turon quier 2002). Interestingly, another abalone sperm protein, Center for Advanced Studies of Blanes (CEAB, CSIC), Blanes, sp18, a paralog of lysin (Vacquier et al. 1997), is among Girona, Spain the most rapidly evolving metazoan proteins known (Swanson and Vacquier 1995). H. A. Lessios Smithsonian Tropical Research Institute, Balboa, Republic In sea urchins, the protein bindin constitutes the major of Panama insoluble component of the sperm acrosomal vesicle 123 J Mol Evol (2009) 68:366–376 367 (Vacquier and Moy 1977; Ulrich et al. 1998). When sperm from the Gulf of Guinea to Angola on the African coast and undergo the acrosomal reaction, bindin is deposited on the from Rio de Janeiro to Florianopolis along the coast of tip of the sperm acrosomal process after exocytosis from Brazil (Mortensen 1943). Recent studies suggest that P. the vesicle. This protein mediates adhesion of sperm to lividus can maintain gene flow over thousands of kilome- eggs and fusion between their membranes in a species- tres (Duran et al. 2004; Caldero´n et al. 2008). Similarly, the specific manner, this being the key stage of the recognition presence of P. gaimardi on both sides of the Atlantic Ocean process (Glabe and Vacquier 1977; Glabe and Lennarz suggests that its larvae can also disperse over long dis- 1979; Metz et al. 1994; Vacquier et al. 1995; Vacquier tances. The genetic distance between the two species based 1998). on the mitochondrial ATPase 8 and 6 regions is approxi- The last few years have seen an increase in the number mately 1.6% (Lessios, unpublished data), which, when of studies aimed at understanding the evolution of bindin in calibrated by divergence in the same DNA region of other various sea urchin genera. Zigler and Lessios (2003a) sea urchins by the rise of the Isthmus of Panama (Lessios found that bindin was present in a common ancestor of all 2008), suggests that P. lividus and P. gaimardi have been extant sea urchins [250 million years ago. Different evo- isolated during the last half million years. Thus, these two lutionary patterns have been observed in the 10 genera of allopatric species provide an interesting model for the echinoids for which bindin has been studied thus far study of the evolution of bindin. In this study, we charac- (Lessios 2007). Positive selection has been detected in terized the gene coding for bindin in the genus particular domains of bindin in the genera Echinometra Paracentrotus, and we studied the intraspecific polymor- (Metz and Palumbi 1996; Geyer and Palumbi 2003; Mc- phism and mode of evolution in P. lividus. Cartney and Lessios 2004), Strongylocentrotus (Biermann 1998), and Heliocidaris (Zigler et al. 2003), whereas purifying selection or neutral evolution has been found in Materials and Methods Arbacia (Metz et al. 1998), Tripneustes (Zigler and Lessios 2003b), and Lytechinus (Zigler and Lessios 2004). Inter- Samples of P. lividus used for initial isolation of bindin estingly, these results suggest that positive selection mRNA were collected from Rosas (northwestern Mediter- operates in genera in which species are sympatric; how- ranean; Fig. 1). Gonads were removed and immediately ever, it does not operate in genera in which all (or nearly preserved in RNAlater (Ambion, Austin, TX). Total RNA all) species are allopatric. This pattern is not necessarily was extracted from testis tissue using the Totally RNA Kit related to selection to avoid hybridization in sympatric (Ambion). Bindin was isolated using a 50 and 30 RACE kit species; however, it may simply reflect the fact that species (Invitrogen, Carisbad, CA) according to the manufacturer’s with incompatible gametes can persist in sympatry (Zigler instructions (Frohman et al. 1988; Park et al. 2003). For the and Lessios 2003b; McCartney and Lessios 2004). 50 RACE, first-strand cDNA was synthesized with the High levels of polymorphism in bindin have been found primer CORE200-: 50-TCY.TCY.TCY.TCY.TGC.ATI.G in several species (Metz and Palumbi 1996; Biermann C-30 (Zigler and Lessios 2003b). Initial sequences were obtained 1998), and indications of differential fertilization efficiency by combining degenerate primers used by McCartney and within species related to bindin types have been reported Lessios (2004) and by Zigler and Lessios (2003b): MB1130? (Palumbi 1999; Levitan and Farrell 2006). In addition to (50-TGC.TSG.GTG.CSA.CSA.AGA.TTG.A-30), EL1207? reinforcement, sperm competition, interlocus sexual con- (50-AGG.CAT.CAC.TCC.AAT.CTC.CTG.GC-30), CORE flict, and sexual selection can accelerate divergence in 200- and CORE 157- (50-CIG.GRT.CIC.CHA.TRT.TIG. bindin, leading to species differentiation as a result of C-30). Specific primers for P. lividus were designed for intraspecific processes (Vacquier et al. 1997; Howard the 50 end of the molecule (see later text). For 30 RACE, 1999; McCartney and Lessios 2004; Levitan and Farrell synthesis of first-strand cDNA was conducted with primer 2006). Comparisons between patterns of bindin evolution MOBY (50-AAG.GAT.CCG.TCG.ACA.TCG.ATA.ATA.CGA. 0 of different species of sea urchins can provide information CTC.ACT.ATA.GGG.A(T)18-3 ) using nested primers out2 on the processes that have shaped them. It is thus useful to (50- GAT.CCG.TCG.A CA.TCG.ATA.ATA.CG-30)andin2 characterize this molecule in as many genera as possible. (50-CGA.TAA.TAC.GAC.TCA.CTA.TAG.G-30 (Zigler and The genus Paracentrotus is a member of the order Lessios 2003b). Specific primers for P. lividus were subsequently Echinoida, the only order in which bindin has been found designed from the 30end of the molecule. to evolve under positive selection. This genus contains only The following primers were used for amplification in two species: P. lividus (Lamarck 1816) is abundant in the Paracentrotus: PreCleF (located upstream of the preprob- Mediterranean Sea and is also found in the eastern Atlantic indin cleavage site): 50-CAG.GTG.ATA.CAG.AAA.GAA. from the British islands to South Morocco, including GCG.GT-30 and Mid-30UTR (located downstream of the Macaronesia. P. gaimardi (Blainville 1825) is distributed bindin stop codon): 50-ATG.TCG.TTG.CAA.TCA.TGA. 123 368 J Mol Evol (2009) 68:366–376 Fig. 1 Localities at which P. lividus was sampled 0 AGG-3 . These primers amplified the region coding for the Table 1 Populations of Para- Population No. of entire length of the protein from genomic DNA, including centrotus studied, number of clones clones sequenced, and number the bindin intron (see later text). The same primers were (no. of of unique haplotypes used to amplify one sample of P. gaimardi collected in haplotypes) encountereda Brazil (Baia de Sepetiba, 23°030 S, 43°450 W) and P. lividus (total) 63 (23) preserved in high-salt dimethylsulfoxide solution.
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