Gene duplication, tissue-specific gene expression and sexual conflict in stalk-eyed flies (Diopsidae)

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1600, 2012, Pages 2357-2375

  Baker, Richard H ^a   Narechania, Apurva ^a   Johns, Philip M ^b   Wilkinson, Gerald S ^c  

^a DIVISION OF INVERTEBRATE ZOOLOGY   (United States)

^b BARD COLLEGE   (United States)

^c Bldg 142   (United States)

Author keywords

Gene duplication; Sexual conflict; Spermatogenesis; Stalk eyed flies; Tubulin genes

Indexed keywords

ADAPTATION; ECOLOGICAL MODELING; FLY; GENE EXPRESSION; MORPHOLOGY; SEXUAL CONFLICT; SEXUAL DIMORPHISM; SEXUAL SELECTION;

DIOPSIDAE;

EID: 84863837782     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0287     Document Type: Review

References (149)

1. Emlen, D. J., Corley Lavine, L. & Ewen-Campen, B. 2007 On the origin and evolutionary diversification ofbeetle horns. Proc. Natl Acad. Sci. USA 104, 8661-8668. (doi:10.1073/pnas.0701209104)
2. Hegyi, G., Torok, J., Tóth, L., Garamszegi, L. Z. & Rosivall, B. 2006 Rapid temporal change in theexpression and age-related information content of a sexually selected trait. J. Evol. Biol. 19, 228-238. (doi:10.1111/j.1420-9101.2005.00970.x)
3. Meyer, A. 1997 The evolution of sexually selected traits in male swordtail fishes (Xiphophorus: Poeciliidae). Heredity 79, 329-337. (doi:10.1038/hdy.1997.161)
4. Omland, K. E. & Lanyon, S. M. 2000 Reconstructingplumage evolution in orioles (Icterus): repeated convergence and reversal in patterns. Evolution 54, 2119-2133. (doi:10.1111/j.0014-3820.2000.tb01254.x)
5. van Doorn, G. S. 2009 Intralocus sexual conflict. Ann.NY Acad. Sci. 1168, 52-71. (doi:10.1111/j.1749-6632. 2009.04573.x)
6. Bonduriansky, R. & Chenoweth, S. F. 2009 Intralocus sexual conflict. Trends Ecol. Evol. 24, 280-288.(doi:10.1016/j.tree.2008.12.005)
7. Rice, W. R. 1992 Sexually antagonistic genes: experimental evidence. Science 256, 1436-1439. (doi:10. 1126/science.1604317)
8. Rice, W. R. 1996 Sexually antagonistic male adaptationtriggered by experimental arrest of female evolution. Nature 381, 232-235. (doi:10.1038/381232a0)
9. Chippindale, A. K., Gibson, J. R. & Rice, W. R. 2001 Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc. Natl Acad. Sci. USA 98, 1671-1675. (doi:10.1073/pnas.041378098)
10. Prasad, N. G., Bedhomme, S., Day, T. & Chippendale, A. K. 2007 An evolutionary cost of separate gendersrevealed by male-limited evolution. Am. Nat. 169,29-37. (doi:10.1086/509941)
11. Morrow, E. H., Stewart, A. D. & Rice, W. R. 2008 Assessing the extent of genome-wide intralocus sexualconflict via experimentally enforced gender-limited selection. J. Evol. Biol. 21, 1046-1054. (doi:10.1111/j.1420-9101.2008.01542.x)
12. Gibson, J. R., Chippindale, A. K. & Rice, W. R.2002 The X chromosome is a hot spot for sexuallyantagonistic fitness variation. Proc. R. Soc. Lond. B 269, 499-505. (doi:10.1098/rspb.2001.1863)
13. Rice, W. R. & Chippindale, A. K. 2002 The evolution ofhybrid infertility: perpetual coevolution between genderspecific and sexually antagonistic genes. Genetica 116, 179-188. (doi:10.1023/A:1021205130926)
14. Parisi, M., Nuttall, R., Naiman, D., Bouffard, G., Malley, J., Andrews, J., Eastman, S. & Oliver, B. 2003 Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299, 697-700. (doi:10.1126/science.1079190)
15. Ranz, J. M., Castillo-Davis, C. I., Meiklejohn, C. D. & Hartl, D. L. 2003 Sex-dependent gene expression andevolution of the Drosophila transcriptome. Science 300, 1742-1745. (doi:10.1126/science.1085881)
16. Sturgill, D., Zhang, Y., Parisi, M. & Oliver, B.2007 Demasculinization of X chromosomes in the Drosophila genus. Nature 450, 238-241. (doi:10.1038/nature06330)
17. Schutt, C. & Nothiger, R. 2000 Structure, function andevolution of sex-determining systems in Dipteraninsects. Development 127, 667-677.
