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Reduced Polymorphism in the Chimpanzee Semen Coagulating Protein, Semenogelin I

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Abstract

The semen of many primate species coagulates into a mating plug believed to prevent the sperm of subsequent mating events from accessing the ova. The texture of the coagulum varies among species: from a semisoft mass in humans to a firm plug in chimpanzees. In humans, a component of the coagulum, semenogelin I, also inhibits sperm motility. We tested the hypothesis that polymorphism and divergence at semenogelin I differ among hominoid species with different mating systems. Sequence data for the semenogelin I locus were obtained from 12 humans, 10 chimpanzees, 7 gorillas, and 1 bonobo. Mitochondrial D-loop data were collected from a subset of individuals to assess levels of variation at an unlinked locus. HKA tests using D-loop sequence data revealed a significant reduction of polymorphism at semenogelin I in chimpanzees, consistent with predictions of a selective sweep at this locus. This result was supported by independent HKA tests using polymorphism data from a putatively neutral locus from the literature. Humans show a similar trend toward reduced polymorphism, although HKA tests were only marginally significant. Gorilla sequence data show evidence of functional loss at the semenogelin I locus, indicated by stop codons within the putative open reading frame as well as high levels of polymorphism. Elevated K a/K s ratios within the Pan–Homo clade suggest a history of positive selection at semenogelin I. Our results suggest that there is a positive relationship between the intensity of sperm competition in a species and the strength of positive Darwinian selection on the seminal protein semenogelin I.

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References

  1. M Aguadé (1999) ArticleTitlePositive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila. Genetics 152 543–551 Occurrence Handle10353898

    PubMed  Google Scholar 

  2. MJ Anderson AF Dixson (2002) ArticleTitleSperm competition: Motility and the midpiece in primates. Nature 416 496 Occurrence Handle10.1038/416496a Occurrence Handle11932733

    Article  PubMed  Google Scholar 

  3. DJ Begun P Whitley BL Todd HM Waldrip-Dail AG Clark (2000) ArticleTitleMolecular population genetics of male accessory gland proteins in Drosophila. Genetics 156 1879–1888 Occurrence Handle11102381

    PubMed  Google Scholar 

  4. CH Biermann (1998) ArticleTitleThe molecular evolution of sperm bindin in six species of sea urchins (Echinoida: Strongylocentrotidae). Mol Biol Evol 15 1761–1771 Occurrence Handle1:CAS:528:DyaK1MXjtVyk Occurrence Handle9866210

    CAS  PubMed  Google Scholar 

  5. TR Birkhead AP Moller (Eds) (1998) Sperm competition and sexual selection. Academic Press San Diego

    Google Scholar 

  6. T Chapman (2001) ArticleTitleSeminal fluid-mediated fitness traits in Drosophila. Heredity 87 511–521 Occurrence Handle10.1046/j.1365-2540.2001.00961.x Occurrence Handle11869341

    Article  PubMed  Google Scholar 

  7. F-C Chen W-H Li (2001) ArticleTitleGenomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet 68 444–456

    Google Scholar 

  8. FC Chen EJ Vallender H Wang CS Tzeng WH Li (2001) ArticleTitleGenomic divergence between human and chimpanzee estimated from large-scale alignments of genomic sequences. J Hered 92 481–489 Occurrence Handle10.1093/jhered/92.6.481 Occurrence Handle11948215

    Article  PubMed  Google Scholar 

  9. A Deinard K Kidd (1999) ArticleTitleEvolution of a HOXB6 intergenic region within the great apes and humans. J Hum Evol 36 687–703 Occurrence Handle1:STN:280:DyaK1M3msVChtQ%3D%3D Occurrence Handle10330333

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  11. A Di Rienzo AC Wilson (1991) ArticleTitleBranching pattern in the evolutionary tree for human mitochondrial DNA. Proc Natl Acad Sci USA 88 1597–1601 Occurrence Handle2000368

    PubMed  Google Scholar 

  12. AF Dixson (1998) Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and human beings. Oxford University Press Oxford 22–50

    Google Scholar 

  13. AF Dixson NI Mundy (1994) ArticleTitleSexual behavior, sexual swelling, and penile evolution in chimpanzees (Pan troglodytes). Arch Sex Behav 23 267–280 Occurrence Handle1:STN:280:ByuB1MnisFM%3D Occurrence Handle8024440

    CAS  PubMed  Google Scholar 

  14. WG Eberhard (1985) Sexual selection and animal genitalia. Harvard University Press Cambridge, MA 2–3

    Google Scholar 

  15. R Grantham (1974) ArticleTitleAmino acid difference formula to help explain protein evolution. Science 185 862–864 Occurrence Handle1:CAS:528:DyaE2cXlsVOiuro%3D Occurrence Handle4843792

    CAS  PubMed  Google Scholar 

  16. TA Hall (1999) ArticleTitleBioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41 95–98 Occurrence Handle1:CAS:528:DC%2BD3cXhtVyjs7Y%3D

