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The Molecular Evolution of Sperm Bindin in Six Species of Sea Urchins (Echinoida: Strongylocentrotidae)

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The Molecular Evolution of Sperm Bindin in Six Species of Sea Urchins (Echinoida: Strongylocentrotidae) The Molecular Evolution of Sperm Bindin in Six Species of Sea Urchins (Echinoida: Strongylocentrotidae) Christiane H. Biermann1 Department of Ecology and Evolution, State University of New York at Stony Brook The acrosomal protein bindin attaches sperm to eggs during sea urchin fertilization. Complementary to ongoing functional biochemical studies, I take a comparative approach to explore the molecular evolution of bindin in a group of closely related free-spawning echinoid species. Two alleles of the mature bindin gene were sequenced for each of six species in the sea urchin family Strongylocentrotidae. The nucleotide sequences diverged by at least 1% per Myr at both silent and replacement sites. Two short sections ¯anking the conserved block show an excess of nonsynonymous substitutions. Each is homologous to a region that had been identi®ed as a target of selection in other sea urchin comparisons. A large proportion of the bindin-coding sequence consists of a highly variable repeat region. Bindin sequences, even including the large intron, could not resolve the branching order among ®ve of the species. Introduction For several sympatric groups of free-spawning ma- polypeptide backbone (Foltz 1994; Stears and Lennarz rine animals, gamete recognition proteins have been 1997). Bindin, on the contrary, is 100% protein (Minor, found to be under positive selection for interspeci®c di- Gao, and Davidson 1989), and therefore potentially con- vergence (Vacquier and Lee 1993; Swanson and Vac- tains speci®city information in its primary structure. quier 1995; Metz and Palumbi 1996). The sea urchin With recombinant deletion mutants, Lopez, Miraglia, family Strongylocentrotidae contains at least nine exter- and Glabe (1993) showed that either of the two variable nally fertilizing species, all of which occur in the North domains of bindin, on either side of the conserved mid- Paci®c with partly overlapping ranges (Jensen 1974; Ba- dle region, is suf®cient to impart speci®c gamete agglu- zhin 1998). If their sperm bindin is involved in repro- tination between Strongylocentrotus franciscanus and ductive isolation, evolutionary analyses of the gene may Strongylocentrotus purpuratus. Minor, Britten, and Da- indicate natural selection or functional domains. This is vidson (1993) identi®ed a number of peptides, small particularly interesting, as the genus Strongylocentrotus bindin segments of these two congeners, that interfere has been the primary model system for biochemical with sperm±egg binding. On average, the joint effect of analyses of bindin (e.g., Glabe and Clark 1991; Minor three peptides was necessary to inhibit fertilization. One et al. 1991). 30-residue peptide, matching the S. franciscanus se- Bindin is involved in the species-speci®c recogni- quence, showed inhibitory effects signi®cantly different tion between sperm and eggs in echinoid echinoderms, between the two species. serving to bind sperm cells to the egg surface. The pro- Strongylocentrotus franciscanus and S. purpuratus tein is exocytosed from the vesicle at the tip of the have overlapping ranges and spawning seasons (Strath- sperm head when sperm undergo the acrosome reaction mann 1987). However, they are separated evolutionarily (Vacquier and Moy 1977; Gao et al. 1986). Although by at least 20 Myr (Smith 1988), during which accu- other phases during sperm±egg recognition can be spe- mulation of silent or multiple substitutions may have cies-speci®c (SeGall and Lennarz 1979; unpublished obscured molecular traces of initial divergent selection. data), the interaction of bindin with the egg surface is a It may be more informative to compare mating barriers key stage, one that has received much recent attention in more recently derived species (Palumbi 1994; Coyne (e.g., Foltz and Lennarz 1993; Hofmann and Glabe and Orr 1997). This study analyzes sperm bindin for the 1994; Vacquier, Swanson, and Hellberg 1995; Cameron species that bridge the phylogenetic gap between S. et al. 1996; Metz and Palumbi 1996). franciscanus and S. purpuratus. Two alleles of the entire Ideally, both sides of a recognition system should mature bindin were sequenced for each of six species, be examined jointly, but it is probably not a straightfor- and their molecular evolution is compared between ex- ward matter to pinpoint key recognition sites in the gene ons and introns and to a protein-coding region of mi- for the putative sperm receptor on the egg surface (Gla- tochondrial DNA. be and Vacquier 1978; Giusti, Hoang, and Foltz 1997; Mauk et al. 1997). This is because the interaction of Materials and Methods bindin with its receptor is a multistep process involving Samples and Sequencing both the receptor's carbohydrate components and the The six sea urchin species were sampled from 1 Present address and address for correspondence and reprints: Christiane H. Biermann, Department of Biological Sciences, Univer- around the Paci®c Ocean between 1994 and 1996. The sity of Hull, Hull HU6 7RX, United Kingdom. E-mail: species abbreviations are as follows: drob, Strongylo- [email protected]. centrotus droebachiensis; pall, Strongylocentrotus pal- Key words: sea urchin, Strongylocentrotus, sperm bindin, fertil- lidus; purp, S. purpuratus; poly, Strongylocentrotus po- ization, reproductive isolation, tandem repeats. lyacanthus; Allo, Allocentrotus fragilis; Hemi, Hemi- Mol. Biol. Evol. 15(12):1761±1771. 