Mating systems and protein-protein interactions determine evolutionary rates of primate sperm proteins

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1775, 2013, Pages

  Schumacher, Julia ^a   Rosenkranz, David ^a   Herlyn, Holger ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Brain proteins; Functional constraint; Mating system; Sexual selection; Sperm competition; Sperm proteins

Indexed keywords

COMPLEMENTARY DNA;

BIOCHEMICAL COMPOSITION; BRAIN; EVOLUTIONARY BIOLOGY; FUNCTIONAL ROLE; GENOME; PRIMATE; PROTEIN; REPRODUCTIVE STRATEGY; SEXUAL SELECTION; SPERM; SPERM COMPETITION;

ANIMAL; ARTICLE; BRAIN PROTEINS; CHEMISTRY; DNA SEQUENCE; FUNCTIONAL CONSTRAINT; GENETICS; HAPLORHINI; MALE; MATE CHOICE; MATING SYSTEM; METABOLISM; MOLECULAR EVOLUTION; PROTEIN DOMAIN; SEXUAL BEHAVIOR; SEXUAL SELECTION; SPERM COMPETITION; SPERM PROTEINS; SPERMATOZOON; TESTIS;

BRAIN PROTEINS; FUNCTIONAL CONSTRAINT; MATING SYSTEM; SEXUAL SELECTION; SPERM COMPETITION; SPERM PROTEINS;

ANIMALS; CHEMISTRY; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; GENETICS; HAPLORHINI; MALE; MATING PREFERENCE, ANIMAL; METABOLISM; PROTEIN INTERACTION DOMAINS AND MOTIFS; SEQUENCE ANALYSIS, DNA; SEXUAL BEHAVIOR, ANIMAL; SPERMATOZOA; TESTIS;

EID: 84902665477     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.2607     Document Type: Article

References (61)

