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a Department of Laboratory Medicine, Lund University, University Hospital, Malmö, S-205 02 Malmö, Sweden
ABSTRACT
The human seminal vesicles secrete two proteins, semenogelin I and semenogelin II, at very high concentrations. It has previously been shown that the cotton-top tamarin (Sanguinus oedipus), a New World monkey, is lacking the semenogelin II gene. We have now determined the nucleotide sequence of DNA located 5–13 kilobases (kb) downstream of the tamarin semenogelin I gene—a region that in man is occupied by the semenogelin II gene. Two regions with homology to the human semenogelin II gene were identified in the tamarin DNA. The first region, of 3.5 kb, is homologous to DNA upstream of the human gene, and the second region, of 0.6 kb, is mainly derived from the second intron. Between these regions, equivalent to 594 base pairs (bp) upstream of the transcription initiation site to 12 bp downstream of the stop codon in the human semenogelin II gene, the cotton-top tamarin DNA carries a truncated LINE1 repeat. In another set of experiments, the tamarin DNA hybridizing to the mouse semenoclotin gene was investigated. It was concluded that hybridization is with the second intron of the semenoclotin gene, but very likely, the material does not represent a cotton-top tamarin semenoclotin gene. Thus, a mammalian ancestor probably carried a single gene that in the rodent lineage developed into the semenoclotin gene and in the primate lineage into a progenitor of the semenogelin genes.
gene regulation, male reproductive tract, seminal vesicles, sperm motility and transport
INTRODUCTION
Mammalian semen consists of spermatozoa and seminal plasma provided by the accessory sex glands—predominantly the prostate and the seminal vesicles. In man the prostate contributes around one third of the semen volume and the seminal vesicles around two thirds. Some mammalian species, e.g., carnivores like cats and dogs, do not have seminal vesicles and hence their seminal plasma is mainly derived from fluid secreted by the prostate [1].
The seminal vesicles of most mammals secrete a limited number of proteins at very high concentrations. Generally these proteins are involved in semen coagulation. In man, they are semenogelin I (SgI) and semenogelin II (SgII), two homologous proteins that to a large extent consist of structural elements repeated in tandem [2, 3]. Most conspicuous are repeats of 60 amino acid residues, of which SgI carry two and SgII four, leading to a mass difference of 13 kDa between the molecules [3]. The molecular mass of SgI is 50 kDa and of SgII 63 kDa, but because of partial glycosylation, the latter is present in two molecular forms with molecular masses estimated by SDS-PAGE to 71 kDa for the nonglycosylated form and 76 kDa for the glycosylated form [4]. Shortly after ejaculation, the semenogelins are proteolytically degraded by prostate-specific antigen, leading to dissolution of the seminal coagulum in a process known as semen liquefaction [5]. The physiological significance of the coagulation and liquefaction processes is not known, but the end result is that the spermatozoa become highly motile and display propulsive mobility.
The two genes encoding human SgI and SgII are located 11.6 kb apart on chromosome 20q12–13.1 [6]. Both consist of three exons of which the first codes for the signal peptide and the three amino-terminal residues of the mature polypeptide [7]. The relatively large second exon codes for the rest of the protein and carries the stop codon and a few 3' nontranslated nucleotides, while the third exon encompasses 3' nontranslated nucleotides only and carries the polyadenylation signal. Results of DNA hybridization indicate that probably all higher primates carry semenogelin genes, but because of an unusual evolution leading to an internal expansion of the second exon, the structures of the secreted semenogelin molecules differ significantly between species [7]. For instance, the rhesus monkey SgII is 22% larger than the human protein, and SgI from the cotton-top tamarin is 32% larger than the human orthologue [8, 9].
The predominant proteins secreted by the rodent seminal vesicles are homologous to the semenogelins as revealed by structural conservation of their genes [10]. However, because the structure of the second exon that encodes all but the three amino terminal residues of the secreted protein has gone through a very dramatic evolution, the genes are not recognized by DNA hybridization using semenogelin cDNA probes. Two mechanisms have been described as being responsible for the varying structure of the second exon [10]. In the case of rat seminal vesicle secreted protein II (SVS II) and mouse semenoclotin genes, the difference to the semenogelin genes is caused by an internal expansion of the exon in a way similar to what caused the interspecies variation of semenogelins among primates. However, because of the longer evolutionary distance, there are only some 80 nucleotides in the 5' end and around 30 nucleotides in the 3' end of the exon, with a total size around 1.5 kilobases (kb), that are conserved. The second mechanism leading to structural variation involves novel selection of splice sites. By this mechanism, the second exon was created in the rat SVS IV and SVS V genes and in the gene encoding the polyprotein from which three of the four proteins secreted by the guinea pig seminal vesicles are derived [10, 11].