1998 centrotus pulcherrimus. PurpCA and Allo3 were from q 1998 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038 California, Allo7 was from the Eastern Bering Sea, and 1761 1762 Biermann the Hemicentrotus individual (both bindin alleles se- don usage, as well as base composition percentages of quenced) was from Japan. ``F'' stands for Friday Harbor, the nucleotide sequences, were calculated for one allele Wash.; ``K'' for Kamchatka, Siberia, and ``R'' for Res- per species in MEGA (Kumar, Tamura, and Nei 1993). olute, Northwest Territories. The species identity of each The number of nonsynonymous (amino acid re- animal was con®rmed with mitochondrial DNA. Part of placement) substitutions per nonsynonymous site and the ATPase subunit 6 gene was sequenced for those in- the number of synonymous (silent) substitutions per si- dividuals that were not included in a larger mitochon- lent site (Dn and Ds, respectively; Lee, Ota, and Vacquier drial phylogenetic study (Kessing 1991; unpublished 1995; Hughes 1997) were estimated by Nei and Gojo- data). Sequences from the mitochondrial project provid- bori's (1986) method. Dn and Ds and their standard er- ed an independent locus for all of the species in this rors were computed in MEGA (Kumar, Tamura, and Nei study, referred to as ``mtDNA'' below. The sequences 1993) for sliding windows along the sequence. Windows include two regions of mitochondrial DNA: one cover- were 30 codons in length and moved by 10 codons for ing 145 codons of the CO1 gene, corresponding to po- each step, making the plot directly comparable to ®gure sitions 6835±7270 in the complete S. purpuratus mito- 3 in Metz and Palumbi (1996). When either Dn or Ds chondrial sequence (Jacobs et al. 1988), and the other exceeded 0.4 for a particular window, the p distance stretching from the end of CO2 through ATPase 8 into (proportion of differences) was used instead of the Jukes- ATPase 6 (positions 8356±9005 in Jacobs et al. 1988), Cantor corrected distance for both Dn and Ds in that excluding the Lys-tRNA. window (Kumar, Tamura, and Nei 1993). PCR primers were designed for near the 39 end of prebindin upstream of the cleavage site between prepro- Repeat Network and mature bindin, and, after RT-PCR, for the untrans- Because orthology/paralogy relationships in the re- lated region 39 of the stop codon. Sequencing primers peat region are uncertain, the individual segments were were spaced no more than 300 bp apart on both strands. taken apart. A name (single letter) was assigned to each Primer locations and sequences are available from the of the variations of the motif to visualize the order of author. their occurrence in the alleles. There are too few infor- DNA was isolated from gonad tissue, PCR-ampli- mative sites in the 21-nt repeat to construct an overall ®ed, and initially sequenced directly (with Sequenase bifurcating tree of the 29 different motifs. Therefore, a from Amersham, following the method of Khorana, Ga- mutational network was constructed from a pairwise dis- gel, and Cote 1994). However, because of the frequency tance matrix of individual repeats (Templeton, Crandall, of heterozygous length mutations, most PCR products and Sing 1992; Crandall and Templeton 1993). This had to be cloned before sequencing (pGEM-T vector method was developed for population-level data with from Promega, transformation into XL Blue Escherichia small numbers of changes; it evaluates parsimonious coli). In spite of using DNA polymerases with proof- connections between alleles on a pairwise basis. Net- reading ability (ExTaq and LATaq from TaKaRa, Bio- works are useful for population data (including a ``pop- X-Act from BioExpress, Expand High Fidelity from ulation'' of repeats within a gene), because they include Boehringer Mannheim), a substantial number of point ancestral sequences as internal nodes and allow the de- mutations and recombinations between alleles were ev- piction of ambiguities (Crandall and Templeton 1996; ident in the cloned PCR products (e.g., Bradley and Hil- Fitch 1996). lis 1997). Hence, at least two clones were sequenced in their entirety for each allele; whenever there was a dis- Phylogenetic Sequence Analyses crepancy, an additional clone was sequenced until two Phylogenetic trees were reconstructed with the help identical sequences were obtained. Mitochondrial DNA of PAUP* (test versions 4.0.0d59±63). A minimum- was always sequenced directly. The mature bindin se- evolution (distance) tree delineates the overall relation- quences have been deposited in GenBank under acces- ships of 13 bindin sequences, excluding the repeat re- sion numbers AF077309±AF077321. gion (®g. 6). The total number of nucleotides from the (nonrepeat) coding region and the intron, aligned in- Sequence Analyses cluding the S.
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