Genetic architecture of natural variation in cuticular hydrocarbon composition in Drosophila melanogaster

eLife

Volumn 4, Issue NOVEMBER2015, 2015, Pages

  Dembeck, Lauren M ^a,b   Böröczky, Katalin ^a,c   Huang, Wen ^a   Schal, Coby ^a   Anholt, Robert R H ^a   Mackay, Trudy F C ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CUTICULAR HYDROCARBON; FAT; UNCLASSIFIED DRUG; HYDROCARBON;

ARTICLE; DROSOPHILA MELANOGASTER; FATTY ACID METABOLISM; FEMALE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; MALE; NONHUMAN; PHENOTYPE; AFRICA; ANIMAL; CARIBBEAN; CHEMISTRY; GENE INACTIVATION; GENETICS; INTEGUMENTARY SYSTEM; METABOLISM;

AFRICA; ANIMALS; CARIBBEAN REGION; DROSOPHILA MELANOGASTER; FEMALE; GENE KNOCKOUT TECHNIQUES; HYDROCARBONS; INTEGUMENTARY SYSTEM; MALE; METABOLIC NETWORKS AND PATHWAYS;

EID: 84955281489     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.09861.001     Document Type: Article

References (63)

1. Antony C, Jallon J-M. 1982. The chemical basis for sex recognition in Drosophila melanogaster. Journal of Insect Physiology 28:873-880. doi: 10.1016/0022-1910(82)90101-9
2. Arienti M, Antony C, Wicker-Thomas C, Delbecque JP, Jallon JM. 2010. Ontogeny of Drosophila melanogaster female sex-appeal and cuticular hydrocarbons. Integrative Zoology 5:272-282. doi: 10.1111/j.1749-4877.2010. 00213.x
3. Billeter JC, Atallah J, Krupp JJ, Millar JG, Levine JD. 2009. Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461:987-991. doi: 10.1038/nature08495
4. Blomquist GJ, Bagnères A-G. (eds) 2010. Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology. Cambridge:Cambridge University Press. doi: 10.1017/CBO9780511711909
5. Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC, Goodman MM, Harjes C, Guill K, Kroon DE, Larsson S, Lepak NK, Li H, Mitchell SE, Pressoir G, Peiffer JA, Rosas MO, Rocheford TR, Romay MC, Romero S, Salvo S, Sanchez Villeda H, da Silva HS, Sun Q, Tian F, Upadyayula N, Ware D, Yates H, Yu J, Zhang Z, Kresovich S, McMullen MD. 2009. The genetic architecture of maize flowering time. Science 325:714-718. doi: 10.1126/science.1174276
6. Böröczky K, Wada-Katsumata A, Batchelor D, Zhukovskaya M, Schal C. 2013. Insects groom their antennae to enhance olfactory acuity. Proceedings of the National Academy of Sciences of the United States of America 110:3615-3620. doi: 10.1073/pnas.1212466110
7. Chan EK, Rowe HC, Corwin JA, Joseph B, Kliebenstein DJ. 2011. Combining genome-wide association mapping and transcriptional networks to identify novel genes controlling glucosinolates in Arabidopsis thaliana. PLoS Biology 9:e1001125 doi: 10.1371/journal.pbio.1001125
8. Cheng JB, Russell DW. 2004. Mammalian wax biosynthesis. i. identification of two fatty acyl-coenzyme a reductases with different substrate specificities and tissue distributions. The Journal of Biological Chemistry 279:37789-37797. doi: 10.1074/jbc.M406225200
9. Chertemps T, Duportets L, Labeur C, Ueyama M, Wicker-Thomas C. 2006. A female-specific desaturase gene responsible for diene hydrocarbon biosynthesis and courtship behaviour in Drosophila melanogaster. Insect Molecular Biology 15:465-473. doi: 10.1111/j.1365-2583.2006.00658.x
10. Chertemps T, Duportets L, Labeur C, Ueda R, Takahashi K, Saigo K, Wicker-Thomas C. 2007. A female-biased expressed elongase involved in long-chain hydrocarbon biosynthesis and courtship behavior in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America 104:4273-4278. doi: 10.1073/pnas.0608142104
11. Chung H, Loehlin DW, Dufour HD, Vaccarro K, Millar JG, Carroll SB. 2014. A single gene affects both ecological divergence and mate choice in Drosophila. Science 343:1148-1151. doi: 10.1126/science.1249998
12. Chung H, Sztal T, Pasricha S, Sridhar M, Batterham P, Daborn PJ. 2009. Characterization of Drosophila melanogaster cytochrome P450 genes. Proceedings of the National Academy of Sciences of the United States of America 106:5731-5736. doi: 10.1073/pnas.0812141106
