The evolution of novelty in conserved genes; Evidence of positive selection in the Drosophila fruitless gene is localised to alternatively spliced exons

Heredity

Volumn 112, Issue 3, 2014, Pages 300-306

  Parker, D J ^a   Gardiner, A ^b   Neville, M C ^c   Ritchie, M G ^a   Goodwin, S F ^c  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b UNIVERSITÉ DE LYON   (France)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

alternative splicing; Drosophila; fru; gene diversity; positive selection

Indexed keywords

DROSOPHILA PROTEIN; FRU PROTEIN, DROSOPHILA; NERVE PROTEIN; TRANSCRIPTION FACTOR;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BINDING SITE; BIOLOGICAL MODEL; CHROMOSOME MAP; DROSOPHILA; DROSOPHILA MELANOGASTER; EXON; FEMALE; GENETIC SELECTION; GENETICS; MALE; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CHROMOSOME MAPPING; CONSERVED SEQUENCE; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EXONS; FEMALE; MALE; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; SELECTION, GENETIC; TRANSCRIPTION FACTORS;

EID: 84894033872     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2013.106     Document Type: Article

References (69)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990). Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Anand A, Villella A, Ryner LC, Carlo T, Goodwin SF, Song HJ, et al. (2001). Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics 158: 1569-1595.
3. Ast G (2004). How did alternative splicing evolve? Nat Rev Genet 5: 773-782.
4. Baker DA, Meadows LA, Wang J, Dow JA, Russell S (2007). Variable sexually dimorphic gene expression in laboratory strains of Drosophila melanogaster. BMC Genomics 8: 454.
5. Bertossa RC, van de Zande L, Beukeboom LW (2009). The fruitless gene in Nasonia displays complex sex-specific splicing and contains new zinc finger domains. Mol Biol Evol 26: 1557-1569.
6. Billeter JC, Rideout EJ, Dornan AJ, Goodwin SF (2006a). Control of male sexual behavior in Drosophila by the sex determination pathway. Curr Biol 16: R766-R776.
7. Billeter JC, Villella A, Allendorfer JB, Dornan AJ, Richardson M, Gailey DA, et al. (2006b). Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene. Curr Biol 16: 1063-1076.
8. Birney E, Clamp M, Durbin R (2004). GeneWise and genomewise. Genome Res 14: 988-995.
9. Boerjan B, Tobback J, De Loof A, Schoofs L, Huybrechts R (2011). fruitless RNAi knockdown in males interferes with copulation success in Schistocerca gregaria. Insect Biochem Mol Biol 41: 340-347.
10. Bonchuk A, Denisov S, Georgiev P, Maksimenko O (2011). Drosophila BTB/POZ domains of 'ttk group' can form multimers and selectively interact with each other. J Mol Biol 412: 423-436.
11. Carroll SB (2005). Evolution at two levels: on genes and form. PLoS Biol 3: 1159-1166.
12. Chothia C, Gough J, Vogel C, Teichmann SA (2003). Evolution of the protein repertoire. Science 300: 1701-1703.
13. Clynen E, Ciudad L, Belles X, Piulachs MD (2011). Conservation of fruitless, role as master regulator of male courtship behaviour from cockroaches to flies. Dev Genes Evol 221: 43-48.
14. Coyne JA, Orr HA (2004). Speciation. Sinauer: Sunderland, MA, USA.
15. Da Lage JL, Kergoat GJ, Maczkowiak F, Silvain JF, Cariou ML, Lachaise D (2007). A phylogeny of Drosophilidae using the Amyrel gene: questioning the Drosophila melanogaster species group boundaries. J Zool System Evol Res 45: 47-63.
16. Drosophila 12 Genomes Consortium (2007). Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218.
17. Ellegren H, Smeds L, Burri R, Olason PI, Backstrom N, Kawakami T, et al. (2012). The genomic landscape of species divergence in Ficedula flycatchers. Nature 491: 756-760.
18. Ermakova EO, Nurtdinov RN, Gelfand MS (2006). Fast rate of evolution in alternatively spliced coding regions of mammalian genes. BMC Genomics. 7: 84.