18. Connallon, T. & Clark, A. G. 2011 The resolution ofsexual antagonism by gene duplication. Genetics 187,919-937. (doi:10.1534/genetics.110.123729)
19. Gallach, M. & Betran, E. 2011 Intralocus sexual conflictresolved through gene duplication. Trends Ecol. Evol. 26, 222-228. (doi:10.1016/j.tree.2011.02.004)
20. Vicoso, B. & Charlesworth, B. 2006 Evolution on the Xchromosome: unusual patterns and processes. Nat. Rev.Genet. 7, 645-653. (doi:10.1038/nrg1914)
21. Rice, W. R. 1984 Sex chromosomes and the evolution ofsexual dimorphism. Evolution 38, 735-742. (doi:10.2307/2408385)
22. Fry, J. D. 2010 The genomic location of sexuallyantagonistic variation: some cautionary comments. Evolution 64, 1510-1516. (doi:10.1111/j.1558-5646.2009.00898.x)
23. Zhang, Y., Sturgill, D., Parisi, M., Kumar, S. & Oliver, B. 2007 Constraint and turnover in sex-biased geneexpression in the genus Drosophila. Nature 450, 233-238. (doi:10.1038/nature06323)
24. Baker, D. A. & Russell, S. 2011 The role of testis-specific gene expression in sex chromosome evolutionof Anopheles gambiae. Genetics 189, 1117-1120. (doi:10.1534/genetics.111.133157)
25. Prince, E. G., Kirkland, D. & Demuth, J. P. 2010 Hyperexpression of the X chromosome in both sexesresults in extensive female bias of X-linked genes in the flour beetle. Genome Biol. Evol. 2, 336-346. (doi:10.1093/gbe/evq024)
26. Hense, W., Baines, J. F. & Parsch, J. 2007 X chromosomeinactivation during Drosophila spermatogenesis. PLoSBiol. 5, 2288-2295. (doi:10.1371/journal.pbio.0050273)
27. Lifschytz, E. & Lindsley, D. L. 1972 The role of X-chromosome inactivation during spermatogenesis. Proc. Natl Acad. Sci. USA 69, 182-186. (doi:10.1073/pnas.69.1.182)
28. Betran, E., Thornton, K. & Long, M. 2002 Retroposednew genes out of the X in Drosophila. Genome Res. 12,1854-1859. (doi:10.1101/gr.6049)
29. Kemkemer, C., Hense, W. & Parsch, J. 2011 Fine-scaleanalysis of X chromosome inactivation in the male germline of Drosophila melanogaster. Mol. Biol. Evol. 28, 1561-1563. (doi:10.1093/molbev/msq355)
30. Vibranovski, M. D., Zhang, Y. & Long, M. Y. 2009General gene movement off the X chromosome in theDrosophila genus. Genome Res. 19, 897-903. (doi:10. 1101/gr.088609.108)
31. Vibranovski, M. D., Lopes, H. F., Karr, T. L. & Long, M. 2009 Stage-specific expression profiling ofDrosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testis-expressed genes. PLoS Genet. 5, e1000731. (doi:10.1371/journal.pgen.1000731)
32. Meisel, R. P., Han, M. V. & Hahn, M. W. 2009 A com-plex suite of forces drives gene traffic from Drosophila Xchromosomes. Genome Biol. Evol. 2009, 176-188. (doi:10.1093/gbe/evp018)
33. Wu, C. I. & Xu, E. Y. 2003 Sexual antagonism and Xinactivation-the SAXI hypothesis. Trends Genet. 19,243-247. (doi:10.1016/S0168-9525(03)00058-1)
34. Vicoso, B. & Charlesworth, B. 2009 The deficit ofmale-biased genes on the, D. melanogaster X chromosome is expression-dependent: a consequence of dosage compensation? J. Mol. Evol. 68, 576-583. (doi:10.1007/s00239-009-9235-4)
35. Bai, Y., Casola, C., Feschotte, C. & Betran, E. 2007 Comparative genomics reveals a constant rate of orig-ination and convergent acquisition of functional retrogenes in Drosophila. Genome Biol. 8, R11. (doi:10.1186/gb-2007-8-1-r11)
36. Schrider, D. R., Stevens, K., Cardeno, C. M., Langley, C. H. & Hahn, M. W. 2011 Genome-wide analysis of ret-rogene polymorphisms in Drosophila melanogaster. Genome Res. 21, 2087-2095. (doi:10.1101/gr.116434.110)
37. Mikhaylova, L. & Nurminsky, D. 2011 Lack ofglobal meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome. BMC Biol. 9, 29. (doi:10.1186/1741-7007-9-29)
38. Meiklejohn, C. D., Landeen, E. L., Cook, J. M., Kingan, S. B. & Presgraves, D. C. 2010 Sex chromo-some-specific regulation in the Drosophila male germline but little evidence for chromosomal dosage compensation or meiotic inactivation. PLoS Biol. 9, e1001126. (doi:10.1371/journal.pbio.1001126)