    CAS  Google Scholar 

  17. 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 

  18. ME Hellberg VD Vacquier (1999) ArticleTitleRapid evolution of fertilization selectivity and lysine cDNA sequences in teguline gastropods. Mol Biol Evol 16 839–848 Occurrence Handle1:CAS:528:DyaK1MXjslGitbc%3D Occurrence Handle10368961

    CAS  PubMed  Google Scholar 

  19. J Hey (1997) ArticleTitleMitochondrial and nuclear genes present conflicting portraits of human origins. Mol Biol Evol 14 166–172 Occurrence Handle1:CAS:528:DyaK2sXhtVKit7o%3D Occurrence Handle9029794

    CAS  PubMed  Google Scholar 

  20. Hey J (2001) HKA: A computer program for tests of natural selection (http://lifesci.rutgers.edu/~heylab/ ).

  21. RR Hudson M Kreitman M Aguade (1987) ArticleTitleA test of neutral molecular evolution based on nucleotide data. Genetics 116 153–159 Occurrence Handle1:CAS:528:DyaL2sXktlCgsLk%3D Occurrence Handle3110004

    CAS  PubMed  Google Scholar 

  22. MI Jensen-Seaman AS Deinard KK Kidd (2001) ArticleTitleModern African ape populations as genetic and demographic models of the last common ancestors of humans, chimpanzees, and gorillas. J Hered 92 475–480 Occurrence Handle10.1093/jhered/92.6.475 Occurrence Handle11948214

    Article  PubMed  Google Scholar 

  23. H Kaessmann V Wiebe S Paabo (1999) ArticleTitleExtensive nuclear DNA sequence diversity among chimpanzees. Science 286 1159–1162 Occurrence Handle1:CAS:528:DyaK1MXnt1KrsrY%3D Occurrence Handle10550054

    CAS  PubMed  Google Scholar 

  24. S Kumar K Tamura M Nei (1993) MEGA: Molecular evolutionary genetic analysis, version 1.01. The Pennsylvania State University University Park 24–26

    Google Scholar 

  25. D Levinson M Ember (Eds) (1996) Encyclopedia of cultural anthropology. Henry Holt and Company New York

    Google Scholar 

  26. WH Li CI Wu CC Luo (1984) ArticleTitleNonrandomness of point mutation as reflected in nucleotide substitutions in pseudogenes and its evolutionary implications. J Mol Evol 21 58–71 Occurrence Handle1:CAS:528:DyaL2MXntlGhuw%3D%3D Occurrence Handle6442359

    CAS  PubMed  Google Scholar 

  27. H Lilja (1985) ArticleTitleA kallikrein-like serine protease in prostatic fluid cleaves the predominant seminal vesicle protein. J Clin Invest 76 1899–1903

    Google Scholar 

  28. H Lilja P-A Abrahamsson A Lundwall (1989) ArticleTitleSemenogelin, the predominant protein in human semen. J Biol Chem 264 1894–1900 Occurrence Handle2912989

    PubMed  Google Scholar 

  29. 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 

  30. J Marson D Gervais S Meuris RW Cooper P Jouannet (1989) ArticleTitleInfluence of ejaculation frequency on semen characteristics in chimpanzees (Pan troglodytes). J Reprod Fertil 85 43–50

    Google Scholar 

  31. JH McDonald M Kreitman (1991) ArticleTitleAdaptive protein evolution at the Adh locus in Drosophila. Nature 351 652–654 Occurrence Handle1:CAS:528:DyaK3MXks1yrtLs%3D Occurrence Handle1904993

    CAS  PubMed  Google Scholar 

  32. EC Metz SR Palumbi (1996) ArticleTitlePositive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol Biol Evol 13 397–406 Occurrence Handle1:CAS:528:DyaK28Xnt12hsA%3D%3D Occurrence Handle8587504

    CAS  PubMed  Google Scholar 

  33. PA Morin JJ Moore R Chakraborty L Jin J Goodall DS Woodruff (1994) ArticleTitleKin selection, social structure, gene flow, and the evolution of chimpanzees. Science 265 1193–1201 Occurrence Handle1:CAS:528:DyaK2cXmsFahtr0%3D Occurrence Handle7915048

    CAS  PubMed  Google Scholar 

  34. MW Nachman (2001) ArticleTitleSingle nucleotide polymorphism and recombination rate in humans. Trends Genet 17 481–485 Occurrence Handle10.1016/S0168-9525(01)02409-X Occurrence Handle11525814

    Article  PubMed  Google Scholar 

  35. MW Nachman WM Brown M Stoneking CF Aquadro (1996) ArticleTitleNonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics 142 953–963