19. Fitzpatrick MJ, Ben-Shahar Y, Smid HM, Vet LEM, Robinson GE, Sokolowski MB (2005). Candidate genes for behavioural ecology. Trends Ecol Evol 20: 96-104.
20. Gailey DA, Billeter JC, Liu JH, Bauzon F, Allendorfer JB, Goodwin SF (2006). Functional conservation of the fruitless male sex-determination gene across 250Myr of insect evolution. Mol Biol Evol 23: 633-643.
21. Gaunt MW, Miles MA (2002). An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol Biol Evol 19: 748-761.
22. Gleason JM, Ritchie MG (2004). Do quantitative trait loci (QTL) for a courtship song difference between Drosophila simulans and D. sechellia coincide with candidate genes and intraspecific QTL? Genetics 166: 1303-1311.
23. Gloor GB, Preston CR, Johnsonschlitz DM, Nassif NA, Phillis RW, Benz WK, et al. (1993). Type-I repressors of P-element mobility. Genetics 135: 81-95.
24. Graveley BR (2001). Alternative splicing: increasing diversity in the proteomic world. Trends Genet 17: 100-107.
25. Harr B, Turner LM (2010). Genome-wide analysis of alternative splicing evolution among Mus subspecies. Mol Ecol 19: 228-239.
26. Hoekstra HE, Coyne JA (2007). The locus of evolution: Evo devo and the genetics of adaptation. Evolution 61: 995-1016.
27. Hughes AL (2011). Runaway evolution of the male-specific exon of the doublesex gene in Diptera. Gene 472: 1-6.
28. Innan H, Kondrashov F (2010). The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11: 97-108.
29. Ito H, Fujitani K, Usui K, ShimizuNishikawa K, Tanaka S, Yamamoto D (1996). Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc Natl Acad Sci USA 93: 9687-9692.
30. Jin L, Kryukov K, Clemente JC, Komiyama T, Suzuki Y, Imanishi T, et al. (2008). The evolutionary relationship between gene duplication and alternative splicing. Gene 427: 19-31.
31. Kopelman NM, Lancet D, Yanai I (2005). Alternative splicing and gene duplication are inversely correlated evolutionary mechanisms. Nature Genet. 37: 588-589.
32. Kraaijeveld K, Kraaijeveld-Smit FJL, Maan ME (2011). Sexual selection and speciation: the comparative evidence revisited. Biol Rev 86: 367-377.
33. Lagisz M, Wen SY, Routtu J, Klappert K, Mazzi D, Morales-Hojas R, et al. (2012). Two distinct genomic regions, harbouring the period and fruitless genes, affect male courtship song in Drosophila montana. Heredity 108: 602-608.
34. Locker J (2001). Transcription Factors. Academic Press: San Diego, CA, USA.
35. Long M, Betran E, Thornton K, Wang W (2003). The origin of new genes: glimpses from the young and old. Nat Rev Genet 4: 865-875.
36. Lynch M, Conery JS (2000). The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
37. Lynch M, O'Hely M, Walsh B, Force A (2001). The probability of preservation of a newly arisen gene duplicate. Genetics 159: 1789-1804.
38. Martin A, Orgogozo V (2013). The Loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation. Evolution 67: 1235-1250.
39. Matsuo T, Sugaya S, Yasukawa J, Aigaki T, Fuyama Y (2007). Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biol 5: e118.
40. Mendelson TC, Shaw KL (2005). Sexual behaviour: rapid speciation in an arthropod. Nature 433: 375-376.
41. Mount SM, Burks C, Hertz G, Stormo GD, White O, Fields C (1992). Splicing signals in Drosophila - intron size, information-content, and consensus sequences. Nucleic Acids Res 20: 4255-4262.
42. Powell JR (1997). Progress and prospects in evolutionary biology: the Drosophila model. Oxford University Press.
43. Ramensky VE, Nurtdinov RN, Neverov AD, Mironov AA, Gelfand MS (2008). Positive selection in alternatively spliced exons of human genes. Am J Human Genet 83: 94-98.
44. Rundle HD, Nosil P (2005). Ecological speciation. Ecol Lett 8: 336-352.
45. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, et al. (1996). Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87: 1079-1089.