39. Metta, M. & Schlotterer, C. 2010 Non-random geno-mic integration-an intrinsic property of retrogenes in Drosophila? BMC Evol. Biol. 10, 114. (doi:10.1186/1471-2148-10-114)
40. White-Cooper, H. 2010 Molecular mechanisms ofgene regulation during Drosophila spermatogenesis. Reproduction 139, 11-21. (doi:10.1530/REP-09-0083)
41. Chintapalli, V. R., Wang, J. & Dow, J. A. 2007 UsingFlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 39, 715-720. (doi:10.1038/ng2049)
42. White-Cooper, H. & Bausek, N. 2010 Evolutionand spermatogenesis. Phil. Trans. R. Soc. B 365, 1465-1480. (doi:10.1098/rstb.2009.0323)
43. Mikhaylova, L. M., Nguyen, K. & Nurminsky, D. I.2008 Analysis of the Drosophila melanogaster testes tran-scriptome reveals coordinate regulation of paralogous genes. Genetics 179, 305-315. (doi:10.1534/genetics. 107.080267)
44. Hiller, M. et al. 2004 Testis-specific TAF homologs collab-orate to control a tissue-specific transcription program. Development 131, 5297-5308. (doi:10.1242/dev.01314)
45. Hiller, M. A., Lin, T-Y., Wood, C. & Fuller, M. T. 2001 Developmental regulation of transcription by a tissuespecific TAF homolog. Genes Dev. 15, 1021-1030. (doi:10.1101/gad.869101)
46. Torgerson, D. G. & Singh, R. S. 2004 Rapid evolutionthrough gene duplication and subfunctionalization ofthe testes-specific a4 proteasome subunits in Drosophila. Genetics 168, 1421-1432. (doi:10.1534/genetics.104. 027631)
47. Belote, J. M. & Zhong, L. 2009 Duplicated proteasomesubunit genes in Drosophila and their roles in spermato-genesis. Heredity 103, 23-31. (doi:10.1038/hdy.2009.23)
48. Tracy, C., Rio, J., Motiwale, M., Christensen, S. M. Betran, E. 2010 Convergently recruited nuclear transport retrogenes are male biased in expression and evolving under positive selection in Drosophila. Genetics 184, 1067-1076. (doi:10.1534/genetics.109.113522)
49. Nielsen, M., Gadagkar, S. & Gutzwiller, L. 2010 Tubu-lin evolution in insects: gene duplication and subfunctionalization provide specialized isoforms in a functionally constrained gene family. BMC Evol. Biol. 10, 113. (doi:10.1186/1471-2148-10-113)
50. Gallach, M., Chandrasekaran, C. & Betran, E.2010 Analyses of nuclearly encoded mitochondrialgenes suggest gene duplication as a mechanism for resolving intralocus sexually antagonistic conflict in Drosophila. Genome Biol. Evol. 2, 835-850. (doi:/10. 1093/gbe/evq069)
51. Gallach, M., Domingues, S. & Betran, E. 2011 Geneduplication and the genome distribution of sex-biasedgenes. Int. J. Evol. Biol. 2011, 1-20. (doi:10.4061/2011/989438)
52. Proulx, S. R. & Phillips, P. C. 2006 Allelic diver-gence precedes and promotes gene duplication. Evolution 60, 881-892. (doi:10.1111/j.0014-3820.2006.tb01168.x)
53. Wilkinson, G. S. & Dodson, G. 1997 Function andevolution of antlers and eye stalks in flies. In The evol-ution of mating systems in insects and arachnids (eds J. Choe & B. Crespi), pp. 310-328. Cambridge, UK: Cambridge University Press.
54. Yeates, D. K. & Wiegmann, B. M. 1999 Congruenceand controversy: toward a higher-level phylogeny ofDiptera. Annu. Rev. Entomol. 44, 397-428. (doi:10.1146/annurev.ento.44.1.397)
55. Burkhardt, D. & de la Motte, I. 1985 Selective press-ures, variability, and sexual dimorphism in stalk-eyedflies (Diopsidae). Naturwissenschaften 72, 204-206. (doi:10.1007/BF01195763)
56. Feijen, H. R. 2011 The genus Teleopsis Rondani (Dip-tera, Diopsidae): discussion of its taxonomic positionand revision of the species occurring in the Philippines. Zool. Meded. 85, 79-140.
57. Feijen, H. R. 1989 Diopsidae. In Flies of the nearcticregion (ed. G. C. D. Griffiths), pp. 1-122. Stuttgart,Germany: E. Schweizerbart'sche Verlagsbuchhandlung.
