Reproduction and immunity-driven natural selection in the human WFDC locus

Molecular Biology and Evolution

Volumn 30, Issue 4, 2013, Pages 938-950

  Ferreira, Zélia ^a,b   Seixas, Susana ^b   Andrés, Aida M ^c   Kretzschmar, Warren W ^d   Mullikin, James C ^a   Cherukuri, Praveen F ^a   Cruz, Pedro ^a   Swanson, Willie J ^e   Clark, Andrew G ^f   Green, Eric D ^a   Hurle, Belen ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF PORTO   (Portugal)

^c MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF WASHINGTON   (United States)

^f Department of Molecular Biology and Genetics   (United States)

Author keywords

innate immunity; natural selection; reproduction; semenogelins; serine protease inhibitors; WFDC

Indexed keywords

PROTEIN; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG; WHEY ACIDIC PROTEIN FOUR DISULFIDE CORE DOMAIN;

ALLELE; AMINO ACID SUBSTITUTION; AMPLICON; ANTIMICROBIAL ACTIVITY; ARTICLE; ASIAN; BALANCING SELECTION; CAUCASIAN; CHROMOSOME 20Q; DNA FLANKING REGION; DNA SEQUENCE; FERTILITY; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC VARIABILITY; HAPLOTYPE; HOMEOSTASIS; HOMOZYGOSITY; HUMAN; HUMAN CHROMOSOME; IMMUNITY; INDEL MUTATION; INNATE IMMUNITY; MUTATION RATE; NATURAL SELECTION; NEGRO; PHYLOGENY; POPULATION DIFFERENTIATION; POPULATION STRUCTURE; PROTEIN FUNCTION; PURIFYING SELECTION; REPRODUCTION; SELECTIVE SWEEP; SINGLE NUCLEOTIDE POLYMORPHISM; SPERM; SPERMATOZOON;

ADAPTATION, BIOLOGICAL; AMINO ACID SUBSTITUTION; CHROMOSOMES, HUMAN, PAIR 20; EVOLUTION, MOLECULAR; FERTILITY; GENE FREQUENCY; HAPLOTYPES; HUMANS; IMMUNITY; LINKAGE DISEQUILIBRIUM; MODELS, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; PRINCIPAL COMPONENT ANALYSIS; PROTEINS; SELECTION, GENETIC; SEMINAL VESICLE SECRETORY PROTEINS; SEQUENCE ANALYSIS, DNA;

VERTEBRATA;

EID: 84875635332     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mss329     Document Type: Article

References (89)