Because of the structural similarity and the common evolutionary pattern, the major seminal vesicle-transcribed genes constitute a separate gene family. It was named the rapidly evolving substrates of transglutaminase (REST) gene family because of the rapid evolution and because all members thus far seem to encode proteins that are good substrates for various transglutaminases. Later it was shown that the gene for the protease inhibitor elafin and perhaps also the gene for the secretory leukocyte-protease inhibitor belong to the REST gene family [12]. In man the two semenogelin genes and the two protease inhibitor genes are at the same locus on chromosome 20.
In previous studies we have shown that the cotton-top tamarin (Sanguinus oedipus) carries an SgI gene but no SgII gene [9]. The simultaneous demonstration of mouse semenoclotin gene hybridization to tamarin DNA suggested that the SgII gene might have been replaced by a semenoclotin gene in the cotton-top tamarin. In other primates there is no indication of a semenoclotin gene, and no semenogelin gene has ever been observed in rodents. With respect to the principle of genetic parsimony, this is an unusual situation, as it requires that the semenoclotin gene was deleted from the genome of most primates and that the semenogelin genes were deleted from the rodent genome. To investigate this further, we have now determined the nucleotide sequence downstream of the tamarin SgI where other primates carry an SgII gene. We have also reanalyzed the mouse semenoclotin gene hybridization to cotton-top tamarin DNA.
MATERIALS AND METHODS
Molecular Cloning
The construction of a genomic library containing cotton-top tamarin DNA in 
EMBL3 and the conditions for screening of the library have been described earlier [9]. The probe was the 3-kb insert of subclone pMuSX3-1, containing the mouse semenoclotin gene [13]. It was radiolabeled to a specific activity exceeding 1 x 109 dpm/µg using 32P-
-dCTP and the Megaprime labeling kit (Amersham Pharmacia, Uppsala, Sweden). Hybridizing clones were purified and DNA was isolated from phage preparations using standard techniques [14]. Subclones were generated in the plasmid vectors pUC18 and pGEM3Z.
Southern Blot
DNA was isolated from the liver of a cotton-top tamarin as described elsewhere [9]. Portions of 15 µg were digested by restriction enzymes as recommended by the supplier of the enzymes (Amersham Pharmacia). The material was separated by electrophoresis in 0.7% agarose gel using 10 mM Tris-borate-buffer pH, 7.8, containing 1 mM EDTA and then transferred by vacuum-blotting to a Hybond N+ membrane (Amersham Pharmacia). The membrane filter was prehybridized at 55°C for 2 h in 5x NaCl/Pi/EDTA (1x NaCl/Pi/EDTA: 0.15 M NaCl, 1 mM EDTA, 10 mM sodium phosphate, pH 6.8), 10x Denhardt solution, 0.5 % SDS, 200 µg/ml denatured fish DNA, and then hybridized for 16 h at the same temperature and in the same solution after addition of 2 x 106 dpm/ml radioactively labeled probe. The probe was either the 3-kb insert of subclone pMuSX3-1 or a 974-base pair (bp) fragment, SE974, extending from a SnaBI site located 34 bp upstream of exon 2 to an EcoRV site 155 bp upstream of intron 2. The subfragments XB1.3 and BX1.6 were generated from the 5', respectively, and the 3' end of pMuSX3-1 by cleavage of the insert with the restriction enzyme BstXI. The probes were labeled as described above. Following hybridization the membranes were washed in 2x NaCl/Pi/EDTA, 0.1% SDS first at ambient temperature and then at 55°C for 15 min. Autoradiograms were generated by a phosphoimager (Molecular Dynamics Phosphoimager SI).
DNA Sequencing
Sequencing reactions were done using the Big Dye terminator cycle sequencing kit and then analyzed on an Applied Biosystems 373 DNA sequencer upgraded to Big Dye chemistry (Applied Biosystems, Foster City, CA). Sequences were generated from subclone ends using the 17-mer universal forward- and reverse-sequencing primers. Sequences were gradually extended by reactions primed by 20-mer oligonucleotides that were designed from sequences generated in the previous step. The DNA sequences were aligned and analyzed using the GCG computer program package (Genetics Computer Group, Madison, WI) [15]. The sequences were scanned for DNA repeats using the program RepeatMask available through the BCM Search Launcher at Baylor Collage of Medicine (http://www.hgsc.bcm.tmc.edu).