58. Baker, R. H. & Wilkinson, G. S. 2001 Phylogene-tic analysis of sexual dimorphism and eye-span allometry in stalk-eyed flies (Diopsidae). Evolution 55, 1373-1385. (doi:10.1111/j.0014-3820.2001.tb00659.x)
59. Baker, R. H., Wilkinson, G. S. & DeSalle, R. 2001 Thephylogenetic utility of different types of molecular dataused to infer evolutionary relationships among stalkeyed flies (Diopsidae). Syst. Biol. 50, 87-105. (doi:10.1080/106351501750107512)
60. Burkhardt, D., de la Motte, I. & Lunau, K. 1994 Signalling fitness: larger males sire more offspring.Studies of the stalk-eyed fly Cyrtodiopsis whitei (Diopsidae, Diptera). J. Comp. Physiol. A 174, 61-64. (doi:10.1007/BF00192006)
61. Small, J., Cotton, S., Fowler, K. & Pomiankowski, A.2009 Male eyespan and resource ownership affect con-test outcome in the stalk-eyed fly, Teleopsis dalmanni. Anim. Behav. 78, 1213-1220. (doi:10.1016/j.anbehav.2009.08.009)
62. Panhuis, T. M. & Wilkinson, G. S. 1999 Exaggeratedmale eye span influences contest outcome in stalk-eyed flies. Behav. Ecol. Sociobiol. 46, 221-227. (doi:10.1007/s002650050613)
63. Lorch, P. D., Wilkinson, G. S. & Reillo, P. R. 1993 Copulation duration and sperm precedence in thestalk-eyed fly Cyrtodiopsis whitei (Diptera, Diopsidae). Behav. Ecol. Sociobiol. 32, 303-311. (doi:10.1007/BF00183785)
64. Kotrba, M. 1996 Sperm transfer by spermatophore inDiptera: new results from the Diopsidae. Zool. J. Linn.Soc. 117, 305-323. (doi:10.1111/j.1096-3642.1996.tb02192.x)
65. Wilkinson, G. S., Kahler, H. & Baker, R. H. 1998 Evolution of female mating preferences in stalk-eyedflies. Behav. Ecol. 9, 525-533. (doi:10.1093/beheco/9.5.525)
66. Hingle, A., Fowler, K. & Pomiankowski, A. 2001 Size-dependent mate preference in the stalk-eyed flyCyrtodiopsis dalmanni. Anim. Behav. 61, 589-595. (doi:10.1006/anbe.2000.1613)
67. Burkhardt, D. & de la Motte, I. 1988 Big 'antlers' arefavoured: female choice in stalk-eyed flies (Diptera,Insecta), field collected harems and laboratory experiments. J. Comp. Physiol. A 162, 649-652. (doi:10. 1007/BF01342640)
68. Cotton, S., Rogers, D. W., Small, J., Pomiankowski, A. & Fowler, K. 2006 Variation in preference for a male orna-ment is positively associated with female eyespan in the stalk-eyed fly Diasemopsis meigenii. Proc. R. Soc. B 273, 1287-1292. (doi:10.1098/rspb.2005.3449)
69. Lande, R. 1981 Models of speciation by sexual selectionon polygenic traits. Proc. Natl Acad. Sci. USA 78,3721-3725. (doi:10.1073/pnas.78.6.3721)
70. Wilkinson, G. S. & Reillo, P. R. 1994 Female choiceresponse to artificial selection on an exaggerated maletrait in a stalk-eyed fly. Proc. R. Soc. Lond. B 255, 1-6. (doi:10.1098/rspb.1994.0001)
71. Wilkinson, G. S. & Taper, M. 1999 Evolution of geneticvariation for condition dependent traits in stalk-eyedflies. Proc. R. Soc. Lond. B 266, 1685-1690. (doi:10. 1098/rspb.1999.0832)
72. Wilkinson, G. S. 1993 Artificial sexual selection altersallometry in the stalk-eyed fly Cyrtodiopsis dalmanni(Diptera: Diopsidae). Genet. Res. 62, 213-222. (doi:10.1017/S001667230003192X)
73. Pomiankowski, A. & Møller, A. P. 1995 A resolution ofthe lek paradox. Proc. R. Soc. Lond. B 260, 21-29. (doi:10.1098/rspb.1995.0054)
74. Tomkins, J. L., Radwan, J., Kotiaho, J. S. & Tregenza, T. 2004 Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19, 323-328. (doi:10.1016/j.tree.2004.03.029)
75. Rowe, L. & Houle, D. 1996 The lek paradox and thecapture of genetic variance by condition-dependenttraits. Proc. R. Soc. Lond. B 263, 1415-1421. (doi:10. 1098/rspb.1996.0207)
76. Cotton, S. & Pomiankowski, A. 2007 Sexual selection:does condition dependence fail to resolve the 'lek para-dox'? Curr. Biol. 17, R335-R337. (doi:10.1016/j.cub.2007.03.004)
