Rapid evolution of outer egg membrane proteins in the Drosophila melanogaster subgroup: A case of ecologically driven evolution of female reproductive traits

Molecular Biology and Evolution

Volumn 24, Issue 4, 2007, Pages 929-938

  Jagadeeshan, Santosh ^a   Singh, Rama S ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Chorion proteins; Ecological diversification; Gametic surface proteins; Positive selection; Sex and reproduction related genes; Speciation; Vitelline proteins

Indexed keywords

OUTER MEMBRANE PROTEIN;

ARTICLE; CHORION; COMPARATIVE STUDY; CONTROLLED STUDY; DROSOPHILA; DROSOPHILA ERECTA; DROSOPHILA MELANOGASTER; DROSOPHILA SECHELLIA; ECOLOGICAL GENETICS; EGG SHELL; EVOLUTIONARY ADAPTATION; FEMALE; FEMALE GENITAL SYSTEM; GAMETE; GENETIC POLYMORPHISM; GENETIC TRAIT; GENETIC VARIABILITY; MOLECULAR EVOLUTION; MORPHOLOGY; NONHUMAN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SEXUAL SELECTION; SPERMATOZOON; VITELLINE MEMBRANE;

AMINO ACID SEQUENCE; ANIMALS; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EGG PROTEINS; EVOLUTION, MOLECULAR; FEMALE; LIKELIHOOD FUNCTIONS; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; OVUM; POLYMORPHISM, GENETIC; REPRODUCTION; SELECTION (GENETICS); SEQUENCE HOMOLOGY, AMINO ACID;

DROSOPHILA ERECTA; DROSOPHILA MELANOGASTER; DROSOPHILA SECHELLIA; HEXAPODA; MELANOGASTER SUBGROUP; SUBGROUP A;

EID: 34047222491     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msm009     Document Type: Article

References (64)