Calculation of Substitutions
Substitutions at the SgI locus were identified as sites with nucleotide differences between the human and the tamarin gene sequences. Insertions and deletions were calculated as one event regardless of the number of nucleotides involved. The mutation was assigned to the gene that also differed from the SgII genes at this site. In cases where the mutation could not be assigned to any of the genes (10.6% of the cases), substitutions were assigned to the genes in proportion to the ratio of unambiguous mutations. The number of back mutations was considered to be proportional to the number of observed mutations, and the total number of substitutions/site (ST) was calculated by the equation ST = So + ST x So (or ST = So/1 - So), where So is the number of observed substitutions/site. Substitutions at the SgII locus were calculated in the same way. In this case, the fraction of ambiguous substitutions was 11.7%.
Substitutions occurring prior to the separation of New and Old World monkeys were identified as differences between the SgI gene and the SgII gene at locations where the orthologous genes are conserved. In some instances, either the SgI or the SgII gene was conserved but the other gene pair differed so as to suggest that an early transversal substitution had been followed by a transitional substitution after the separation of New and Old World monkeys. If this number is multiplied by the ratio of transversions to transitions in the genes after the separation of New and Old World monkeys, we obtain the number of transversal substitutions that were followed by transversal substitutions, and hence the total number of early transversions that were followed by a second mutation can be calculated. The ratio of transitions to transversions prior to the separation of New and Old World monkeys is calculated from the uncorrected data, and if this ratio is multiplied by the total number of early transversions that were followed by a second mutation, we will obtain the total number of early transitions that were followed by a second mutation. By adding the calculated number of early mutations that were followed by a second mutation and the observed number of substitutions, we get a measure of the total number of mutations. This can be corrected for back mutations by the equation above to yield the total number of substitutions prior to the separation of New and Old World monkeys.
RESULTS
The human SgII gene is located 11.6 kb downstream of the SgI gene. In a previous work, a clone, TSgA1, was described that has its 5' end located immediately upstream of the cotton-top tamarin's SgI gene and that extends 16 kb in the 3' direction [8]. Thus, it could potentially contain DNA homologous to the human SgII gene. To identify such homologous regions, the nucleotide sequence of clone TSgA1 was determined from the EcoRI site located 4.8 kb downstream of the SgI gene to the Sau3AI site at the clone's 3' end. The novel sequence is 7960 bp, and the 5' EcoRI site overlaps the 3' EcoRI site in the previously reported sequence of the cotton-top tamarin SgI gene [9], giving rise to a contiguous sequence of 19 292 bp (available at EMBL sequence data bank under accession no. AJ002153).
The extended sequence of the tamarin semenogelin gene locus was compared to that of the human semenogelin gene locus [6]. The result was displayed in a dotplot (Fig. 1). As can be seen, the tamarin sequence between 1.2 kb and 10.1 kb, encompassing the SgI gene, is similar to the region between 5.3 and 13.8 kb containing the human SgI gene, as has previously been reported [9]. Thereafter follows a stretch of 3.4 kb where there is no similarity between the tamarin and the human sequences. The region is of similar size in man and tamarin and contains several truncated LINE1 repeats interspersed with Alu repeats. In the tamarin this is part of a larger region with LINE1 repeats extending from 9.1 to 14.9 kb. About 1 kb at each end of this repeat region is conserved at the human semenogelin locus, but in the central part, human DNA carries two truncated LINE1 repeats in the opposite orientation. The similarity to the human semenogelin gene locus resumes around 13.5 kb and continues almost to the end of the clone, the exception being the region between 17.1 and 18.4 kb, which in human DNA is occupied by the SgII gene.