13. Cobb M, Jallon J-M. 1990. Pheromones, mate recognition and courtship stimulation in the Drosophila melanogaster species sub-group. Animal Behaviour 39:1058-1067. doi: 10.1016/S0003-3472(05)80778-X
14. Coyne JA, Wicker-Thomas C, Jallon JM. 1999. A gene responsible for a cuticular hydrocarbon polymorphism in Drosophila melanogaster. Genetical Research 73:189-203. doi: 10.1017/S0016672398003723
15. Coyne JA, Elwyn S. 2006. Does the Desaturase-2 locus in Drosophila melanogaster cause adaptation and sexual isolation? Evolution; International Journal of Organic Evolution 60:279-291. doi: 10.1111/j.0014-3820.2006. tb01106.x
16. Dallerac R, Labeur C, Jallon JM, Knipple DC, Roelofs WL, Wicker-Thomas C. 2000. A delta 9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America 97:9449-9454. doi: 10.1073/pnas.150243997
17. Dembeck LM, Huang W, Magwire MM, Lawrence F, Lyman RF, Mackay TF. 2015. Genetic architecture of abdominal pigmentation in Drosophila melanogaster. PLoS Genetics 11:e1005163 doi: 10.1371/journal.pgen. 1005163
18. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, Couto A, Marra V, Keleman K, Dickson BJ. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151-156. doi: 10.1038/nature05954
19. Dweck HK, Ebrahim SA, Thoma M, Mohamed AA, Keesey IW, Trona F, Lavista-Llanos S, SvatošA, Sachse S, Knaden M, Hansson BS. 2015. Pheromones mediating copulation and attraction in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 112: E2829-E2835. doi: 10.1073/pnas. 1504527112
20. Everaerts C, Farine JP, Cobb M, Ferveur JF. 2010. Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PloS One 5:e9607 doi: 10.1371/journal.pone.0009607
21. Fabian DK, Kapun M, Nolte V, Kofler R, Schmidt PS, Schlötterer C, Flatt T. 2012. Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America. Molecular Ecology 21:4748-4769. doi: 10.1111/j.1365-294X.2012.05731.x
22. Fang S, Takahashi A, Wu CI. 2002. A mutation in the promoter of Desaturase 2 is correlated with sexual isolation between Drosophila behavioral races. Genetics 162:781-784.
23. Fang S, Ting CT, Lee CR, Chu KH, Wang CC, Tsaur SC. 2009. Molecular evolution and functional diversification of fatty acid desaturases after recurrent gene duplication in Drosophila. Molecular Biology and Evolution 26: 1447-1456. doi: 10.1093/molbev/msp057
24. Ferveur J-F, Jallon J-M. 1993. Nerd, a locus on chromosome III, affects male reproductive behavior in Drosophila melanogaster. Naturwissenschaften 80:474-475. doi: 10.1007/BF01136042
25. Ferveur J-F, Jallon J-M. 1996. Genetic control of male cuticular hydrocarbons in Drosophila melanogaster. Genetical Research 67:211-218. doi: 10.1017/S0016672300033693
26. Ferveur JF. 2005. Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behavior Genetics 35:279-295. doi: 10.1007/s10519-005-3220-5
27. Foley B, Chenoweth SF, Nuzhdin SV, Blows MW. 2007. Natural genetic variation in cuticular hydrocarbon expression in male and female Drosophila melanogaster. Genetics 175:1465-1477. doi: 10.1534/genetics.106. 065771
28. Gibbs AG. 1998. Water-proofing properties of cuticular lipids. American Zoologist 38:471-482. doi: 10.1093/icb/ 38.3.471
29. Gibbs AG. 2002. Lipid melting and cuticular permeability: new insights into an old problem. Journal of Insect Physiology 48:391-400. doi: 10.1016/S0022-1910(02)00059-8
30. Gleason JM, Jallon JM, Rouault JD, Ritchie MG. 2005. Quantitative trait loci for cuticular hydrocarbons associated with sexual isolation between Drosophila simulans and D. sechellia. Genetics 171:1789-1798. doi: 10.1534/genetics.104.037937
31. Greenberg AJ, Moran JR, Coyne JA, Wu CI. 2003. Ecological adaptation during incipient speciation revealed by precise gene replacement. Science 302:1754-1757. doi: 10.1126/science.1090432