1. Andrenacci D, Cernilogar FM, Taddei C, Rotoli D, Cavaliere V, Graziani F, Gavrilets S. 2001. Specific domains drive Vm32E protein distribution and integration in Drosophila eggshell layers. J Cell Sci. 114:2819-2829.
2. Cariou ML, Silvain JF, Daubin V, Da Lage JL, Lachaise D. 2001. Divergence between Drosophila santomea and allopatric or sympatric populations of D. yakuba using paralogous amylase genes and migration scenarios along the Cameroon volcanic line. Mol Ecol. 10:649-660.
3. Carson HL, Templeton AR. 1984. Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annu Rev Ecol Syst. 15:97-131.
4. Chakir M, Chafik A, Moreteau B, Gibert P, David JR. 2002. Male sterility thermal thresholds in Drosophila: D. simulans appears more cold-adapted than its sibling D. melanogaster. Genetica. 114:195-205.
5. Chakir M, David JR, Pla E, Capy P. 1995. Genetic basis of some morphological differences between temperate and equatorial populations of Drosophila melanogaster. Experientia. 51:744-748.
6. 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.
7. Clark NL, Aagaard JE, Swanson WJ. 2006. Evolution of reproductive proteinsfromanimalsandplants. Reproduction. 131:11-22.
8. Coulthart MB, Singh RS. 1988. High level of divergence of male-reproductive-tract proteins, between Drosophila melanogaster and its sibling species, D. simulans. Mol Biol Evol. 5:182-191.
9. David JR, Allemand R, Capy P, Chakir M, Gibert P, Petavy G, Moreteau B. 2004. Comparative life histories and ecophysiology of Drosophila melanogaster and D. simulans. Genetica. 120:151-163.
10. Fay JC, Wu C-I. 2000. Hitchiking under positive Darwinian selection. Genetics. 155:1405-1413.
11. Fay JC, Wykoff GJ, Wu C-I. 2001. Positive and negative selection on the human genome. Genetics. 158:1227-1234.
12. Fenerjian MG, Martinez-Cruzado JC, Swimmer C, King D, Kafatos FC. 1989. Evolution of the autosomal chorion cluster in Drosophila. II. Chorion gene expression and sequence comparisons of the s16 and s19 genes in evolutionarily distant species. J Mol Evol. 29:108-125.
13. Fu YX, Li WH. 1993. Statistical tests of neutrality of mutations. Genetics. 133:693-709.
14. Gibert P, Capy P, Imasheva A, Moreteau B, Morin JP, Petavy G, David JR. 2004. Comparative analysis of morphological traits among Drosophila melanogaster and D. simulans: genetic variability, clines and phenotypic plasticity. Genetica. 120:165-179.
15. Griffin-Shea R, Thireos G, Kafatos FC. 1982. Organization of a cluster of four chorion genes in Drosophila and its relationship to developmental expression and amplification. Dev Biol. 91:325-336.
16. Hatzopoulos AK, Regier JC. 1987. Evolutionary changes in the developmental expression of silkmoth chorion genes and their morphological consequences. Proc Natl Acad Sci USA. 84:479-483.
17. Hinton HE. 1981. Biology of insect eggs. Oxford: Pergamon Press.
18. Jagadeeshan S, Singh RS. 2005. Rapidly evolving genes of Drosophila: differing levels of selective pressure in testis, ovary and head tissues between sibling species. Mol Biol Evol. 22:1793-1801.
19. Jones CD. 2005. The genetics of adaptation in Drosophila sechellia. Genetica. 123:137-145.
20. Kambysellis MP. 1975. Ultrastructure of the chorion proteins in very closely related Drosophila species endemic to Hawaii. Syst Zool. 23:507-512.
21. Kambysellis MP. 1993. Ultrastructural diversity in the egg chorion of Hawaiian Drosophila and Scaptomyza: ecological and phylogenetic considerations. Int J Insect Morphol Embryol. 22:417-446.
22. Kambysellis MP, Ho KF, Craddock EM, Piano F, Parisi M, Cohen J. 1995. Pattern of ecological shifts in the diversification of Hawaiian Drosophila inferred from a molecular phylogeny. Curr Biol. 5:1129-1139.
23. Lachaise D, Tsacas L. 1983. Breeding-sites in tropical African drosophilids. London: Academic Press. p. 221-332.
24. Lachaise D, Cariou M-L, David JR, Lemeunier F, Tscacas L, Ashburner M. 1988. Historical biogeography of the Drosophila melanogaster species subgroup. Evol Biol. 22:159-224.
25. Lachaise D, Silvain JF. 2004. How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica. 120:17-39.
26. Lachaise D, Tsacas L, Couturier G. 1982. The Drosophilidae associated with tropical African figs. Evolution. 36:141-151.
27. Legal L, David JR, Jallon M. 1992. Toxicity and attraction effects produced by Morinda citrifolia fruits on the Drosophila melanogaster complex of species. Chemoecology. 3:125-129.
28. Margaritis LH, Kafatos FC, Petri WH. 1980. The eggshell of Drosophila melanogaster. J Cell Sci. 43:1-35.
29. Markow TA, O'Grady PM. 2005. Evolutionary genetics of reproductive behavior in Drosophila: connecting the dots. Annu Rev Genet. 39:263-291.
30. Martinez-Cruzado JC, Swimmer C, Fenerjian MG, Kafatos FC. 1988. Evolution of the autosomal chorion locus in Drosophila. I. General organization of the locus and sequence comparisons of genes s15 and s19 in evolutionary distant species. Genetics. 119:663-677.