77. Van Homrigh, A., Higgie, M., McGuigan, K. & Blows, M. W. 2007 The depletion of genetic variance by sexualselection. Curr. Biol. 17, 528-532. (doi:10.1016/j.cub.2007.01.055)
78. Pischedda, A. & Chippindale, A. K. 2006 Intralocussexual conflict diminishes the benefits of sexual selec-tion. PLoS Biol. 4, e356. (doi:10.1371/journal.pbio.0040356)
79. Johnstone, R. A. 1995 Sexual selection, honest adver-tisement and the handicap principle: reviewing theevidence. Biol. Rev. 70, 11-65. (doi:10.1111/j.1469-185X.1995.tb01439.x)
80. Cotton, S., Fowler, K. & Pomiankowski, A. 2004 Dosexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc. R. Soc. Lond. B 271, 771-783. (doi:10.1098/rspb.2004.2688)
81. Ahuja, A., De Vito, S. & Singh, R. 2011 Condi-tion dependence and the nature of genetic variationfor male sex comb bristle number in Drosophila melanogaster. Genetica 139, 505-510. (doi:10.1007/s10709-011-9572-2)
82. David, P., Hingle, A., Greig, D., Rutherford, A., Pomiankowski, A. & Fowler, K. 1998 Male sexualornament size but not asymmetry reflects condition in stalk-eyed flies. Proc. R. Soc. Lond. B 265, 2211-2216. (doi:10.1098/rspb.1998.0561)
83. Cotton, S., Fowler, K. & Pomiankowski, A. 2004 Condition dependence of sexual ornament size andvariation in the stalk-eyed fly Cyrtodiopsis dalmanni (Diptera:Diopsidae). Evolution 58, 1038-1046. (doi:10.1111/j.0014-3820.2004.tb00437.x)
84. Cotton, S., Fowler, K. & Pomiankowski, A. 2004 Heightened condition dependence is not a generalfeature of male eyespan in stalk-eyed flies (Diptera: Diopsidae). J. Evol. Biol. 17, 1310-1316. (doi:10.1111/j.1420-9101.2004.00754.x)
85. David, P., Bjorksten, T., Fowler, K. & Pomiankowski, A. 2000 Condition-dependent signalling of genetic vari-ation in stalk-eyes flies. Nature 406, 186-188. (doi:10. 1038/35018079)
86. Wilkinson, G. S., Swallow, J. G., Christianson, S. J. & Madden, K. 2003 Phylogeography of sex ratio and mul-tiple mating in stalk-eyed flies from southeast Asia. Genetica 117, 37-46. (doi:10.1023/A:1022360531703)
87. Presgraves, D. C., Severence, E. & Wilkinson, G. S.1997 Sex chromosome meiotic drive in stalk-eyed flies. Genetics 147, 1169-1180.
88. Wilkinson, G. S. & Sanchez, M. I. 2001 Sperm devel-opment, age and sex chromosome meiotic drive in thestalk-eyed fly, Cyrtodiopsis whitei. Heredity 87, 17-24. (doi:10.1046/j.1365-2540.2001.00898.x)
89. Lande, R. & Wilkinson, G. S. 1999 Models of sex-ratiomeiotic drive and sexual selection in stalk-eyed flies. Genet. Res. 74, 245-253. (doi:10.1017/S0016672399004218)
90. Wilkinson, G. S., Presgraves, D. C. & Crymes, L. 1998 Male eye span in stalk-eyed flies indicates genetic qual-ity by meiotic drive suppression. Nature 391, 276-278. (doi:10.1038/34640)
91. Johns, P. M., Wolfenbarger, L. L. & Wilkinson, G. S.2005 Genetic linkage between a sexually selected traitand X chromosome meiotic drive. Proc. R. Soc. B 272, 2097-2103. (doi:10.1098/rspb.2005.3183)
92. Wolfenbarger, L. L. & Wilkinson, G. S. 2001 Sex-linkedexpression of a sexually selected trait in the stalk-eyedfly, Cyrtodiopsis dalmanni. Evolution 55, 103-110. (doi:10.1111/j.0014-3820.2001.tb01276.x)
93. Wilkinson, G. S. & Fry, C. L. 2001 Meiotic drive alterssperm competitive ability in stalk-eyed flies. Proc. R. Soc. Lond. B 268, 2559-2564. (doi:10.1098/rspb.2001.1831)
94. Fry, C. L. & Wilkinson, G. S. 2004 Sperm survival infemale stalk-eyed flies depends on seminal fluid andmeiotic drive. Evolution 58, 1622-1626. (doi:10.1111/j.0014-3820.2004.tb01743.x)
95. Wilkinson, G. S., Amitin, E. G. & Johns, P. M. 2005 Sex-linked correlated responses in female reproductivetraits to selection on male eye span in stalk-eyed flies. Int. Comp. Biol. 45, 500-510. (doi:10.1093/icb/45.3.500)
96. Johns, P. M. & Wilkinson, G. S. 2007 X chromosomeinfluences sperm length in the stalk-eyed fly Cyrtodiopsis dalmanni. Heredity 99, 56-61. (doi:10.1038/sj.hdy. 6800963)