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The novel tamarin sequence was compared in more detail to the human SgII gene and its flanking DNA as illustrated in Figure 2. There is one sequence of 3492 bp that is homologous to a region 595–4177 bp upstream to the human SgII gene. The homologous region contains one Alu repeat both in the human and the tamarin DNA but at different locations, suggesting that both were inserted after the separation of New and Old World primates. A second homologous region of 553 bp extends from 12 bp downstream of the stop codon to 530 bp into the second intron of the human SgII gene. In man, the sequence between the two homology regions encompasses the upstream promoter, the first exon, the first intron, and most of the second exon of the SgII gene, including all of the coding nucleotides. In the tamarin, the corresponding region is homologous to members of the LINE1 family of long interspersed repeats. Thus, it appears like the SgII gene in the cotton-top tamarin has been replaced by a LINE1 repeat. In the middle of the LINE1 repeat, there has also been insertion of an Alu repeat. Downstream of the second homology region in the tamarin there is a stretch of 45 bp LINE1 repeat followed by an Alu repeat that extends to the end of the clone. When searching the EMBL nucleotide sequence database with the 45-bp LINE1 sequence, the top-scoring match was a sequence located 3.5 kb downstream of the human SgII gene. It has 41 out of 45 nucleotides identically placed, giving a sequence similarity around 91%, or of the same magnitude as between the human and the tamarin sequence in the homology regions described above. Other top-scoring sequences at best only had 34 out of 45 identically placed nucleotides (76%), and therefore the 45-bp LINE1 sequence is probably orthologous to the sequence located 3.5 kb downstream of the human SgII gene. Thus, also a region of 4 kb, encompassing the 3' end of the second intron, the third exon and nucleotides flanking the 3' end of the human SgII gene, has been deleted from the tamarin genome.
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To confirm that the new sequence is orthologous to DNA flanking the human SgII gene and not the result of an SgI gene duplication occurring after the separation of Old and New World monkeys, the nucleotide sequence was aligned with available sequences flanking semenogelin genes. The comparison shows that 3.7 kb surrounding the human SgII gene is 90% conserved in the new sequence. The figure for the human SgI gene is 82% in 1.8 kb flanking DNA and for the tamarin SgI gene it is 80% in 1.7 kb flanking DNA. The results clearly demonstrate that the new sequence is derived from DNA that has been flanking an SgII gene. The new tamarin sequence was also compared to that of the mouse semenoclotin gene [13]. The comparison shows that one part of the sequence is 61% similar to DNA located 886–1587 nucleotides upstream of the semenoclotin gene, and another part is 64% similar to 535 bp starting five nucleotides downstream of the stop codon.
In order to calculate the number of base substitutions, conserved nucleotide sequences of the two human and the two tamarin semenogelin genes were aligned (Fig. 3). The number of substitutions occurring in the semenogelin flanking regions since the separation of New World monkeys from Old World monkeys and apes was calculated to 4.3 and 4.4 per 100 nucleotides for the human SgI and SgII genes, respectively. The rate of base substitutions in the cotton-top tamarin appears to be 1.56 times faster, as in this species there are 6.7 substitutions per 100 nucleotides in SgI gene and 6.9 in the remnants of the SgII gene. The ratio of transitional to transversional mutations was 2.34. An attempt was also made to calculate the number of substitutions occurring after the duplication that yielded the two semenogelin genes but prior to the separation of Old and New World monkeys. This calculation yielded 11.4 substitutions/100 bp. Based on these figures, the divergence between the human SgI and SgII genes in the regions compared is 20.1%. The observed sequence difference is 16.0%, but calculations by various methods in the GCG program package yielded divergences varying from 18.6% to 21.8%. A similar calculation for the semenogelin genes of the tamarin yielded a divergence of 25.0%, compared with the observed sequence difference of 20.0%.
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Previous results indicated that the SgII gene might have been replaced by a semenoclotin gene in the cotton-top tamarin [9]. In order to address this, approximately 7 x 105 clones of a cotton-top tamarin library were screened at low stringency using a DNA fragment encompassing the mouse semenoclotin gene. Four clones were isolated that hybridized relatively weakly, but stably, to the probe. Restriction mapping and DNA sequencing showed that three of the clones were overlapping and probably hybridized to the first intron of the semenoclotin gene. The fourth clone was unique and probably hybridized to the upstream promoter region of the semenoclotin gene. The library screening, even if done at low stringency, was presumably relatively specific as three out of the four isolated clones carried overlapping DNA. Thus, the genomic fragments carried by these clones probably represent the best hybridizing DNA in the library.
