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Evolution of the Hominoid Semenogelin Genes, the Major Proteins of Ejaculated Semen

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Abstract

The hominoid primates (apes and humans) exhibit remarkable diversity in their social and sexual behavioral systems. This is reflected in many ways in their anatomy and physiology. For example, the testes and seminal vesicles are relatively large in species with high sperm competition like the chimpanzee and small in species with low or no sperm competition like the gorilla. Additionally, the chimpanzee is the only hominoid primate known to produce a firm copulatory plug, which presumably functions in sperm competition by blocking insemination of subsequent males. Here we examine the molecular evolution of the semenogelin genes (SEMG1 and SEMG2), which code for the predominant structural proteins in human semen. High molecular weight complexes of these proteins are responsible for the viscous gelatinous consistency of human semen; their rodent homologs are responsible for the formation of a firm copulatory plug. Chimpanzees have an expanded SEMG1 gene caused by duplications of tandem repeats, each encoding 60 amino acids, resulting in a protein nearly twice as long as that of humans. In contrast, at both SEMG1 and SEMG2 we observed several gorilla haplotypes that contain at least one premature stop codon. We suggest that these structural changes in the semenogelin proteins that have arisen since the human–chimpanzee–gorilla split may be responsible for the physiological differences between these species ejaculated semen that correlate with their sociosexual behavior.

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References

  1. MJ Anderson AF Dixson (2002) ArticleTitleMotility and the midpiece in primates. Nature 416 496 Occurrence Handle10.1038/416496a Occurrence Handle11932733

    Article  PubMed  Google Scholar 

  2. SA Asdell (1964) Patterns of mammalian reproduction. Comstock Ithaca, NY

    Google Scholar 

  3. . de Lamirande K Yoshida M Yoshiike T Iwamoto C Gagnon (2001) ArticleTitleSemenogelin, the main protein of semen coagulum, inhibits sperm capacitation by interfering with the superoxide anion generated during this process. J Androl 22 672–679 Occurrence Handle11451365

    PubMed  Google Scholar 

  4. DA Dewsbury (1988) ArticleTitleA test of the role of copulatory plugs in sperm competition in deer mice (Peromyscus maniculatus). J Mammal 69 854–857

    Google Scholar 

  5. AF Dixson (1998a) Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and human beings. Oxford University Press Oxford

    Google Scholar 

  6. AF Dixson (1998b) ArticleTitleSexual selection and evolution of the seminal vesicles in primates. Folia Primatol 69 300–306

    Google Scholar 

  7. AF Dixson MJ Anderson (2002) ArticleTitleSexual selection, seminal coagulation and copulatory plug formation in primates. Folia Primatol 73 63–69 Occurrence Handle10.1159/000064784 Occurrence Handle12207054

    Article  PubMed  Google Scholar 

  8. HJ Dubbink NS Verkaik PW Faber J Trapman FH Schroder JC Romjin (1996) ArticleTitleTissue-specific and androgen-regulated expression of human prostate-specific transglutaminase. Biochem J 315 901–908 Occurrence Handle8645175

    PubMed  Google Scholar 

  9. J Felsenstein (1993) PHYLIP (phylogenetic inference package) version 3.5c. University of Washington Seattle

    Google Scholar 

  10. J Frayne L Hall (1998) ArticleTitleThe gene for the human tMDC I sperm surface protein is non-functional: Implications for its proposed role in mammalian sperm-egg recognition. Biochem J 334 171–176 Occurrence Handle9693117

    PubMed  Google Scholar 

  11. J Frayne EAC Dimsey JA Jury L Hall (1999) ArticleTitleTranscripts encoding the sperm surface protein tMDC II are non-functional in the human. Biochem J 341 771–775 Occurrence Handle10.1042/0264-6021:3410771 Occurrence Handle10417343

    Article  PubMed  Google Scholar 

  12. J Goodall (1986) The chimpanzees of Gombe: Patterns of behavior. Belknap Press Harvard, Cambridge, MA

    Google Scholar 

  13. AH Harcourt PH Harvey SG Larson RV Short (1981) ArticleTitleTestis weight, body weight and breeding system in primates. Nature 293 55–57 Occurrence Handle1:STN:280:Bi6B2s%2FnsFE%3D Occurrence Handle7266658