97. Baker, R. H., Morgan, J., Wang, X., Boore, J. L. & Wilkinson, G. S. 2009 Genomic analysis of a sexually-selected character: EST sequencing and microarray analysis of eye-antennal imaginal discs in the stalkeyed fly Teleopsis dalmanni (Diopsidae). BMC Genomics 10, 1-20. (doi:10.1186/1471-2164-10-361)
98. Stankiewicz, P. & Beaudet, A. L. 2007 Use of arrayCGH in the evaluation of dysmorphology, malfor-mations, developmental delay, and idiopathic mental retardation. Curr. Opin. Genet. Dev. 17, 182-192. (doi:10.1016/j.gde.2007.04.009)
99. Zhang, F., Gu, W., Hurles, M. E. & Lupski, J. R. 2009 Copy number variation in human health, disease, and evol-ution. Annu. Rev. Genomics Hum. Genet. 10, 451-481. (doi:10.1146/annurev.genom.9.081307.164217)
100. Baker, R. H. & Wilkinson, G. S. 2010 Comparativegenomic hybridization (CGH) reveals a neo-X chromosome and biased gene movement in stalk-eyed flies (Genus Teleopsis). PLoS Genet. 6, e1001121. (doi:10.1371/journal.pgen.1001121)
101. Zdobnov, E. M. et al. 2002 Comparative genome andproteome analysis of Anopheles gambiae and Drosophilamelanogaster. Science 298, 149-159. (doi:10.1126/science.1077061)
102. Severson, D. W., deBruyn, B., Lovin, D. D., Brown, S. E., Knudson, D. L. & Morlais, I. 2004 Comparativegenome analysis of the yellow fever mosquito Aedes aegypti with Drosophila melanogaster and the malaria vector mosquito Anopheles gambiae. J. Hered. 95, 103-113. (doi:10.1093/jhered/esh023)
103. Davies, N. & Roderick, G. K. 2005 Dipteran sexchromosomes in evolutionary developmental biology. In The Evolutionary biology of flies (ed. D. K. Yeates &B. M. Weigmann), pp. 196-213. New York, NY: Columbia University Press.
104. Charlesworth, D., Charlesworth, B. & Marais, G.2005 Steps in the evolution of heteromorphic sex chromo-somes. Heredity 95, 118-128. (doi:10.1038/sj.hdy.6800697)
105. Zhang, Y. E., Vibranovski, M. D., Krinsky, B. H. & Long, M. 2010 Age-dependent chromosomal distri-bution of male-biased genes in Drosophila. Genome Res. 20, 1526-1533. (doi:10.1101/gr.107334.110)
106. Birol, I. et al. 2009 De novo transcriptome assemblywith ABySS. Bioinformatics 25, 2872-2877. (doi:10.1093/bioinformatics/btp367)
107. Simpson, J. T., Wong, K., Jackman, S. D., Schein, J. E., Jones, S. J. M. & Birol, I. 2009 ABySS: a parallel assem-bler for short read sequence data. Genome Res. 19, 1117-1123. (doi:10.1101/gr.089532.108)
108. Drummond, A. J. et al. 2010 Geneious v. 5.4. See http://www.geneious.com
109. Rice, P., Longden, I. & Bleasby, A. 2000 EMBOSS: theEuropean molecular biology open software suite. TrendsGenet. 16, 276-277. (doi:10.1016/S0168-9525(00)02024-2)
110. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.2009 Ultrafast and memory-efficient alignment ofshort DNA sequences to the human genome. Genome Biol. 10, R25. (doi:10.1186/gb-2009-10-3-r25)
111. Aoyagi, N. & Wassarman, D. A. 2000 Genes encodingDrosophila melanogaster RNA polymerase. II General transcription factors: diversity in TFIIA and TFIID components contributes to gene-specific transcriptional regulation. J. Cell Biol. 150, F45-F50. (doi:10.1083/jcb.150.2.F45)
112. Gu, Z., Rifkin, S. A., White, K. P. & Li, W-H. 2004 Duplicate genes increase gene expression diversitywithin and between species. Nat. Genet. 36, 577-579. (doi:10.1038/ng1355)
113. Huerta-Cepas, J., Dopazo, J., Huynen, M. A. & Gabaldón, T. 2011 Evidence for short-time divergenceand long-time conservation of tissue-specific expression after gene duplication. Brief. Bioinf. 12, 442-448. (doi:10.1093/bib/bbr022)
114. Iwabe, N., Kuma, K. & Miyata, T. 1996 Evolution ofgene families and relationship with organismal evolution:rapid divergence of tissue-specific genes in the early evolution of chordates. Mol. Biol. Evol. 13, 483-493. (doi:10.1093/oxfordjournals.molbev.a025609)