1. Fairbairn DJ, Vermette R, Kapoor NN, Zahiri N. 2003 Functional significance of sexually selected genitalia in the water strider, Aquarius remigis. Can. J. Zool. 81, 400-413. (doi:10.1139/z03-021)
2. Maan ME, Seehausen O, Söderberg L, Johnson L, Ripmeester EA, Mrosso HD, Taylor MI, van Dooren TJ, van Alphen JJ. 2004 Intraspecific sexual selection on a speciation trait, male coloration, in the Lake Victoria cichlid Pundamilia nyererei. Proc. R. Soc. Lond. B 271, 2445-2452. (doi:10.1098/rspb.2004.2911)
3. Harcourt AH, Harvey PH, Larson SG, Short RV. 1981 Testis weight, body weight and breeding system in primates. Nature 293, 55-57. (doi:10.1038/ 293055a0)
4. Anderson MJ, Dixson AF. 2002 Sperm competition: motility and the midpiece in primates. Nature 416, 496. (doi:10.1038/416496a)
5. Carnahan SJ, Jensen-Seaman MI. 2008 Hominoid seminal protein evolution and ancestral mating behaviour. Am. J. Primatol. 70, 939-948. (doi:10. 1002/ajp.20585)
6. Ramm SA, McDonald L, Hurst JL, Beynon RJ, Stockley P. 2009 Comparative proteomics reveals evidence for evolutionary diversification of rodent seminal fluid and its functional significance in sperm competition. Mol. Biol. Evol. 26, 189-198. (doi:10.1093/molbev/msn237)
7. Torgerson DG, Kulathinal RJ, Singh RS. 2002 Mammalian sperm proteins are rapidly evolving: evidence of positive selection in functionally diverse genes. Mol. Biol. Evol. 19, 1973-1980. (doi:10. 1093/oxfordjournals.molbev.a004021)
8. Wyckoff GJ, Wang W, Wu CI. 2000 Rapid evolution of male reproductive genes in the descent of man. Nature 403, 304-309. (doi:10.1038/35002070)
9. 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. (doi:10. 1038/ng1471)
10. Herlyn H, Zischler H. 2007 Sequence evolution of the sperm ligand zonadhesin correlates negatively with body weight dimorphism in primates. Evolution 61, 289-298. (doi:10.1111/j.1558-5646.2007.00035.x)
11. 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. (doi:10.1093/molbev/ msm242)
12. Martin-Coello J, Dopazo H, Arbiza L, Ausió J, Roldan ERS, Gomendio M. 2009 Sexual selection drives weak positive selection in protamine genes and high promoter divergence, enhancing sperm competitiveness. Proc. R. Soc. B 276, 2427-2436. (doi:10.1098/rspb.2009.0257)
13. Prothmann A, Laube I, Dietz J, Roos C, Mengel K, Zischler H, Herlyn H. 2012 Sexual size dimorphism predicts rates of sequence evolution of sperm adhesion molecule 1 (SPAM1, also PH-20) in monkeys, but not in hominoids (apes including humans). Mol. Phylogenet. Evol. 63, 52-63. (doi:10.1016/j.ympev.2011.12.008)
14. Yeates SE, Einum S, Fleming IA, Megens HJ, Stet RJM, Hindar K, Holt WV, Van Look KJW, Gage MJG. 2009 Atlantic salmon eggs favour sperm in competition that have similar major histocompatibility alleles. Proc. R. Soc. B 276, 559-566. (doi:10.1098/rspb.2008.1257)
15. Gasparini C, Pilastro A. 2011 Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy. Proc. R. Soc. B 278, 2495-2501. (doi:10.1098/rspb.2010.2369)
16. Gavrilets S. 2000 Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403, 886-889. (doi:10.1038/35002564)
17. Dorus S, Busby SA, Gerike U, Shabanowitz J, Hunt DF, Karr TL. 2006 Genomic and functional evolution of the Drosophila melanogaster sperm proteome. Nat. Genet. 38, 1440-1445. (doi:10.1038/ng1915)
18. Dean MD, Clark NL, Findlay GD, Karn RC, Yi X, Swanson WJ, MacCoss MJ, Nachman MW. 2009 Proteomics and comparative genomic investigations reveal heterogeneity in evolutionary rate of male reproductive proteins in mice (Mus domesticus). Mol. Biol. Evol. 26, 1733-1743. (doi:10.1093/ molbev/msp094)
19. Haerty W et al. 2007 Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177, 1321-1335. (doi:10.1534/genetics.107.078865)
20. Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF. 2001 Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc. Natl Acad. Sci. USA 98, 7375-7379. (doi:10.1073/pnas.131568198)
