Comparative proteomics uncovers the signature of natural selection acting on the ejaculate proteomes of two cricket species isolated by postmating, prezygotic phenotypes

Molecular Biology and Evolution

Volumn 28, Issue 1, 2011, Pages 423-435

  Marshall, Jeremy L ^a   Huestis, Diana L ^a,c   Garcia, Christopher ^b   Hiromasa, Yasuaki ^a   Wheeler, Shanda ^a   Noh, Suegene ^a   Tomich, John M ^a   Howard, Daniel J ^b  

^a KANSAS STATE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

2D DIGE; accessory gland; positive selection; reproductive isolation; seminal fluid; speciation gene

Indexed keywords

PROTEOME; SERINE PROTEINASE;

ANIMAL CELL; ARTICLE; CELL ISOLATION; COMPARATIVE PROTEOMICS; CRICKET; DNA POLYMORPHISM; GENE FLOW; GENETIC VARIABILITY; INSECT; MATING; NATURAL SELECTION; NONHUMAN; PHENOTYPE; PROTEOMICS; SPECIES DIFFERENTIATION; SPERM; THORAX;

ANIMALS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; FEMALE; GENETIC VARIATION; GRYLLIDAE; INSECT PROTEINS; MALE; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PHENOTYPE; PROTEOME; PROTEOMICS; REPRODUCTION; SELECTION, GENETIC; SEMEN; SPECIES SPECIFICITY;

ALLONEMOBIUS; ALLONEMOBIUS FASCIATUS; ALLONEMOBIUS SOCIUS;

EID: 78650430639     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq230     Document Type: Article

References (57)

