Mammalian sperm proteins are rapidly evolving: Evidence of positive selection in functionally diverse genes

Molecular Biology and Evolution

Volumn 19, Issue 11, 2002, Pages 1973-1980

  Torgerson, Dara G ^a   Kulathinal, Rob J ^a,b   Singh, Rama S ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Positive Darwinian selection; Rapid evolution; Sperm; Tissue specific genes

Indexed keywords

ADAM 2 PRECURSOR PROTEIN; CELL ADHESION MOLECULE; CELL PROTEIN; EGG BINDING PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PROTAMINE; PROTAMINE P1; SPERM ADHESION MOLECULE 1; SPERM PROTEIN; UNCLASSIFIED DRUG; PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING SITE; CELL SPECIFICITY; GENE EXPRESSION REGULATION; GENETIC SELECTION; GENETIC VARIABILITY; GLYCOLYSIS; HUMAN; INTRASPECIFIC VARIATION; MALE; MOLECULAR EVOLUTION; MUTATION RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN BINDING; REPRODUCTION; SEXUAL BEHAVIOR; SEXUAL SELECTION; SPERM; SPERMATOZOON; STRUCTURE ACTIVITY RELATION; TISSUE SPECIFICITY; UNINDEXED SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; FEMALE; GENETICS; METABOLISM; MOUSE; MUTAGENESIS; STATISTICAL MODEL;

ANIMALIA; DARWINIA; MAMMALIA;

AMINO ACID SUBSTITUTION; ANIMALS; EVOLUTION, MOLECULAR; FEMALE; HUMANS; LIKELIHOOD FUNCTIONS; MALE; MICE; MUTAGENESIS; ORGAN SPECIFICITY; PROTEINS; REPRODUCTION; SELECTION (GENETICS); SPERMATOZOA;

EID: 0036856302     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.molbev.a004021     Document Type: Article

References (48)