    CAS  PubMed  Google Scholar 

  14. PH Harvey AH Harcourt (1984) Sperm competition, testes size, and breeding systems in primates. RL Smith (Eds) Sperm competition and the evolution of animal mating systems. Academic Press Orlando, FL

    Google Scholar 

  15. R Ivell W Pusch M Balvers M Valentin N Walther G Weinbauer (2000) ArticleTitleProgressive inactivation of the haploid expressed gene for the sperm-specific endozepine-like peptide (ELP) through primate evolution. Gene 255 335–345 Occurrence Handle11024294

    PubMed  Google Scholar 

  16. JA Jury J Frayne L Hall (1997) ArticleTitleThe human fertilin α gene is non-functional: Implications for its proposed role in fertilization. Biochem J 321 577–581 Occurrence Handle9032439

    PubMed  Google Scholar 

  17. JA Jury J Frayne L Hall (1998) ArticleTitleSequence analysis of a variety of primate fertilin α genes: Evidence for non-functional genes in the gorilla and man. Mol Reprod Dev 51 92–97 Occurrence Handle10.1002/(SICI)1098-2795(199809)51:1<92::AID-MRD11>3.0.CO;2-W Occurrence Handle9712322

    Article  PubMed  Google Scholar 

  18. H Koistinen T Soini J Leinonen C Hyden-Granskog J Salo M Halttunen UH Stenman M Seppala R Koistinen (2002) ArticleTitleMonoclonal antibodies, immunofluorometric assay, and detection of human semenogelin in male reproductive tract, no association with in vitro fertilizing capacity of sperm. Biol Reprod 66 624–628

    Google Scholar 

  19. S Kumar K Tamura IB Jakobsen M Nei (2001) ArticleTitleMEGA2: Molecular Evolutionary Genetics Analysis software. Bioinformatics 17: 1244–1245 Occurrence Handle10.1093/bioinformatics/17.12.1244

    Article  Google Scholar 

  20. W-H Li (1993) ArticleTitleUnbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36 96–99 Occurrence Handle1:CAS:528:DyaK3sXnsVCmsA%3D%3D Occurrence Handle8433381

    CAS  PubMed  Google Scholar 

  21. H Lilja J Oldbring G Rannevik CB Laurell (1987) ArticleTitleSeminal vesicle-secreted proteins and their reactions during gelation and liquefaction of human semen. J Clin Invest 80 281–285 Occurrence Handle3611349

    PubMed  Google Scholar 

  22. H Lilja PA Abrahamsson A Lundwall (1989) ArticleTitleSemenogelin, the predominant protein in human semen: Primary structure and identification of closely related proteins in the male accessory sex glands and on the spermatozoa. J Biochem 264 1894–1900

    Google Scholar 

  23. H Lilja A Lundwall (1992) ArticleTitleMolecular cloning of epididymal and seminal vesicular transcripts encoding a semenogelin related protein. Proc Natl Acad Sci USA 89 4559–4563 Occurrence Handle1584792

    PubMed  Google Scholar 

  24. H-J Lin C-W Luo Y-H Chen (2002) ArticleTitleLocalization of the transglutaminase cross-linking site in SVS III, a novel glycoprotein secreted from mouse seminal vesicle. J Biol Chem 277 3632–3639 Occurrence Handle10.1074/jbc.M107578200 Occurrence Handle11723121

    Article  PubMed  Google Scholar 

  25. A Lundwall C Lazure (1995) ArticleTitleA novel gene family encoding proteins with highly differing structure because of a rapidly evolving exon. FEBS Lett 374 53–56 Occurrence Handle10.1016/0014-5793(95)01076-Q Occurrence Handle7589511

    Article  PubMed  Google Scholar 

  26. A Lundwall (1996a) ArticleTitleThe cloning of a rapidly evolving seminal-vesicle-transcribed gene encoding the major clot-forming protein of mouse semen. Eur J Biochem 235 424–430

    Google Scholar 

  27. A Lundwall (1996b) ArticleTitleThe structure of the semenogelin locus: Nucleotide sequence of the intergenic and the flanking DNA. Eur J Biochem 235 466–470