1. 1000 Genomes Project Consortium. 2010. A map of human genome variation from population-scale sequencing. Nature 467: 1061-1073.
2. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. 2010. A method and server for predicting damaging missense mutations. Nat Methods. 7:248-249..
3. Agbaje IM, Rogers DA, McVicar CM, McClure N, Atkinson AB, Mallidis C, Lewis SE. 2007. Insulin dependant diabetes mellitus: implications for male reproductive function. Hum Reprod. 22:1871-1877..
4. Andrés AM, Dennis MY, Kretzschmar WW, et al. (13 co-authors). 2010. Balancing selection maintains a form of ERAP2 that undergoes nonsense-mediated decay and affects antigen presentation. PLoS Genet. 6:e1001157..
5. Bandelt HJ, Forster P, Rohl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 16:37-48..
6. Barreiro LB, Ben-Ali M, Quach H, et al. (18 co-authors). 2009. Evolutionary dynamics of human Toll-like receptors and their different contributions to host defense. PLoS Genet. 5:e1000562..
7. Barreiro LB, Laval G, Quach H, Patin E, Quintana-Murci L. 2008. Natural selection has driven population differentiation in modern humans. Nat Genet. 40:340-345..
8. Barrett JC. 2009. Haploview: visualization and analysis of SNP genotype data. Cold Spring Harb Protoc. 2009:pdb.ip71..
9. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B. 57:289-300..
10. Bingle CD, Vyakarnam A. 2008. Novel innate immune functions of the whey acidic protein family. Trends Immunol. 29:444-453..
11. Bouchard D, Morisset D, Bourbonnais Y, Tremblay GM. 2006. Proteins with whey-acidic-protein motifs and cancer. Lancet Oncol. 7: 167-174..
12. Bourgeon F, Evrard B, Brillard-Bourdet M, Colleu D, Jegou B, Pineau C. 2004. Involvement of semenogelin-derived peptides in the antibacterial activity of human seminal plasma. Biol Reprod. 70:768-774..
13. Carnahan SJ, Jensen-Seaman MI. 2008. Hominoid seminal protein evolution and ancestral mating behavior. Am J Primatol. 70:939-948..
14. Chowdhury MA, Kuivaniemi H, Romero R, Edwin S, Chaiworapongsa T, Tromp G. 2006. Identification of novel functional sequence variants in the gene for peptidase inhibitor 3. BMC Med Genet. 7:49..
15. Clauss A, Lilja H, Lundwall A. 2005. The evolution of a genetic locus encoding small serine proteinase inhibitors. Biochem Biophys Res Commun. 333:383-389..
16. Clauss A, Persson M, Lilja H, Lundwall.A°. 2011. Three genes expressing Kunitz domains in the epididymis are related to genes of WFDCtype protease inhibitors and semen coagulum proteins in spite of lacking similarity between their protein products. BMC Biochem. 12:55..
17. Chimpanzee Sequencing and Analysis Consortium C. 2005. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437:69-87..
18. Coop G, Griffiths RC. 2004. Ancestral inference on gene trees under selection. Theor Popul Biol. 66:219-232..
19. Coop G, Pickrell JK, Novembre J, Kudaravalli S, Li J, Absher D, Myers RM, Cavalli-Sforza LL, Feldman MW, Pritchard JK. 2009. The role of geography in human adaptation. PLoS Genet. 5:e1000500..
20. de Lamirande E. 2007. Semenogelin, the main protein of the human semen coagulum, regulates sperm function. Sem Thromb Hemost. 33:60-68..
21. Dorus S, Evans PD,Wyckoff GJ, Choi SS, Lahn BT. 2004. Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nat Genet. 36:1326-1329..
22. Drmanac R, Sparks AB, Callow MJ, et al. (65 co-authors). 2010. Human genome sequencing using unchained base reads on self-assembling DNA nanoarrays. Science 327:78-81..
23. Edstrom AM, Malm J, Frohm B, Martellini JA, Giwercman A, Morgelin M, Cole AM, Sorensen OE. 2008. The major bactericidal activity of human seminal plasma is zinc-dependent and derived from fragmentation of the semenogelins. J Immunol. 181: 3413-3421..
24. Excoffier L. 2002. Human demographic history: refining the recent African origin model. Curr Opin Genet Dev. 12:675-682..
25. Excoffier L, Laval G, Schneider S. 2007. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online. 1:47-50..
26. Fay JC, Wu C-I. 2000. Hitchhiking under positive Darwinian selection. Genetics 155:1405-1413..
27. Ferreira Z, Hurle B, Rocha J, Seixas S. 2011. Differing evolutionary histories of WFDC8 (short-term balancing) in Europeans and SPINT4 (incomplete selective sweep) in Africans. Mol Biol Evol. 28: 2811-2822..
28. Fornarino S, Laval G, Barreiro LB, Manry J, Vasseur E, Quintana-Murci L. 2011. Evolution of the TIR domain-containing adaptors in humans: swinging between constraint and adaptation. Mol Biol Evol. 28: 3087-3097..
29. Fu YX. 1996. New statistical tests of neutrality for DNA samples from a population. Genetics 143:557-570..