1. Aguadé, M., N. Miyashita, and C. H. Langley. 1992. Polymorphism and divergence in the Mst26A male accessory gland gene region in Drosophila. Genetics 130:755-770.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Carson, H. L. 1997. Sexual selection: A driver of genetic change in Hawaiian Drosophila. J. Hered. 88:343-352.
4. Casane, D., S. Boissinot, B. H. J. Chang, L. C. Shimmin, and W.-H. Li. 1997. Mutation pattern variation among regions of the primate genome. J. Mol. Evol. 45:216-226.
5. Cirera, S., and M. Aguadé. 1997. Evolutionary history of the sex-peptide (Acp70A) gene region in Drosophila melanogaster. Genetics 147:189-197.
6. Civetta, A., and R. S. Singh. 1995. High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species. J. Mol. Evol. 41:1085-1095.
7. Clark, A. G., M. Aguade, T. Prout, L. G. Harshman, and C. H. Langley. 1995. Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics 139:189-201.
8. Coulthart, M. B., and R. S. Singh. 1988. Differing amounts of genetic polymorphism in testes and male accessory glands of Drosophila melanogaster and Drosophila simulans. Mol. Biol. Evol. 5:182-191.
9. Curry, M. R., and P. F. Watson. 1995. Sperm structure and function. Pp. 45-69 in J. G. Grudzinskas and J. L. Vovich, eds. Gametes - The Spermatozoon. Cambridge University Press, Cambridge.
10. Darwin, C. 1871. The Descent of Man, and Selection in Relation to Sex. John Murray, London.
11. Duret, L., and D. Mouchiroud. 2000. Determinants of substitution rates in mammalian genes: Expression pattern affects selection intensity but not mutation rate. Mol. Biol. Evol. 17:68-74.
12. Eberhard, W. G. 1985. Sexual Selection and Animal Genitalia. Harvard University Press, Cambridge.
13. Hirsh, A. E., and H. B. Fraser. 2001. Protein dispensability and rate of evolution. Nature 411:1046-1049.
14. Hughes, A. L. 1997. Rapid evolution of immunoglobulin superfamily C2 domains expressed in immune system cells. Mol. Biol. Evol. 14:1-5.
15. Hughes, A. L., and M. Nei. 1988. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167-170.
16. Hughes, A. L., T. Ota, and M. Nei. 1990. Evolutionary relationships of class II major-histocompatibility-complex genes in mammals. Mol. Biol. Evol. 7:491-514.
17. Karr, T. L., and S. Pitnick. 1999. Sperm competition: Defining the rules of engagement. Curr. Biol. 9:R787-R790.
18. Kuma, K., N. Iwabe, and T. Miyata. 1995. Functional constraints against variations on molecules from the tissue level: slowly evolving brain-specific genes demonstrated by protein kinase and immunoglobulin supergene families. Mol. Biol. Evol. 12:123-130.
19. Lande, R. 1981. Models of speciation by sexual selection on polygenic traits. Proc. Natl. Acad. Sci. USA 78:3721-3725.
20. Li, W. 1993. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol. Evol. 26:96-99.
21. Makalowski, W., and M. S. Boguski. 1998. Evolutionary parameters of the transcribed mammalian genome: An analysis of 2,820 orthologous rodent and human sequences. Proc. Natl. Acad. Sci. USA 95:9407-9412.
22. Matassi, G., P. M. Sharp, and C. Gautier. 1999. Chromosomal location effects on gene sequence evolution in mammals. Curr. Biol. 9:786-791.
23. Metz, E. C., and S. R. Palumbi. 1996. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein binding. Mol. Biol. Evol. 13:397-406.
24. Mouchiroud, D., C. Gautier, and G. Bernardi. 1995. Frequencies of synonymous substitutions in mammals are gene-specific and correlated with frequencies of nonsynonymous substitutions. J. Mol. Evol. 40:107-113.
25. Nurminsky, D. I., M. V. Nurminskaya, D. De Aguiar, and D. L. Hartl. 1998. Selective sweep of a newly evolved sperm-specific gene in Drosophila. Nature 396:572-575.
26. Ohtsuki, K., Y. Nishikawa, H. Saito, H. Munakata, and T. Kato. 1996. DNA-binding sperm proteins with oligo-arginine clusters function as potent activators for egg CK-II. FEBS Lett. 378:115-120.
27. Pitnick, S. 1996. Investment in testes and the cost of making long sperm in Drosophila. Am. Nat. 148:57-80.
28. Rice, W. R. 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232-234.
29. Rooney, A. P., and J. Zhang. 1999. Rapid evolution of a primate sperm protein: Relaxation of functional constraint or positive Darwinian selection? Mol. Biol. Evol. 16:706-710.
30. Saitou, N., and M. Nei. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
31. SINGH, R. S., and R. J. Kulathinal. 2000. Sex gene pool evolution and speciation: A new paradigm. Genes Genet. Syst. 75:119-130.
32. Swanson, W. J., C. F. Aquadro, and V. D. Vacquier. 2001. Polymorphism in abalone fertilization proteins is consistent with the neutral evolution of the egg's receptor for lysin (VERL) and positive Darwinian selection of sperm lysin. Mol. Biol. Evol. 18:376-383.
33. Swanson, W. J., A. G. Clark, H. M. Waldrip-dail, M. F. Wolfner, and C. F. Aquadro. 2001a. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc. Natl. Acad. Sci. USA 98:7375-7379.
34. Swanson, W. J., and V. D. Vacquier. 1995. Extraordinary divergence and positive Darwinian selection in a fusagenic protein coating the acrosomal process of abalone spermatozoa. Proc. Natl. Acad. Sci. USA 92:4957-4961.
35. -. 1998. Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein. Science 281:710-712.
36. -. 2002. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3:137-144.
37. Swanson, W. J., Z. Yang, M. F. Wolfner, and C. F. Aquadro. 2001b. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc. Natl. Acad. Sci. USA 98:2509-2514.
38. Tanaka, T., and M. Nei. 1989. Positive Darwinian selection observed at the variable-region genes of immunoglobulins. Mol. Biol. Evol. 6:447-459.
39. Thompson, J. D., W. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876-4883.
40. Tsaur, S., C. Ting, and C. Wu. 1998. Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism. Mol. Biol. Evol. 15:1040-1046.
41. Welch, J. E., P. L. Brown, D. A. O'Brien, P. L. Magyar, D. O. Bunch, C. Mori, and E. M. Eddy. 2000. Human glyceraldehyde 3-phosphate dehydrogenase-2 gene is expressed specifically in spermatogenic cells. J. Androl. 21:328-338.
42. Williams, E. J. B., and L. D. Hurst. 2000. The proteins of linked genes evolve at similar rates. Nature 407:900-903.
43. Williamson, M. P. 1994. The structure and function of proline-rich regions in proteins. Biochem. J. 297:249-260.
44. Wolfe, K. H., and P. M. Sharp. 1993. Mammalian gene evolution; nucleotide sequence divergence between mouse and rat. J. Mol. Evol. 37:441-456.
45. Wolfe, K. H., P. M. Sharp, and W.-H. Li. 1989. Mutation rates differ among regions of the mammalian genome. Nature 337:283-285.
46. Wyckoff, G. J., W. Wang, and C. Wu. 2000. Rapid evolution of male reproductive genes in the descent of man. Nature 503:304-309.
47. Yang, Z. 1994. Estimating the pattern of nucleotide substitution. J. Mol. Evol. 39:105-111.
48. -. 1997. PAML: A program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13: 555-556.