1. Andrés JA, Maroja LS, Bogdanowicz SM, Swanson WJ, Harrison RG. 2006. Molecular evolution of seminal proteins in field crickets. Mol Biol Evol. 23:1574-1584.
2. Andrés JA, Maroja LS, Harrison RG. 2008. Searching for candidate speciation genes using a proteomic approach: seminal proteins in field crickets. Proc R Soc Lond B Biol Sci. 275:1975-1983.
3. Birge LM, Hughes AL, Marshall JL, Howard DJ. 2010. Mating behavior differences and the cost of mating in Allonemobius fasciatus and A. socius. J Insect Behav. 23:268-289.
4. Broughton RE, Harrison RG. 2003. Nuclear gene genealogies reveal historical, demographic and selective factors associated with speciation in field crickets. Genetics 163:1389-1401.
5. Civetta A, Singh RS. 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.
6. Civetta A, Singh RS. 1998. Sex-related genes, directional sexual selection, and speciation. Mol Biol Evol. 15:901-909.
7. Clark NL, Aagaard JE, Swanson WJ. 2006. Evolution of reproductive proteins from animals and plants. Reproduction 131:11-22.
8. Clement M, Posada D, Crandall K. 2000. TCS: a computer program to estimate gene genealogies. Mol Ecol. 9:1657-1660.
9. Coulthart MB, Singh RS. 1988a. Differing amounts of genetic polymorphism in testes and male accessory glands of Drosophila melanogaster and Drosophila simulans. Biochem Genet. 26: 153-164.
10. Coulthart MB, Singh RS. 1988b. High level of divergence of male-reproductive-tract proteins between Drosophila melanogaster and its sibling species, D. simulans. Mol Biol Evol. 5:182-191.
11. Coulthart MB, Singh RS. 1988c. Low genic variation in the male-reproductive-tract proteins of Drosophila melanogaster and D. simulans. Mol Biol Evol. 5:167-181.
12. Coyne JA, Orr HA. 2004. Speciation. Sunderland (MA): Sinauer Associates.
13. Dean MD, Clark NL, Findlay GD, Karn RC, Yi K, Swanson WJ, MacCoss MJ, Nachman MW. 2009. Proteomic and comparative genomic investigations reveal heterogeneity in evolutionary rate of male reproductive proteins in mice (Mus domesticus). Mol Biol Evol. 26:1733-1743.
14. Dean MD, Nachman MW. 2008. Faster fertilization rate in conspecific versus heterospecific matings in house mice. Evolution 63:20-28.
15. Doherty JA, Howard DJ. 1996. Lack of preference for conspecific calling songs in female crickets. Anim Behav. 51:981-990.
16. Findlay GD, Yi X, MacCoss MJ, Swanson WJ. 2008. Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating. PLoS Biol. 6:e178.
17. Fulton BB. 1931. A study of the genus Nemobius (Orthoptera: Gryllidae). Ann Entomol Soc Am. 24:205-237.
18. Gregory PG, Howard DJ. 1993. Laboratory hybridization studies of Allonemobius fasciatus and A. socius (Orthoptera: Gryllidae). Ann Entomol Soc Am. 86:694-701.
19. Gregory PG, Howard DJ. 1994. A post-insemination barrier to fertilization isolates two closely related ground crickets. Evolution 48:705-710.
20. Gregory PG, Howard DJ. 1998. Patterns of mating between two closely related ground crickets are not influenced by sympatry. Entomol Exp Appl. 87:263-270.
21. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 41:95-98.
22. Harrison RG. 1983. Barriers to gene exchange between closely related cricket species. I. Laboratory hybridization studies. Evolution 37:245-251.
23. Herndon LA, Wolfner MF. 1995. A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating. Proc Natl Acad Sci USA. 92:10114-10118.
24. Howard DJ. 1986. A zone of overlap and hybridization between two ground cricket species. Evolution 40:34-43.
25. Howard DJ. 1999. Conspecific sperm and pollen precedence and speciation. Ann Rev Ecol Syst. 30:109-132.
26. Howard DJ, Furth DG. 1986. Review of the Allonemobius fasciatus (Orthoptera: Gryllidae) complex with the description of two new species separated by electrophoresis, songs, and morpho-metrics. Ann Entomol Soc Am. 79:472-481.
27. Howard DJ, Gregory PG, Chu J, Cain ML. 1998. Conspecific sperm precedence is an effective barrier to hybridization between closely related species. Evolution 52:511-516.
28. Howard DJ, Palumbi SR, Birge LM, Manier MK. 2009. Sperm and speciation. In: Birkhead TR, Hosken DJ, Pitnick S, editors. Sperm biology: an evolutionary perspective. Oxford: Academic Press. p. 367-403.
29. Howard DJ, Reece M, Gregory PG, Chu J, Cain ML. 1998. The evolution of barriers to fertilization between closely related organisms. In: Howard DJ, Berlocher SH, editors. Endless forms: species and speciation. New York: Oxford University Press. p. 279-288.
30. Howard DJ, Waring GL. 1991. Topographic diversity, zone width, and the strength of reproductive isolation in a zone of overlap and hybridization. Evolution 45:1120-1135.