Southern blots with genomic DNA from the tamarin yielded a 19-kb BamHI fragment, a 4.8-kb EcoRI fragment, and an 8.5-kb XbaI fragment that hybridized to a full-length semenoclotin gene probe (Fig. 4). The fragment sizes are not compatible with the restriction maps of the cloned material, which therefore could not be responsible for the hybridization with genomic DNA. In order to localize the hybridizing nucleotides, the Southern blot was reprobed using subfragments of the semenoclotin gene. These were an XbaI to BstXI fragment, XB1.3, extending from the XbaI site located 0.8 kb upstream of the semenoclotin gene to the BstXI site located 0.15 kb into exon 2; a 974-bp SnaBI to EcoRV fragment, encompassing most of the coding nucleotides; and finally a 3' fragment BB1.6, extending from the BstXI site in exon 2 to another BstXI site located 66 nucleotides into exon 3. Of these only the BB1.6 fragment hybridized, suggesting that the nucleotides hybridizing to tamarin DNA most probably reside in the second intron. Characteristically, members of the REST gene family, of which the semenoclotin gene is one, are most conserved in the first and the third exon. Because of this, it is not very likely that the signal generated by mouse semenoclotin gene probes in the Southern blots represents hybridization to a tamarin REST gene, and thus, the cotton-top tamarin probably does not carry a semenoclotin gene.
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DISCUSSION
In previous investigations on the semenogelin genes in primates, we have concluded that Old World monkeys carry both an SgI gene and an SgII gene [8]. In New World monkeys, the situation is more uncertain because of a difference in hybridization pattern between the closely related callitrichinaean species—common marmoset and cotton-top tamarin. The former species yielded two hybridizing bands in Southern blots that were indicative of two semenogelin genes, while the latter species only displayed one hybridizing band, suggesting a single semenogelin gene [8]. Later the SgI gene of the tamarin was cloned and sequenced and it was also confirmed by hybridization that genomic DNA from cotton-top tamarin does not contain an SgII gene [9]. However, the higher sequence similarity of the tamarin SgI gene to the human SgI gene than to the human or the rhesus monkey SgII gene suggested that the duplication yielding two semenogelin genes occurred prior to the separation of Old and New World monkeys. Thus, an ancestor of the tamarins must have had two semenogelin genes, of which one, the SgII gene, was lost during the evolution that yielded the cotton-top tamarin. By sequencing DNA downstream of the tamarin SgI gene, we are now able to identify nucleotide sequences with homology to the human SgII gene. However, all translated nucleotides as well as the upstream promoter region are absent, thereby explaining the lack of hybridization in previous experiments using probes derived from coding nucleotides [9].
It is not obvious by which mechanism the SgII gene was replaced by a LINE1 repeat in the tamarin. Generally, LINE1 repeats are spread in the genome via an intermediate RNA copy by retroposition, but such a mechanism cannot explain how the tamarin SgII gene disappeared. Another possibility is that the gene was removed by homologous recombination between LINE repeats. This scenario requires that the tamarin SgII gene was surrounded by LINES. However, there are no LINE sequences in the human SgII gene at positions orthologous to the site of integration. Therefore, it is not likely that a tamarin ancestor carried LINE sequences at these positions either, and hence the replacement of the tamarin SgII gene by a LINE1 repeat is probably not the result of homologous recombination only. We must therefore assume that the rearrangement at the tamarin SgII gene locus is the reflection of two events—insertion of the LINE1 element by retroposition and elimination of the SgII gene by recombination. An attractive hypothesis would be that the insertion of a LINE1 repeat rendered the gene nonfunctional and therefore it was subsequently deleted from the genome together with part of the LINE1 repeat. The hypothesis might be tested by analysis of the SgII gene in a closely related callitrichinaean species like the common marmoset. It is not unlikely that the insertion of a LINE1 repeat occurred in an ancestor of both tamarins and marmosets. In the latter species the SgII gene may not have been removed as in the cotton-top tamarin but instead remained as a pseudogene—thereby explaining the result of Southern blots indicating two semenogelin genes in the marmoset.
Elucidating the evolution of the SgII gene in New World monkeys may also have an impact on our understanding of the role of semenogelins in human reproduction. In man, the production of semenogelins is very high in the seminal vesicles and it might be speculated that the function of the proteins, in some way, is related to sperm transport in the reproductive tract. In such a system, it is easy to envision that a rapid adaptation to the loss of one semenogelin gene may not have a profound effect on male reproductive function. However, it has also been reported that small amounts of SgII, but not SgI, are produced in the caudal part of the human epididymis [3, 16]. This site of synthesis suggests that SgII in man might have a more subtle function in regard to the maturation or storage of spermatozoa. Perhaps comparative studies on epididymal function in man and tamarins can reveal some interesting differences that in turn might be related to the presence or absence of SgII.