21. Ficarro S et al. 2003 Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. J. Biol. Chem. 278, 11 579-11 589. (doi:10.1074/jbc.M202325200)
22. Martínez-Heredia J, Estanyol JM, Ballescà JL, Oliva R. 2006 Proteomic identification of human sperm proteins. Proteomics 6, 4356-4369. (doi:10.1002/ pmic.200600094)
23. Parte PP, Rao P, Redij S, Lobo V, D'Souza SJ, Gajbhiye R, Kulkarni V. 2012 Sperm phosphoproteome profiling by ultra performance liquid chromatography followed by data independent analysis (LC-MSE) reveals altered proteomic signatures in asthenozoospermia. J. Proteomics 75, 5861-5871. (doi:10.1016/j.jprot.2012.07.003)
24. Penn O, Privman E, Ashkenazy H, Landan G, Graur D, Pupko T. 2010 GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res. 38, W23-W28. (doi:10.1093/nar/gkq443)
25. Yang Z. 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591. (doi:10.1093/molbev/msm088)
26. Swanson WJ, Nielsen R, Yang Q. 2003 Pervasive adaptive evolution in mammalian fertilization proteins. Mol. Biol. Evol. 20, 18-20. (doi:10.1093/ oxfordjournals.molbev.a004233)
27. Lindenfors P. 2002 Sexually antagonistic selection on primate size. J. Evol. Biol. 15, 595-607. (doi:10. 1046/j.1420-9101.2002.00422.x)
28. Dooley H, Judge D. 2007 Vocal responses of captive gibbon groups to a mate change in a pair of whitecheeked gibbons (Nomascus leucogenys). Folia Primatol. 78, 228-239. (doi:10.1159/000102318)
29. Digby LJ, Ferrari SF. 1994 Multiple breeding females in free-ranging groups of Callithrix jacchus. Int. J. Primatol. 15, 389-397. (doi:10.1007/ BF02696100)
30. Digby LJ. 1999 Sexual behavior and extragroup copulations in a wild population of common marmosets (Callithrix jacchus). Folia Primatol. 70, 136-145. (doi:10.1159/000021686)
31. Utami SS, Goossens B, Bruford MW, de Ruiter JR, van Hooff JARAM. 2002 Male bimaturism and reproductive success in Sumatran orang-utans. Behav. Ecol. 13, 643-652. (doi:10.1093/beheco/13.5.643)
32. Knott CD, Thompson EM, Stumpf RM, McIntyre MH. 2010 Female reproductive strategies in orangutans, evidence for female choice and counterstrategies to infanticide in a species with frequent sexual coercion. Proc. R. Soc. B 277, 105-113. (doi:10. 1098/rspb.2009.1552)
33. Hapke A, Zinner D, Zischler H. 2001 Mitochondrial DNA variation in Eritrean hamadryas baboons (Papio hamadryas hamadryas): life history influences population genetic structure. Behav. Ecol. Sociobiol. 50, 483-492. (doi:10.1007/s002650100393)
34. Zinner D, Groeneveld LF, Keller C, Roos C. 2009 Mitochondrial phylogeography of baboons (Papio spp.): indication for introgressive hybridization? BMC Evol. Biol. 9, 83. (doi:10.1186/1471-2148-9-83)
35. Walters JR, Harrison RG. 2010 Combined EST and proteomic analysis identifies rapidly evolving seminal fluid proteins in Heliconius butterflies. Mol. Biol. Evol. 27, 2000-2013. (doi:10.1093/ molbev/msq092)
36. Dumont D, Noben JP, Verhaert P, Stinissen P, Robben J. 2006 Gel-free analysis of the human brain proteome: application of liquid chromatography and mass spectrometry on biopsy and autopsy samples. Proteomics 6, 4967-4977. (doi:10.1002/pmic.200600080)
37. Bayés A, van de Lagemaat LN, Collins MO, Croning MD, Whittle IR, Choudhary JS, Grant SG. 2011 Characterization of the proteome, diseases and evolution of the human postsynaptic density. Nat. Neurosci. 14, 19-21. (doi:10.1038/nn.2719)
38. Metz EC, Palumbi SR. 1996 Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol. Biol. Evol. 13, 397-406. (doi:10.1093/ oxfordjournals.molbev.a025598)
39. Hellberg ME, Vacquier VD. 1999 Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Mol. Biol. Evol. 16, 839-848. (doi:10.1093/oxfordjournals.molbev.a026168)
40. Gatesy J, Swanson WJ. 2007 Adaptive evolution and phylogenetic utility of ACR (acrosin), a rapidly evolving mammalian fertilization gene. J. Mammal. 88, 32-42. (doi:10.1644/05-MAMM-S-345R1.1)