30. Fumagalli M, Cagliani R, Pozzoli U, Riva S, Comi GP, Menozzi G, Bresolin N, Sironi M. 2009. Widespread balancing selection and pathogen-driven selection at blood group antigen genes. Genome Res. 19:199-212..
31. Fumagalli M, Sironi M, Pozzoli U, Ferrer-Admetlla A, Pattini L, Nielsen R. 2011. Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet. 7:e1002355..
32. Gabriel SB, Schaffner SF, Nguyen H, et al. (18 co-authors). 2002. The structure of haplotype blocks in the human genome. Science 296: 2225-2229..
33. Gibbs RA, Rogers J, Katze MG, et al. (177 co-authors). 2007. Evolutionary and biomedical insights from the rhesus macaque genome. Science 316:222-234..
34. Griffiths RC, Tavare S. 1994. Sampling theory for neutral alleles in a varying environment. Philos Trans R Soc Lond B Biol Sci. 344: 403-410..
35. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD. 2009. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 5: e1000695..
36. Hancock AM, Clark VJ, Qian Y, Di Rienzo A. 2011. Population genetic analysis of the uncoupling proteins supports a role for UCP3 in human cold resistance. Mol Biol Evol. 28:601-614..
37. Hernandez RD, Kelley JL, Elyashiv E, Melton SC, Auton A, McVean G, Sella G, Przeworski M. 2011. Classic selective sweeps were rare in recent human evolution. Science 331:920-924..
38. Hudson RR. 2002. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18:337-338..
39. Hudson RR, Bailey K, Skarecky D, Kwiatowski J, Ayala FJ. 1994. Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics 136:1329-1340..
40. Hudson RR, Kreitman M, AguadéM. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116:153-159..
41. Hurle B, Swanson W, Program NCS, Green ED. 2007. Comparative sequence analyses reveal rapid and divergent evolutionary changes of the WFDC locus in the primate lineage. Genome Res. 17:276-286..
42. Jensen-Seaman MI, LiWH. 2003. Evolution of the hominoid semenogelin genes, the major proteins of ejaculated semen. J Mol Evol. 57: 261-270..
43. Kingan SB, Tatar M, Rand DM. 2003. Reduced polymorphism in the chimpanzee semen coagulating protein, semenogelin I. J Mol Evol. 57:159-169..
44. Kumar P, Henikoff S, Ng PC. 2009. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc. 4:1073-1082..
45. Lundwall A. 2007. A locus on chromosome 20 encompassing genes that are highly expressed in the epididymis. Asian J Androl. 9: 540-544..
46. Lundwall A, Bjartell A, Olsson AY, Malm J. 2002. Semenogelin I and II, the predominant human seminal plasma proteins, are also expressed in non-genital tissues. Mol Hum Reprod. 8:805-810..
47. Lundwall A, Clauss A. 2011. Genes encoding WFDC- and Kunitz-type protease inhibitor domains: are they related? Biochem Soc Trans. 39: 1398-1402..
48. Martellini JA, Cole AL, Venkataraman N, Quinn GA, Svoboda P, Gangrade BK, Pohl J, Sorensen OE, Cole AM. 2009. Cationic polypeptides contribute to the anti-HIV-1 activity of human seminal plasma. FASEB J. 23:3609-3618..
49. McKiernan PJ, McElvaney NG, Greene CM. 2011. SLPI and inflammatory lung disease in females. Biochem Soc Trans. 39:1421-1426..
50. McNeely TB, Shugars DC, Rosendahl M, Tucker C, Eisenberg SP, Wahl SM. 1997. Inhibition of human immunodeficiency virus type 1 infectivity by secretory leukocyte protease inhibitor occurs prior to viral reverse transcription. Blood 90:1141-1149..
51. Navarro-Casado L, Juncos-Tobarra MA, Chafer-Rudilla M, Iniguez-de Onzono L, Blazquez-Cabrera JA, Miralles-Garcia JM. 2010. Effect of experimental diabetes and STZ on male fertility capacity: study in rats. J Androl. 31:584-592..
52. Nickerson DA, Tobe VO, Taylor SL. 1997. PolyPhred: automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing. Nucleic Acids Res. 25:2745-2751..
53. Nielsen R, Hubisz MJ, Hellmann I, et al. (13 co-authors). 2009. Darwinian and demographic forces affecting human protein coding genes. Genome Res. 19:838-849..
54. Patterson N, Price AL, Reich D. 2006. Population structure and eigenanalysis. PLoS Genet. 2:e190..
55. Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D. 2006. Genetic evidence for complex speciation of humans and chimpanzees. Nature 441:1103-1108..
56. Penttinen J, Pujianto DA, Sipila P, Huhtaniemi I, Poutanen M. 2003. Discovery in silico and characterization in vitro of novel genes exclusively expressed in the mouse epididymis. Mol Endocrinol. 17: 2138-2151..
57. Peter A, Lilja H, Lundwall A, Malm J. 1998. Semenogelin I and semenogelin II, the major gel-forming proteins in human semen, are substrates for transglutaminase. Eur J Biochem. 252:216-221..
58. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D. 2006. Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet. 38:904-909..
59. Pritchard JK, Pickrell JK, Coop G. 2010. The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr Biol. 20:208-215..
60. Prugnolle F, Manica A, Charpentier M, Guegan JF, Guernier V, Balloux F. 2005. Pathogen-driven selection and worldwide HLA class I diversity. Curr Biol. 15:1022-1027..
61. Przeworski M, Coop G, Wall JD. 2005. The signature of positive selection on standing genetic variation. Evolution 59(11):2312-2323..
62. Rajesh A, Madhubabu G, Yenugu S. 2011. Identification and characterization of Wfdc gene expression in the male reproductive tract of the rat. Mol Reprod Dev. 78:633-641..
63. Ramm SA, Oliver PL, Ponting CP, Stockley P, Emes RD. 2008. Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Mol Biol Evol. 25:207-219..
64. Robert M, Gagnon C. 1999. Semenogelin I: a coagulum forming, multifunctional seminal vesicle protein. Cell Mol Life Sci. 55:944-960..
65. Robert M, Gibbs BF, Jacobson E, Gagnon C. 1997. Characterization of prostate-specific antigen proteolytic activity on its major physiological substrate, the sperm motility inhibitor precursor/semenogelin I. Biochemistry 36:3811-3819..
66. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497..
67. Sabeti PC, Reich DE, Higgins JM, et al. (17 co-authors). 2002. Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832-837..
68. Schaffner SF, Foo C, Gabriel S, Reich D, Daly MJ, Altshuler D. 2005. Calibrating a coalescent simulation of human genome sequence variation. Genome Res. 15:1576-1583..
69. Seixas S, Ivanova N, Ferreira Z, Rocha J, Victor BL. 2011. Loss and Gain of Function in SERPINB11: an example of a gene under selection on standing variation, with implications for host-pathogen interactions. PLoS One 7(2):e32518..
70. Stephens M, Donnelly P. 2003. A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet. 73:1162-1169..
71. Stephens M, Smith NJ, Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 68:978-989..
72. Storey JD. 2002. A direct approach to false discovery rates. J R Stat Soc Ser B. 64:479-498..
73. Storey JD, Taylor JE, Siegmund D. 2004. Strong control, conservative point estimation, and simultaneous conservative consistency of false discovery rates: a unified approach. J R Stat Soc Ser B. 66: 187-205..
74. Storey JD, Tibshirani R. 2003. Statistical significance for genome-wide experiments. Proc Natl Acad Sci U S A. 100:9440-9445..
75. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595..
76. Thimon V, Calvo E, Koukoui O, Legare C, Sullivan R. 2008. Effects of vasectomy on gene expression profiling along the human epididymis. Biol Reprod. 79:262-273..
77. Thornton K. 2003. Libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics 19:2325-2327..
78. Todd JA, Walker NM, Cooper JD, et al. (40 co-authors). 2007. Robust associations of four new chromosome regions from genome-wide analyses of type 1 diabetes. Nat Genet. 39:857-864..
79. Voight BF, Adams AM, Frisse LA, Qian Y, Hudson RR, Di Rienzo A. 2005. Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc Natl Acad Sci U S A. 102:18508-18513..
80. Voight BF, Kudaravalli S, Wen X, Pritchard JK. 2006. A map of recent positive selection in the human genome. PLoS Biol. 4:e72..
81. Wang Z, Widgren EE, Sivashanmugam P, O'Rand MG, Richardson RT. 2005. Association of eppin with semenogelin on human spermatozoa. Biol Reprod. 72:1064-1070..
82. Watterson GA. 1975. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 7:256-276..
83. Weldon S, McGarry N, Taggar CC, McElvaney NG. 2007. The role of secretory leucoprotease inhibitor in the resolution of inflammatory responses. Biochem Soc Trans. 35:273-276..
84. Weldon S, Taggart CC. 2007. Innate host defense functions of secretory leucoprotease inhibitor. Exp Lung Res. 33:485-491..
85. Whitlock MC. 2005. Combining probability from independent tests: the weighted Z-method is superior to Fisher's approach. J Evol Biol. 18: 1368-1373..
86. Williams SE, Brown TI, Roghanian A, Sallenave JM. 2006. SLPI and elafin: one glove, many fingers. Clin Sci. 110:21-35..
87. Yenugu S, Richardson RT, Sivashanmugam P, Wang Z, O'Rand M G, French FS, Hall SH. 2004. Antimicrobial activity of human EPPIN, an androgen-regulated, sperm-bound protein with a whey acidic protein motif. Biol Reprod. 71:1484-1490..
88. Zeng K, Fu YX, Shi S, Wu CI. 2006. Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174: 1431-1439..
89. Zhao H, Lee WH, Shen JH, Li H, Zhang Y. 2008. Identification of novel semenogelin I-derived antimicrobial peptide from liquefied human seminal plasma. Peptides 29:505-511..