32. Grillet M, Everaerts C, Houot B, Ritchie MG, Cobb M, Ferveur JF. 2012. Incipient speciation in Drosophila melanogaster involves chemical signals. Scientific Reports 2:224 doi: 10.1038/srep00224
33. Howard RW, Jackson LL, Banse H, Blows MW. 2003. Cuticular hydrocarbons of Drosophila birchii and D. serrata: identification and role in mate choice in D. serrata. Journal of Chemical Ecology 29:961-976. doi: 10.1023/A: 1022992002239
34. Howard RW, Blomquist GJ. 2005. Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annual Review of Entomology 50:371-393. doi: 10.1146/annurev.ento.50.071803.130359
35. Huang W, Massouras A, Inoue Y, Peiffer J, Ràmia M, Tarone AM, Turlapati L, Zichner T, Zhu D, Lyman RF, Magwire MM, Blankenburg K, Carbone MA, Chang K, Ellis LL, Fernandez S, Han Y, Highnam G, Hjelmen CE, Jack JR, Javaid M, Jayaseelan J, Kalra D, Lee S, Lewis L, Munidasa M, Ongeri F, Patel S, Perales L, Perez A, Pu L, Rollmann SM, Ruth R, Saada N, Warner C, Williams A, Wu YQ, Yamamoto A, Zhang Y, Zhu Y, Anholt RR, Korbel JO, Mittelman D, Muzny DM, Gibbs RA, Barbadilla A, Johnston JS, Stone EA, Richards S, Deplancke B Mackay TF. 2014. Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines. Genome Research 24:1193-1208. doi: 10.1101/gr.171546.113
36. Ishii K, Hirai Y, Katagiri C, Kimura MT. 2001. Sexual isolation and cuticular hydrocarbons in Drosophila elegans. Heredity 87:392-399. doi: 10.1046/j.1365-2540.2001.00864.x
37. Jallon J-M. 1984. A few chemical words exchanged by Drosophila during courtship and mating. Behavior Genetics 14:441-478. doi: 10.1007/BF01065444
38. Jallon J-M, David JR. 1987. Variation in cuticular hydrocarbons among the eight species of the Drosophila melanogaster subgroup. Evolution 41:294-302. doi: 10.2307/2409139
39. Pennanec'h M, Bricard L, Kunesch G, Jallon J-M, Bricard L, Pennanec'h M. 1997. Incorporation of fatty acids into cuticular hydrocarbons of male and female Drosophila melanogaster. Journal of Insect Physiology 43:1111-1116. doi: 10.1016/S0022-1910(97)00082-6
40. Kawano T, Shimoda M, Matsumoto H, Ryuda M, Tsuzuki S, Hayakawa Y. 2010. Identification of a gene, Desiccate, contributing to desiccation resistance in Drosophila melanogaster. The Journal of Biological Chemistry 285:38889-38897. doi: 10.1074/jbc.M110.168864
41. Labeur C, Dallerac R, Wicker-Thomas C. 2002. Involvement of Desat1 gene in the control of Drosophila melanogaster pheromone biosynthesis. Genetica 114:269-274. doi: 10.1023/A:1016223000650
42. Lippert C, Listgarten J, Liu Y, Kadie CM, Davidson RI, Heckerman D. 2011. FaST linear mixed models for genome-wide association studies. Nature Methods 8:833-835. doi: 10.1038/nmeth.1681
43. Mackay TF, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, Casillas S, Han Y, Magwire MM, Cridland JM, Richardson MF, Anholt RR, Barrón M, Bess C, Blankenburg KP, Carbone MA, Castellano D, Chaboub L, Duncan L, Harris Z, Javaid M, Jayaseelan JC, Jhangiani SN, Jordan KW, Lara F, Lawrence F, Lee SL, Librado P, Linheiro RS, Lyman RF, Mackey AJ, Munidasa M, Muzny DM, Nazareth L, Newsham I, Perales L, Pu LL, Qu C, Rà mia M, Reid JG, Rollmann SM, Rozas J, Saada N, Turlapati L, Worley KC, Wu YQ, Yamamoto A, Zhu Y, Bergman CM, Thornton KR, Mittelman D, Gibbs RA. 2012. The Drosophila melanogaster Genetic Reference Panel. Nature 482:173-178. doi: 10.1038/nature10811
44. Marcillac F, Bousquet F, Alabouvette J, Savarit F, Ferveur JF. 2005. A mutation with major effects on Drosophila melanogaster sex pheromones. Genetics 171:1617-1628. doi: 10.1534/genetics.104.033159
45. Martin SJ, Drijfhout FP. 2009. How reliable is the analysis of complex cuticular hydrocarbon profiles by multivariate statistical methods? Journal of Chemical Ecology 35:375-382. doi: 10.1007/s10886-009-9610-z
46. Noor MAF, Coyne JA. 1996. Genetics of a difference in cuticular hydrocarbons between Drosophila pseudoobscura and D. persimilis. Genetical Research 68:117-123. doi: 10.1017/S0016672300034005