41. Good JM, Nachman MW. 2005 Rates of evolution are positively correlated with developmental timing of expression during mouse spermatogenesis. Mol. Biol. Evol. 22, 1044-1052. (doi:10.1093/molbev/ msi087)
42. Dorus S, Wasbrough ER, Busby J, Wilkin EC, Karr TL. 2010 Sperm proteomics reveals intensified selection on mouse sperm membrane and acrosome genes. Mol. Biol. Evol. 27, 1235-1246. (doi:10.1093/ molbev/msq007)
43. Jeong H, Mason SP, Barabási AL, Oltvai ZN. 2001 Lethality and centrality in protein networks. Nature 411, 41-42. (doi:10.1038/35075138)
44. Lee WP, Jeng BC, Pai TW, Tsai CP, Yu CY, Tzou WS. 2006 Differential evolutionary conservation of motif modes in the yeast protein interaction network. BMC Genomics 7, 89. (doi:10.1186/1471-2164-7-89)
45. Wolf YI, Carmel L, Koonin EV. 2006 Unifying measures of gene function and evolution. Proc. R. Soc. B 273, 1507-1515. (doi:10.1098/rspb.2006.3472)
46. Lovell SC, Robertson DL. 2010 An integrated view of molecular coevolution in protein-protein interactions. Mol. Biol. Evol. 27, 2567-2575. (doi:10.1093/molbev/msq144)
47. Mintseris J, Weng Z. 2005 Structure, function, and evolution of transient and obligate protein-protein interactions. Proc. Natl Acad. Sci. USA 102, 10 930-10 935. (doi:10.1073/pnas.0502667102)
48. Fraser HB, Hirsh AE, Steinmetz LM, Scharfe C, Feldman MW. 2002 Evolutionary rate in the protein interaction network. Science 296, 750-752. (doi:10. 1126/science.1068696)
49. Hahn MW, Kern AD. 2005 Comparative genomics of centrality and essentiality in three eukaryotic protein-interaction networks. Mol. Biol. Evol. 22, 803-806. (doi:10.1093/molbev/msi072)
50. Alvarez-Ponce D, Fares MA. 2012 Evolutionary rate and duplicability in the Arabidopsis thaliana protein-protein interaction network. Genome Biol. Evol. 4, 1263-1274. (doi:10.1093/ gbe/evs101)
51. Albert R, Barabási AL. 2002 Statistical mechanics of complex networks. Rev. Mod. Phys. 74, 47. (doi:10. 1103/RevModPhys.74.47)
52. Kim PM, Korbel JO, Gerstein MB. 2007 Positive selection at the protein network periphery: evaluation in terms of structural constraints and cellular context. Proc. Natl Acad. Sci. USA 104, 20 274-20 279. (doi:10.1073/pnas. 0710183104)
53. Birkhead TR, Pizzari T. 2002 Postcopulatory sexual selection. Nat. Rev. Genet. 3, 262-273. (doi:10.1038/ nrg774)
54. Walters JR, Harrison RG. 2011 Decoupling of rapid and adaptive evolution among seminal fluid proteins in Heliconius butterflies with divergent mating systems. Evolution 65, 2855-2871. (doi:10. 1111/j.1558-5646.2011.01351.x)
55. Jansen S, Ekhlasi-Hundrieser M, Töpfer-Petersen E. 2001 Sperm adhesion molecules: structure and function. Cells Tissues Organs 168, 82-92. (doi:10. 1159/000016809)
56. Thomson T, Lin H. 2009 The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu. Rev. Cell Dev. Biol. 25, 355-367. (doi:10.1146/annurev. cellbio.24.110707.175327)
57. Good JM et al. 2013 Comparative population genomics of the ejaculate in humans and the great apes. Mol. Evol. Biol. 30, 964-976. (doi:10.1093/ molbev/mst005)
58. Malik HS, Bayes JJ. 2006 Genetic conflicts during meiosis and the evolutionary origins of centromere complexity. Biochem. Soc. Trans. 34, 569-573. (doi:10.1042/BST0340569)
59. Albert R, Jeong H, Barabási AL. 2000 Error and attack tolerance of complex networks. Nature 406, 278-282. (doi:10.1038/35019019)
60. Khan SA, Jadhav SV, Suryawanshi AR, Bhonde GS, Gajbhiye RK, Khole VV. 2011 Evaluation of contraceptive potential of a novel epididymal sperm protein SFP2 in a mouse model. Am. J. Reprod. Immunol. 66, 185-198. (doi:10.1111/j.1600-0897.2011.01030.x)
61. Primakoff P, Lathrop W, Woolman L, Cowan A, Myles D. 1988 Fully effective contraception in male and female guinea pigs immunized with the sperm protein PH-20. Nature 335, 543-546. (doi:10.1038/ 335543a0)