Despite the dramatic events leading to a very rapid evolution of the second exon in REST genes, the relative rate of evolution at the semenogelin locus as calculated in this work is not very different from what is seen at, for instance, the ß-globin locus [17]. The sequence divergence of the human 
-globin gene from that of the same gene in New World monkeys like spider monkey and owl monkey is 11.0% and 12.4%, compared with the divergence of 11.0–11.3% seen between man and cotton-top tamarin at the semenogelin locus.
The size of the human genome is 3 x 109 bp, and presumably, the cotton-top tamarin genome is of approximately the same size. The screening of 7 x 105 recombinants of a tamarin library, carrying an average 15–20 kb of genomic DNA/clone, is equivalent to approximately four times the genome size. The same filters used here for the screening of a semenoclotin homologue in the cotton-top tamarin were also screened for SgI and ß-microseminoprotein (MSP) genes [9, 18]. In these screenings, 4 SgI and 11 MSP clones were isolated, but then there are at least 3 MSP genes in the tamarin. These figures agree well with what is to be expected if the library contains a random selection of clones. The isolation of three overlapping clones by the semenoclotin gene in this paper—although not representing the material hybridizing in Southern blots—is also an indication that there is a relatively random distribution of DNA fragments in the library. The failure to isolate any clone related to the material hybridizing to the semenoclotin gene in Southern blots suggests that it is located on a piece of DNA that is difficult to clone or that the signal is generated by hybridization to repetitive DNA. In the latter case, each individual copy presumably yields a very weak signal that during library screening is hard to distinguish from the background, but combined they could give rise to the strong signal seen in the Southern blots. However, it appears no longer important to clone the cotton-top tamarin DNA hybridizing to the mouse semenogelin probe in order to solve the phylogenetic relationship between the semenogelin genes and the semenoclotin gene. If the cotton-top tamarin carried both a semenogelin gene and a semenoclotin gene, then a progenitor of primates and rodents also must have had both. The semenogelin gene must then have been deleted from the rodent genome, and likewise the semenoclotin must have been deleted from the genome of most primates. With respect to genetic parsimony this is a very unusual scenario and in fact it is very likely wrong, as in this paper we have shown that the tamarin DNA hybridizing with the semenoclotin gene most probably is not a REST gene. Thus, an ancestor of primates and rodents probably carried a single gene that in the rodent lineage developed into the semenoclotin gene and in the primate lineage into the progenitor of the semenogelin genes that subsequently duplicated to yield the SgI gene and the SgII gene.
ACKNOWLEDGMENTS
The assistance of I. Dahlquist and S. Strömberg in running the automated DNA sequencer is acknowledged.
FOOTNOTES
First decision: 16 February 2001.
1 This work was supported by a grant from the Swedish Medical Research Council (project 8660). 
2 Correspondence: Åke Lundwall, Department of Laboratory Medicine, Division
of Clinical Chemistry, University Hospital, Malmö, S-205 02 Malmö,
Sweden. FAX: 46 40 33 70 43; ake.lundwall{at}klkemi.mas.lu.se
Accepted: March 16, 2001.
Received: January 19, 2001.
REFERENCES
-globin gene and surrounding sequences: Recent and ancient insertion of LINEs and SINEs?. Genomics 1988; 3:237-255[CrossRef][Medline]This article has been cited by other articles:
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  R. C. Karn, N. L. Clark, E. D. Nguyen, and W. J. Swanson Adaptive Evolution in Rodent Seminal Vesicle Secretion Proteins Mol. Biol. Evol., November 1, 2008; 25(11): 2301 - 2310. [Abstract] [Full Text] [PDF]
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 C. Valtonen-Andre, A. Y. Olsson, M. Kullberg, P. L. Nayudu, and A. Lundwall The Common Marmoset (Callithrix jacchus) Has Two Very Similar Semenogelin Genes as the Result of Gene Conversion Biol Reprod, April 1, 2007; 76(4): 604 - 610. [Abstract] [Full Text] [PDF]
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 B. Hurle, W. Swanson, NISC Comparative Sequencing Program, and E. D. Green Comparative sequence analyses reveal rapid and divergent evolutionary changes of the WFDC locus in the primate lineage Genome Res., March 1, 2007; 17(3): 276 - 286. [Abstract] [Full Text] [PDF]
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