115. Langille, M. G. I. & Clark, D. V. 2007 Parent genes of ret-rotransposition-generated gene duplicates in Drosophilamelanogaster have distinct expression profiles. Genomics 90, 334-343. (doi:10.1016/j.ygeno.2007.06.001)
116. Lynch, M. & Conery, J. S. 2000 The evolutionary fateand consequences of duplicate genes. Science 290, 1151-1155. (doi:10.1126/science.290.5494.1151)
117. Zhang, J. 2003 Evolution by gene duplication: anupdate. Trends Ecol. Evol. 18, 292-298. (doi:10.1016/S0169-5347(03)00033-8)
118. Mencarelli, C., Lupetti, P., Dallai, R. & Kwang, W. J.2008 New insights into the cell biology of insect axo-nemes. Int. Rev. Cell Mol. Biol. 268, 95-145. (doi:10.1016/S1937-6448(08)00804-6)
119. Nielsen, M. G., Turner, F. R., Hutchens, J. A. & Raff, E. C. 2001 Axoneme-specific b-tubulin specialization: aconserved C-terminal motif specifies the central pair. Curr. Biol. 11, 529-533. (doi:10.1016/S0960-9822(01)00150-6)
120. Popodi, E. M., Hoyle, H. D., Turner, F. R., Xu, K., Kruse, S. & Raff, E. C. 2008 Axoneme specializationembedded in a 'Generalist' b-tubulin. Cell Motil. Cytoskelet. 65, 216-237. (doi:10.1002/cm.20256)
121. Raff, E. C., Hoyle, H. D., Popodi, E. M. & Turner, F. R. 2008 Axoneme b-tubulin sequence determines attachment of outer dynein arms. Curr. Biol. 18, 911-914. (doi:10.1016/j.cub.2008.05.031)
122. Haerty, W. et al. 2007 Evolution in the fast lane: rapidlyevolving sex-related genes in Drosophila. Genetics 177,1321-1335. (doi:10.1534/genetics.107.078865)
123. Swanson, W. J. & Vacquier, V. D. 2002 The rapidevolution of reproductive protein. Nat. Rev. Genet. 3, 137-144. (doi:10.1038/nrg733)
124. Nielsen, M. G., Caserta, J. M., Kidd, S. J. & Phillips, C.M. 2006 Functional constraint underlies 60 millionyear stasis of Dipteran testis-specific b-tubulin. Evol. Dev. 8, 23-29. (doi:10.1111/j.1525-142X.2006. 05072.x)
125. Foldvari, M., Pomiankowski, A., Cotton, S. & Carr, M. 2007 A morphological and molecular description of anew Teleopsis species (Diptera: Diopsidae) from Thailand. Zootaxa 1620, 37-51.
126. Edgar, R. C. 2004 MUSCLE: multiple sequencealignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. (doi:10.1093/nar/gkh340)
127. Guindon, S. & Gascuel, O. 2003 A simple, fast, andaccurate algorithm to estimate large phylogenies bymaximum likelihood. Syst. Biol. 52, 696-704. (doi:10. 1080/10635150390235520)
128. Pond, S. L. K., Frost, S. D. W. & Muse, S. V.2005 HyPhy: hypothesis testing using phylogenies.Bioinformatics 21, 676-679. (doi:10.1093/bioinfor matics/bti079)
129. Presgraves, D. C., Baker, R. H. & Wilkinson, G. S. 1999 Coevolution of sperm and female reproductive tract mor-phology in stalk-eyed flies. Proc. R. Soc. Lond. B 266, 1041-1047. (doi:10.1098/rspb.1999.0741)
130. Swallow, J. G. & Wilkinson, G. S. 2002 The long andshort of sperm polymorphisms in insects. Biol. Rev.77, 153-182. (doi:10.1017/S1464793101005851)
131. Wedell, N., Gage, M. J. G. & Parker, G. A. 2002 Spermcompetition, male prudence and sperm-limited females. Trends Ecol. Evol. 17, 313-320. (doi:10.1016/S0169-5347(02)02533-8)
132. Byrne, P. G. & Rice, W. R. 2006 Evidence for adap-tive male mate choice in the fruit fly Drosophilamelanogaster. Proc. R. Soc. B 273, 917-922. (doi:10. 1098/rspb.2005.3372)
133. Edward, D. A. & Chapman, T. 2011 The evolution andsignificance of male mate choice. Trends Ecol. Evol. 26,647-654. (doi:10.1016/j.tree.2011.07.012)
134. Urban, F. 2006 Male perception of female matingstatus: its effect on copulation duration, sperm defenceand female fitness. Anim. Behav. 72, 1259-1268. (doi:10.1016/j.anbehav.2006.03.021)
135. Pitnick, S., Hosken, D. J. & Birkhead, T. R. 2009 Spermmorphological diversity. In Sperm biology: an evolutionaryperspective (ed. T. R. Birkhead, D. J. Hosken & S. Pitnick), pp. 69-149. San Diego, CA: Academic Press.