46. Salvemini M, D'Amato R, Petrella V, Aceto S, Nimmo D, Neira M, et al. (2013). The orthologue of the fruitfly sex behaviour gene fruitless in the mosquito Aedes aegypti: evolution of genomic organisation and alternative splicing. PLoS One 8: e48554.
47. Salvemini M, Polito C, Saccone G (2010). fruitless alternative splicing and sex behaviour in insects: an ancient and unforgettable love story? J Genet 89: 287-299.
48. Salvemini M, Robertson M, Aronson B, Atkinson P, Polito LC, Saccone G (2009). Ceratitis capitata transformer-2 gene is required to establish and maintain the autoregulation of Cctra, the master gene for female sex determination. Int J Dev Biol 53: 109-120.
49. Shirangi TR, Dufour HD, Williams TM, Carroll SB (2009). Rapid evolution of sex pheromone-producing enzyme expression in Drosophila. PLoS Biol 7: e1000168.
50. Sobrinho I, de Brito R (2010). Evidence for positive selection in the gene fruitless in Anastrepha fruit flies. BMC Evol Biol 10: 293.
51. Song HJ, Billeter JC, Reynaud E, Carlo T, Spana EP, Perrimon N, et al. (2002). The fruitless gene is required for the proper formation of axonal tracts in the embryonic central nervous system of Drosophila. Genetics 162: 1703-1724.
52. Song HJ, Taylor BJ (2003). fruitless gene is required to maintain neuronal identity in evenskipped-expressing neurons in the embryonic CNS of Drosophila. J Neurobiol 55: 115-133.
53. Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, et al. (2002). The bioperl toolkit: Perl modules for the life sciences. Genome Res 12: 1611-1618.
54. Stern DL (2000). Perspective: evolutionary developmental biology and the problem of variation. Evolution 54: 1079-1091.
55. Stern DL, Orgogozo V (2008). The loci of evolution: how predictable is genetic evolution? Evolution 62: 2155-2177.
56. Stern DL, Orgogozo V (2009). Is genetic evolution predictable? Science 323: 746-751.
57. Swanson WJ, Nielsen R, Yang QF (2003). Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 20: 18-20.
58. Talavera D, Vogel C, Orozco M, Teichmann SA, de la Cruz X (2007). The (In) dependence of alternative splicing and gene duplication. PLoS Comput Biol 3: 375-388.
59. Thompson JD, Higgins DG, Gibson TJ (1994). ClustalW: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
60. Ustinova J, Mayer F (2006). Alternative starts of transcription, several paralogues, and almost-fixed interspecific differences of the gene fruitless in a hemimetabolous insect. J Mol Evol 63: 788-800.
61. Usui-Aoki K, Ito H, Ui-Tei K, Takahashi K, Lukacsovich T, Awano W, et al. (2000). Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat Cell Biol 2: 500-506.
62. Villella A, Hall JC (2008). Neurogenetics of courtship and mating in Drosophila. In: Hall JC (ed). In Advances in Genetics, Vol 62, 67-184.
63. Wilkins AS (1995). Moving up the hierarchy - A hypothesis on the evolution of a genetic sex determination pathway. Bioessays 17: 71-77.
64. Wolfe SA, Nekludova L, Pabo CO (2000). DNA recognition by Cys(2)His(2) zinc finger proteins. Annu Rev Biophys Biomolec Struct 29: 183-212.
65. Wong WSW, Yang ZH, Goldman N, Nielsen R (2004). Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168: 1041-1051.
66. Yang ZH (1997). PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
67. Yang ZH, Bielawski JP (2000). Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15: 496-503.
68. Zdobnov EM, von Mering C, Letunic I, Torrents D, Suyama M, Copley RR, et al. (2002). Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science 298: 149-159.
69. Zollman S, Godt D, Prive GG, Couderc JL, Laski FA (1994). The BTB domain, found primarily in zinc-finger proteins, defines an evolutionarily conserved family that includes several developmentally-regulated genes in Drosophila. Proc Natl Acad Sci USA 91: 10717-10721.