    Google Scholar 

  28. A Lundwall AYM Olsson (2001) ArticleTitleSemenogelin II gene is replaced by a truncated LINE1 repeat in the cotton-top tamarin. Biol Reprod 65 420–425 Occurrence Handle11466209

    PubMed  Google Scholar 

  29. A Lundwall A Peter J Lovgren H Lilja J Malm (1997) ArticleTitleChemical characterization of the predominant proteins secreted by mouse seminal vesicles. Eur J Biochem 249 39–44 Occurrence Handle9363751

    PubMed  Google Scholar 

  30. A Lundwall A Bjartell AY Olsson J Malm (2002) ArticleTitleSemenogelin I and II, the predominant human seminal plasma proteins, are also expressed in non-genital tissues. Mol Hum Reprod 8 805–810 Occurrence Handle10.1093/molehr/8.9.805 Occurrence Handle12200457

    Article  PubMed  Google Scholar 

  31. JR MacKinnon KS MacKinnon (1984) Territoriality, monogamy and song in gibbons and tarsiers. H Preuschoft DJ Chivers WY Brockelman N Creel (Eds) The lesser apes: Evolutionary and behavioral biology. Edinburgh University Press Edinburgh

    Google Scholar 

  32. J Malm J Hellman H Magnusson CB Laurell H Lilja (1996) ArticleTitleIsolation and characterization of the major gel proteins in human semen, semenogelin I and semenogelin II. Eur J Biochem 238 48–53 Occurrence Handle8665951

    PubMed  Google Scholar 

  33. A Mandal AK Bhattacharyya (1995) ArticleTitleSperm hyaluronidase activation by purified predominant and major basic human seminal coagulum proteins. Hum Reprod 10 1745–1750 Occurrence Handle8582973

    PubMed  Google Scholar 

  34. J Martan BA Shepard (1976) ArticleTitleThe role of copulatory plugs in reproduction in the guinea pig. J Exp Zool 196 79–83 Occurrence Handle1:STN:280:CSmB3Mnks1w%3D Occurrence Handle932657

    CAS  PubMed  Google Scholar 

  35. DE Martin KG Gould (1977) The male ape genital tract and its secretions. CE Graham (Eds) Reproductive biology of the great apes: Comparative and biomedical perspectives. Academic Press New York

    Google Scholar 

  36. D Mortimer (1993) Practical laboratory andrology. Oxford University Press New York

    Google Scholar 

  37. A Peter H Lilja A Lundwall J Malm (1998) ArticleTitleSemenogelin I and semenogelin II, the major gel-forming proteins in human semen, are substrates for transglutaminase. Eur J Biochem 252 216–221 Occurrence Handle10.1046/j.1432-1327.1998.2520216.x

    Article  Google Scholar 

  38. GA Parker (1984) Sperm competition and the evolution of animal mating strategies. RL Smith (Eds) Sperm competition and the evolution of animal mating systems. Academic Press Orlando, FL

    Google Scholar 

  39. MM Robbins (1995) ArticleTitleA demographic analysis of male life history and social structure of mountain gorillas. Behaviour 132 21–48 Occurrence Handle1:STN:280:BiuC2M3hvFA%3D Occurrence Handle6703540

    CAS  PubMed  Google Scholar 

  40. M Robert C Gagnon (1999) ArticleTitleSemenogelin I: A coagulum forming, multifunctional seminal vesicle protein. Cell Mol Life Sci 55 944–960 Occurrence Handle10.1007/s000180050346 Occurrence Handle10412373

    Article  PubMed  Google Scholar 

  41. M Robert BF Gibbs E Jacobson C Gagnon (1997) ArticleTitleCharacterization of prolate-specific antigen proteolytic activity on ils major physiological subslrale, the sperm motility inhibitor precursor/semenogelin I. Biochemistry 36 3811–3819 Occurrence Handle10.1021/bi9626158

    Article  Google Scholar 

  42. PS Rodman JC Mitani (1987) Orangutans: Sexual dimorphism in a solitary species. BB Smuts DL Cheney RM Seyfarth RW Wrangham TT Struhsaker (Eds) Primate societies. University of Chicago Press Chicago 146–154