136. Pitnick, S., Markow, T. A. & Spicer, G. S. 1995 Delayed male maturity is a cost of producing large sperm in Drosophila. Proc. Natl Acad. Sci. USA 92, 10614-10618. (doi:10.1073/pnas.92.23.10614)
137. Bjork, A., Dallai, R. & Pitnick, S. 2007 Adaptive modu-lation of sperm production rate in Drosophila bifurca, a species with giant sperm. Biol. Lett. 3, 517-519. (doi:10.1098/rsbl.2007.0219)
138. Rogers, D. W., Grant, C. A., Chapman, T., Pomiankowski, A. & Fowler, K. 2006 The influenceof male and female eyespan on fertility in the stalkeyed fly, Cyrtodiopsis dalmanni. Anim. Behav. 72, 1363-1369. (doi:10.1016/j.anbehav.2006.03.027)
139. Rogers, D. W., Chapman, T., Fowler, K. & Pomian-kowski, A. 2005 Mating-induced reduction in accessory reproductive organ size in the stalk-eyed fly Cyrtodiopsis dalmanni. BMC Evol. Biol. 5, 37. (doi:10. 1186/1471-2148-5-37)
140. Baker, R. H., Ashwell, R. I. S., Richards, T. A., Fowler, K., Chapman, T. & Pomiankowski, A. 2001 Effectsof multiple mating and male eye span on female reproductive output in the stalk-eyed fly, Cyrtodiopsis dalmanni. Behav. Ecol. 12, 732-739. (doi:10.1093/beheco/12.6.732)
141. Cotton, S., Small, J. & Pomiankowski, A. 2010 Eyespan reflects reproductive quality in wild stalk-eyed flies. Evol. Ecol. 24, 83-95. (doi:10.1007/s10682-009-9292-6)
142. Harley, E., Fowler, K. & Cotton, S. 2010 No detectablefertility benefit from a single additional mating in wildstalk-eyed flies. PLoS ONE 5, e14309. (doi:10.1371/journal.pone.0014309)
143. Baker, R. H., Denniff, M., Futerman, P., Fowler, K., Pomiankowski, A. & Chapman, T. 2003 Accessorygland size influences time to sexual maturity and mating frequency in the stalk-eyed fly, Cyrtodiopsis dalmanni. Behav. Ecol. 14, 607-611. (doi:10.1093/beheco/arg053)
144. Al-khairulla, H., Warburton, D. & Knell, R. J. 2003 Do the eyestalks of female diopsid flies have a function inintrasexual aggressive encounters? J. Insect Behav. 16, 679-686. (doi:10.1023/B:JOIR.0000007703.84691.ad)
145. Worthington, A. M. & Swallow, J. G. 2010 Genderdifferences in survival and antipredatory behavior in stalk-eyed flies. Behav. Ecol. 21, 759-766. (doi:/10.1093/beheco/arq050)
146. Kosmidis, S., Botella, J. A., Mandilaras, K., Schneuwly, S., Skoulakis, E. M. C., Rouault, T. A. & Missirlis, F.2011 Ferritin overexpression in Drosophila glia leads toiron deposition in the optic lobes and late-onset behavioral defects. Neurobiol. Dis. 43, 213-219. (doi:10.1016/j.nbd. 2011.03.013)
147. Georgieva, T., Dunkov, B. C., Dimov, S., Ralchev, K. & Law, J. H. 2002 Drosophila melanogaster ferritin: cDNAencoding a light chain homologue, temporal and tissue specific expression of both subunit types. Insect Biochem. Mol. Biol. 32, 295-302. (doi:10.1016/S0965-1748(01)00090-X)
148. Baines, J. F., Sawyer, S. A., Hartl, D. L. & Parsch, J. 2008 Effects of X-linkage and sex-biased geneexpression on the rate of adaptive protein evolution in Drosophila. Mol. Biol. Evol. 25, 1639-1650. (doi:10. 1093/molbev/msn111)
149. Kaessmann, H. 2010 Origins, evolution, and phenotypic impact of new genes. Genome Res. 20, 1313-1326. (doi:10.1101/gr.101386.109)