31. Martinez-Cruzado JC. 1990. Evolution of the autosomal chorion cluster in Drosophila. IV. The Hawaiian Drosophila: rapid protein evolution and constancy in the rate of DNA divergence. J Mol Evol. 31:402-423.
32. Mayr E. 1963. Animal species and evolution. Cambridge: Harvard University Press.
33. McDonald JH, Kreitman M. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 351:652-654.
34. Moriyama EN, Powell JR. 1996. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 13:261-277.
35. Morse GE, Farrell BD. 2005. Interspecific phylogeography of the Stator limbatus species complex: the geographic context of speciation and specialization. Mol Phylogenet Evol. 36:201-213.
36. Nielsen R. 2005. Molecular signatures of natural selection. Annu Rev Genet. 39:197-218.
37. Nielson R, Yang Z. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics. 148:929-936.
38. Panhuis TM, Swanson WJ. 2006. Molecular evolution and population genetic analysis of candidate female reproductive genes in Drosophila. Genetics. 173:2039-2047.
39. Parks S, Wakimoto B, Spradling AC. 1986. Replication and expression of an X-linked cluster of Drosophila chorion genes. Dev Biol. 117:294-305.
40. Pascucci T, Perino J, Mahowald AP, Waring GL. 1996. Eggshell assembly in Drosophila: processing and localization of vitelline membrane and chorion proteins. Dev Biol. 117:590-598.
41. Petri WH, Wyman AR, Kafatos FC. 1976. Specific protein synthesis in cellular differentiation. III. The eggshell proteins of Drosophila melanogaster and their program of synthesis. Dev Biol. 49:185-199.
42. Powell JR. 1997. Progress and prospects in evolutionary biology: the Drosophila model. Oxford: Oxford University press.
43. R'Kha S, Capy P, David JR. 1991. Host-plant specialization in the Drosophila melanogaster species complex: a physiological, behavioral, and genetical analysis. Proc Natl Acad Sci USA. 88:1835-1839.
44. Regier JC, Paukstadt U, Paukstadt LH, Mitter C, Peigler RS. 2005. Phylogenetics of eggshell morphogenesis in Antheraea (lepidoptera: saturniidae): unique origin and repeated reduction of the aeropyle crown. Syst Biol. 54:254-267.
45. Rio B, Lemeunier F, Lachaise D. 1983. Evolution d'une spécialisation saisonnière chez Drosophila erecta (Dipt., Drosophilidae). Ann Soc Entomol Fr. 19:235-248.
46. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analysis by the coalescent and other methods. Bioinformatics. 19:2496-2497.
47. Singh RS, Kulathinal RJ. 2000. Sex gene pool evolution and speciation: a new paradigm. Genes Genet Syst. 75:119-130.
48. Spradling AC. 1981. The organization and amplification of two chromosomal domains containing Drosophila chorion genes. Cell. 27:193-201.
49. Spradling AC. 1993. Developmental genetics of oogenesis. In: Bate M, Martinez-Arias A, editors. The Development of Drosophila melanogaster. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press. p. 1-70.
50. Spradling AC, Mahowald AP. 1980. Amplification of genes for chorion proteins during oogenesis in Drosophila melanogaster. Proc Natl Acad Sci USA. 77:1096-1100.
51. Swanson WJ, Vacquier VD. 1998. Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein. Science. 281:710-712.
52. Swanson WJ, Vacquier VD. 2002. The rapid evolution of reproductive proteins. Nat Rev Genet. 3:137-144.
53. Swanson WJ, Wong A, Wolfner MF, Aquadro CF. 2004. Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics. 168:1457-1465.
54. Tajima F. 1989. Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 123:585-595.
55. Tamura K, Subramanian S, Kumar S. 2004. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol. 21:36-44.
56. Tang H, Wyckoff GJ, Lu J, Wu C-I. 2004. A universal evolutionary index for amino acid changes. Mol Biol Evol. 21:1548-1556.
57. 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.
58. Vermaak D, Henikoff S, Malik HS. 2005. Positive selection drives the evolution of rhino, a member of the heterochromatin protein family 1 in Drosophila. Plos Genetics. 1:96-0108.
59. Wernersson R, Pederson G. 2003. Multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res. 31:3537-3539.
60. Yang Z. 2005. The power of phylogenetic comparison in revealing protein function. Proc Natl Acad Sci USA. 102:3179-3180.
61. Yang Z, Nielsen R, Goldman N, Pederson AM. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics. 155:431-449.
62. Yang Z. 2000. Phylogenetic analysis by maximum likelihood (PAML). London: University College London.
63. Yang Z, Nielsen R. 2000. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol. 17:32-43.
64. Zigler KS, McCartney MA, Levitan DR, Lessios HA. 2005. Sea urchin bindin divergence predicts gamete compatibility. Evolution. 59:2399-2404.