    Google Scholar 

  43. I Sato M Yoshiike T Yamasaki K Yoshida S Takano T Mukai T Iwamoto (2001) ArticleTitleA dot-blot-immunoassay for semen identification using a polyclonal antibody against semenogelin, a powerful seminal marker. Forensic Sci Int 15 27–24 Occurrence Handle10.1016/S0379-0738(01)00435-2

    Article  Google Scholar 

  44. V Sommer U Reichard (2000) Rethinking monogamy: The gibbon case. PM Kappeler (Eds) Primate males: Causes and consequences of variation in group composition. Cambridge University Press Cambridge

    Google Scholar 

  45. WJ Swanson VD Vacquier (2002) ArticleTitleThe rapid evolution of reproductive proteins. Nat Rev Genet 3 137–144 Occurrence Handle10.1038/nrg733 Occurrence Handle1:CAS:528:DC%2BD38XhsV2ntLY%3D Occurrence Handle11836507

    Article  CAS  PubMed  Google Scholar 

  46. Y Takahata H Ihobe G Idani (1996) Comparing copulations of chimpanzees and bonobos: Do females exhibit proceptivity or receptivity?. WC McGrew LF Marchant T Nishida (Eds) Great ape societies. Cambridge University Press Cambridge 146–155

    Google Scholar 

  47. PF Tauber D Propping GFB Schumacher LJD Zaneveld (1980) ArticleTitleBiochemical aspects of the coagulation and liquefaction of human semen. J Androl 1 280–288

    Google Scholar 

  48. JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL 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 Occurrence Handle7984417

    PubMed  Google Scholar 

  49. OL Tinklepaugh (1930) ArticleTitleOccurrence of vaginal plug in a chimpanzee. Anat Rec 46 329–332

    Google Scholar 

  50. DG Torgerson RJ Kulathinal RS Singh (2002) ArticleTitleMammalian sperm proteins are rapidly evolving: Evidence of positive selection in functionally diverse genes. Mol Biol Evol 19 1973–1980 Occurrence Handle12411606

    PubMed  Google Scholar 

  51. M Ulvsback A Lundwall (1997) ArticleTitleCloning of the semenogelin II gene of the rhesus monkey: Duplications of 360 bp extend the coding region in man, rhesus monkey and baboon. Eur J Biochem 245 25–31 Occurrence Handle9128720

    PubMed  Google Scholar 

  52. CP van Schaik JARAM van Hooff (1996) Toward an understanding of the orangutan social system. WC McGrew LF Marchant T Nishida (Eds) Great ape societies. Cambridge University Press Cambridge 3–15

    Google Scholar 

  53. R Voss (1979) ArticleTitleMale accessory glands and the evolution of copulatory plugs in rodents. Occas Pap Mus Zool Univ Mich 689 1–27

    Google Scholar 

  54. DP Watts (1990) ArticleTitleEcology of gorillas and its relationship to female transfer in mountain gorillas. Int J Primatol 11 21–45

    Google Scholar 

  55. GJ Wyckoff W Wang C-I Wu (2000) ArticleTitleRapid evolution of male reproductive genes in the descent of man. Nature 403 304–309 Occurrence Handle10.1038/35002070 Occurrence Handle10659848

    Article  PubMed  Google Scholar 

  56. Z Yang (1998) ArticleTitleLikelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15 568–573 Occurrence Handle9580986

    PubMed  Google Scholar 

  57. AO Zalensky P Yau JW Breneman EM Bradbury (1993) ArticleTitleThe abundant 19-kilodalton protein associated with human sperm nuclei that is related to seminal plasma α-inhibins. Mol Reprod Dev 36 164–173 Occurrence Handle8257566

    PubMed  Google Scholar 

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Acknowledgements

We thank Drs. Amos Deinard (University of California-Davis), Kenneth Kidd (Yale University), and George Amato (Wildlife Conservation Society) for the generous donation of DNA samples and the following zoos for donating blood samples: Miami Metrozoo, San Francisco Zoo, and Kansas City Zoo. Dr. Kateryna Makova provided helpful comments on an early draft of the manuscript. This work was partly supported by NIH Grants GM55759, GM65499, and HD38287.

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Jensen-Seaman, M.I., Li, WH. Evolution of the Hominoid Semenogelin Genes, the Major Proteins of Ejaculated Semen . J Mol Evol 57, 261–270 (2003). https://doi.org/10.1007/s00239-003-2474-x

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