31. Howard DJ, Waring GL, Tibbets CA, Gregory PG. 1993. Survival of hybrids in a mosaic hybrid zone. Evolution 47:789-800.
32. Huestis DL, Marshall JL. 2006. Interaction between maternal effects and temperature affects diapause occurrence in the cricket Allonemobius socius. Oecologica 146:513-520.
33. Jha KN, Shumilin IA, Digilio LC, Chertihin O, Zheng H, Schmitz G, Visconti PE, Flickinger CJ, Minor W, Herr JC. 2008. Biochemical and structural characterization of apolipoprotein A-I binding protein, a novel phosphoprotein with a potential role in sperm capacitation. Endocrinology 149:2108-2120.
34. Marshall JL. 2004. The Allonemobius-Wolbachia host-endosymbiont system: evidence for rapid speciation and against reproductive isolation driven by cytoplasmic incompatibility. Evolution 58: 2409-2425.
35. Marshall JL. 2007. Rapid evolution of spermathecal duct length in the Allonemobius socius complex of crickets: species, population and Wolbachia effects. PLoS One. 2:e720.
36. Marshall JL, Huestis DL, Hiromasa Y, Wheeler S, Oppert C, Marshall SA, Tomich JM, Oppert B. 2009. Identification, RNAi knockdown, and functional analysis of an ejaculate protein that mediates a postmating, prezygotic phenotype in a cricket. PLoS One. 4:e7537.
37. Osanai M, Chen PS. 1993. A comparative study on the arginine degradation cascade for sperm maturation of Bombyx mori and Drosophila melanogaster. Amino Acids. 5:341-350.
38. Pond SLK, Frost SDW. 2004. A genetic algorithm approach to detecting lineage-specific variation in selection pressure. Mol Biol Evol. 22:478-485.
39. Pond SLK, Frost SDW. 2005. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531-2533.
40. 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.
41. Rand DM, Harrison RG. 1989. Ecological genetics of a mosaic hybrid zone: mitochondrial, nuclear, and reproductive differentiation of crickets by soil type. Evolution 43:432-449.
42. Ross CL, Benedix Jr. JH, Garcia C, Lambeth K, Perry R, Selwyn V, Howard DJ. 2008. Scale-independent criteria and scale-dependent agents determining the structure of a ground cricket mosaic hybrid zone (Allonemobius socius-Allonemobius fascia-tus). Biol J Linn Soc. 94:777-796.
43. Rozas JJ, Sanchez-DelBarrio C, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism análisis by the coalescent and other methods. Bioinformatics 19:2496-2497.
44. Singh RS, Coulthart MB. 1982. Genic variation in abundant soluble proteins of Drosophila melanogaster and Drosophila pseudoobscura. Genetics 102:437-453.
45. Swanson WJ, Vacquier VD. 2002a. The rapid evolution of reproductive proteins. Nat Rev Genet. 3:137-144.
46. Swanson WJ, Vacquier VD. 2002b. Reproductive protein evolution. Ann Rev Ecol Syst. 33:161-179.
47. Swanson WJ, Clark AG, Waldrip-Dali 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.
48. Swanson WJ, Wong A, Wolfner MF, Aquadro CF. 2004. Evolutionary expressed sequence tag analysis o Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics 168:1457-1465.
49. Swanson WJ, Yang Z, Wolfner MF, Aquadro CF. 2001. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc Natl Acad Sci USA. 98:2509-2514.
50. Thomas S, Singh RS. 1992. A comprehensive study of genic variation in natural populations of Drosophila melanogaster. VII. Varying rates of genic divergence as revealed by 2-dimensional electrophoresis. Mol Biol Evol. 9:507-525.
51. Traylor T, Birand AC, Marshall JL, Howard DJ. 2008. A zone of overlap and hybridization between Allonemobius socius and a new Allonemobius species. Ann Entomol Soc Am. 101: 30-39.
52. Tsaur SC, Wu CI. 1997. Positive selection and the molecular evolution of a gene of male reproduction, Acp26Aa of Drosophila. Mol Biol Evol. 14:544-549.
53. Turner LM, Hoekstra HE. 2006. Adaptive evolution of fertilization proteins within a genus: variation in ZP2 and ZP3 in deer mice (Peromyscus). Mol Biol Evol. 23:1656-1669.
54. Turner LM, Hoekstra HE. 2008. Causes and consequences of the evolution of reproductive proteins. Int J Dev Biol. 52: 769-780.
55. Turner LM, Chuong EB, Hoekstra HE. 2008. Comparative analysis of testis protein evolution in rodents. Genetics 179:2075-2089.
56. Westermeier R, Naven T, Hopker H-R. 2008. Proteomics in practice: a guide to successful experimental design, 2nd ed. Weinheim (Germany): Wiley-VCH.
57. Zeng L-W, Singh RS. 1993. A combined classical and high resolution two-dimensional electrophoresis approach to the assessment of the number of genes affecting hybrid male sterility in Drosophila simulans and Drosophila sechellia. Genetics 135:135-147.