47. Qiu Y, Tittiger C, Wicker-Thomas C, Le Goff G, Young S, Wajnberg E, Fricaux T, Taquet N, Blomquist GJ, Feyereisen R. 2012. An insect-specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis. Proceedings of the National Academy of Sciences of the United States of America 109:14858-14863. doi: 10. 1073/pnas.1208650109
48. Richard F-J, Hunt JH. 2013. Intracolony chemical communication in social insects. Insectes Sociaux 60:275-291. doi: 10.1007/s00040-013-0306-6
49. Romer F. 1991. The oenocytes of insects: Differentiation, changes during molting, and their possible involvement in the secretion of moulting hormone. In: Gupta A. P (ed) Morphogenetic Hormones of Arthropods. New Brunswick, New Jersey: Rutgers University Press
50. Rundle HD, Chenoweth SF, Doughty P, Blows MW. 2005. Divergent selection and the evolution of signal traits and mating preferences. PLoS Biology 3:e368 doi: 10.1371/journal.pbio.0030368
51. Schal C, Sevala VL, Young HP, Bachmann JAS. 1998. Sites of synthesis and transport pathways of insect hydrocarbons: cuticle and ovary as target tissues. American Zoologist 38:382-393. doi: 10.1093/icb/38.2.382
52. St Pierre SE, Ponting L, Stefancsik R, McQuilton P. FlyBase ConsortiumFlyBase Consortium. 2014. FlyBase 102- advanced approaches to interrogating FlyBase. Nucleic Acids Research 42:D780-788. doi: 10.1093/nar/ gkt1092
53. Stanley-Samuelson DW, Nelson DR. (eds) 1993. Insect Lipids: Chemistry, Biochemistry, and Biology. Lincoln, Nebraska:University of Nebraska Press.
54. Stone EA, Ayroles JF. 2009. Modulated modularity clustering as an exploratory tool for functional genomic inference. PLoS Genetics 5:e1000479 doi: 10.1371/journal.pgen.1000479
55. Takahashi A, Tsaur SC, Coyne JA, Wu CI. 2001. The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America 98:3920-3925. doi: 10.1073/pnas.061465098
56. Takahashi A, Ting C-T. 2004. Genetic basis of sexual isolation in Drosophila melanogaster. Genetica 120:273-284. doi: 10.1023/B:GENE.0000017649.51782.5b
57. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA, Singh CM, Buchholz R, Demsky M, Fawcett R, Francis-Lang HL, Ryner L, Cheung LM, Chong A, Erickson C, Fisher WW, Greer K, Hartouni SR, Howie E, Jakkula L, Joo D, Killpack K, Laufer A, Mazzotta J, Smith RD, Stevens LM, Stuber C, Tan LR, Ventura R, Woo A, Zakrajsek I, Zhao L, Chen F, Swimmer C, Kopczynski C, Duyk G, Winberg ML, Margolis J. 2004. A complementary transposon tool kit for Drosophila melanogaster using P and PiggyBac. Nature Genetics 36: 283-287. doi: 10.1038/ng1314
58. Venard R, Jallon J-M. 1980. Evidence for an aphrodisiac pheromone of female Drosophila. Experientia 36:211-213. doi: 10.1007/BF01953737
59. Wicker-Thomas C, Henriet C, Dallerac R. 1997. Partial characterization of a fatty acid desaturase gene in Drosophila melanogaster. Insect Biochemistry and Molecular Biology 27:963-972. doi: 10.1016/S0965-1748(97) 00077-5
60. Wicker-Thomas C, Chertemps T. 2010. Molecular biology and genetics of hydrocarbon production In: Bloomquist G.J, Bagneres A.-G (eds) Insect Hydrocarbons: Biology, Biochemistry and Chemical Ecology. 1st ed. Cambridge:Cambridge University Press.
61. Wicker-Thomas C, Garrido D, Bontonou G, Napal L, Mazuras N, Denis B, Rubin T, Parvy JP, Montagne J. 2015. Flexible origin of hydrocarbon/pheromone precursors in Drosophila melanogaster. Journal of Lipid Research 56:2094-2101. doi: 10.1194/jlr.M060368
62. Yang J, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR, Madden PA, Heath AC, Martin NG, Montgomery GW, Goddard ME, Visscher PM. 2010. Common SNPs explain a large proportion of the heritability for human height. Nature Genetics 42:565-569. doi: 10.1038/ng.608
63. Yukilevich R, True JR. 2008. African morphology, behavior and phermones underlie incipient sexual isolation between US and Caribbean Drosophila melanogaster. Evolution; International Journal of Organic Evolution 62: 2807-2828. doi: 10.1111/j.1558-5646.2008.00488.x