    Google Scholar 

  36. M Nei (1987) Molecular evolutionary genetics. Columbia University Press New York

    Google Scholar 

  37. R Noda CG Kim O Takenaka RE Ferrell T Tanoue I Hayasaka S Ueda T Ishida N Saitou (2001) ArticleTitleMitochondrial 16S rRNA sequence diversity of hominoids. J Hered 92 490–496 Occurrence Handle10.1093/jhered/92.6.490 Occurrence Handle11948216

    Article  PubMed  Google Scholar 

  38. T Ohta (1995) ArticleTitleSynonymous and nonsynonymous substitutions in mammalian genes and the nearly neutral theory. J Mol Evol 40 56–63

    Google Scholar 

  39. GA Parker (1970) ArticleTitleSperm competition and its evolutionary consequences in the insects. Biol Rev 45 525–567

    Google Scholar 

  40. 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 

  41. 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 

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

    Article  Google Scholar 

  43. JD Roussel CR Austin (1967) ArticleTitleEnzymatic liquefaction of primate semen. Int J Fertil 12 288–290

    Google Scholar 

  44. J Rozas R Rozas (1999) ArticleTitleDnaSP version 3: An integrated program for molecular populations genetics and molecular evolution analysis. Bioinformatics 15 174–175 Occurrence Handle10.1093/bioinformatics/15.2.174 Occurrence Handle1:CAS:528:DyaK1MXisVOksrY%3D Occurrence Handle10089204

    Article  CAS  PubMed  Google Scholar 

  45. RL Smith (Eds) (1984) Sperm competition and the evolution of animal mating systems. Academic Press London

    Google Scholar 

  46. RL Smith (1998) Foreword. TR Birkhead AP Moller (Eds) Sperm competition and sexual selection. Academic Press San Diego

    Google Scholar 

  47. 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 

  48. WJ Swanson AG Clark HM Waldrip-Dail MF Wolfner CF Aquadro (2001a) ArticleTitleEvolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci USA 98 7375–7379

    Google Scholar 

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

    Google Scholar 

  50. PF Tauber LJ Zaneveld D Propping GF Schumacher (1975) ArticleTitleComponents of human split ejaculates. I. J Reprod Fertil 43 249–267

    Google Scholar 

  51. 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

    Google Scholar 

  52. S-C Tsaur C-I Wu (1997) ArticleTitlePositive selection and the molecular evolution of a gene of male reproduction, Acp26Aa of Drosophila. Mol Biol Evol 14 544–549

    Google Scholar 

  53. S-C Tsaur C-T Ting C-I Wu (1998) ArticleTitlePositive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism. Mol Biol Evol 15 1040–1046

    Google Scholar 

  54. S-C Tsaur C-T Ting C-I Wu (2001) ArticleTitleSex in Drosophila mauritiana: A very high level of amino acid polymorphism in a male reproductive protein gene, Acp26Aa. Mol Biol Evol 18 22–26 Occurrence Handle11141189

    PubMed  Google Scholar 

  55. LF van Pelt PE Keyser (1970) ArticleTitleObservations on semen collection and quality in macaques. Lab Anim Care 20 726–733 Occurrence Handle4247969

    PubMed  Google Scholar 

  56. 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 

  57. Z Yang (1997) ArticleTitlePAML: A program package for phylogenetic analysis by maximum Likelihood. CABIOS 13 555–556 Occurrence Handle1:CAS:528:DyaK2sXntlGnu7s%3D Occurrence Handle9367129

    CAS  PubMed  Google Scholar 

  58. Z Yang WJ Swanson VD Vacquier (2000) ArticleTitleMaximum-likelihood analysis of molecular adaptation in abalone sperm lysis reveals variable selective pressures among lineages and sites. Mol Biol Evol 17 1446–1455 Occurrence Handle1:CAS:528:DC%2BD3cXnt1Cnsb4%3D Occurrence Handle11018152

    CAS  PubMed  Google Scholar 

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Acknowledgements

S.B.K. would like to thank Oliver Ryder and Leona Chemnick at the Center for Reproduction of Endangered Species/Zoological Society of San Diego as well as Karen Rice and Mary Sparks at the Southwest National Primate Research Center for providing valuable DNA samples. Michael Palmer, Lea Sheldahl, Faye Lemieux, and Raymond Qwan provided support in conducting this research. Michael Hammer, Michael Nachman, Tasha Altheide, Jason Wilder, and two anonymous reviewers provided helpful comments on the manuscript. This research was funded by the Royce Fellowship for Undergraduate Research at Brown University. Additional support was provided by a grant to M.T. from the NIH (AG16632) and grants to D.M.R. from the NSF (DEB9981497 and DEB0108500).

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  1. Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912, USA

    Sarah B. Kingan, Marc Tatar & David M. Rand

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  1. Sarah B. Kingan
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Correspondence to Sarah B. Kingan.

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Kingan, S.B., Tatar, M. & Rand, D.M. Reduced Polymorphism in the Chimpanzee Semen Coagulating Protein, Semenogelin I . J Mol Evol 57, 159–169 (2003). https://doi.org/10.1007/s00239-002-2463-0

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