Adaptive dynamics of cuticular hydrocarbons in Drosophila

Journal of Evolutionary Biology

Volumn 30, Issue 1, 2017, Pages 66-80

  Rajpurohit, S ^a   Hanus, R ^b   Vrkoslav, V ^b   Behrman, E L ^a   Bergland, A O ^c   Petrov, D ^d   Cvacka J ^b   Schmidt, P S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^c UNIVERSITY OF VIRGINIA   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

cuticular hydrocarbons; Drosophila; experimental evolution; spatiotemporal variation; thermal plasticity

Indexed keywords

ADAPTATION; ALLELE; BIOCHEMICAL COMPOSITION; CUTICLE; ENVIRONMENTAL STRESS; FLY; HYDROCARBON; LOCAL ADAPTATION; MATING BEHAVIOR; PHENOTYPIC PLASTICITY; SEASONAL VARIATION; SPATIOTEMPORAL ANALYSIS;

UNITED STATES;

ARTHROPODA; DROSOPHILA MELANOGASTER; MELANOGASTER;

HYDROCARBON;

ADAPTATION; ANIMAL; CHEMISTRY; CLIMATE; DROSOPHILA; DROSOPHILA MELANOGASTER;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CLIMATE; DROSOPHILA; DROSOPHILA MELANOGASTER; HYDROCARBONS;

EID: 85003741915     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12988     Document Type: Article

References (96)

1. Adrion, J.R., Hahn, M.W. & Cooper, B.S. 2015. Revisiting classic clines in Drosophila melanogaster in the age of genomics. Trends Genet. 31: 434–444.
2. Alves, H., Rouault, J.D., Kondoh, Y., Nakano, Y., Yamamoto, D., Kim, Y.K. et al. 2010. Evolution of cuticular hydrocarbons of Hawaiian Drosophilidae. Behav. Genet. 40: 694–705.
3. Barton, N.H. 1989. Evolutionary quantitative genetics: how little do we know? Annu. Rev. Genet. 23: 337–370.
4. Barton, N.H. 1999. Clines in polygenic traits. Genet. Res. 74: 223–236.
5. Behrman, E.L., Watson, S.S., O'Brien, K.R., Heschel, M.S. & Schmidt, P.S. 2015. Seasonal variation in life history traits in two Drosophila species. J. Evol. Biol. 28: 1691–1704.
6. Bergland, A.O., Behrman, E.L., O'Brien, K.R., Schmidt, P.S. & Petrov, D.A. 2014. Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLoS Genet. 10: e1004775.
7. Bergland, A.O., Tobler, R., Gonzalez, J., Schmidt, P. & Petrov, D. 2016. Secondary contact and local adaptation contribute to genome-wide patterns of clinal variation in Drosophila melanogaster. Mol. Ecol. 25: 1157–1174.
8. Blomquist, G.J. & Bagnères, A.G. 2010. Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology. Cambridge University Press, Cambridge.
9. Chapman, R.F. & Simpson, S. 2012. The Insects: Structure and Function. Cambridge University Press, Cambridge.
10. Chenoweth, S.F., Rundle, H.D. & Blows, M.W. 2008. Genetic constraints and the evolution of display trait sexual dimorphism by natural and sexual selection. Am. Nat. 171: 22–34.
11. Cogni, R., Kuczynski, C., Koury, S., Lavington, E., Behrman, E.L., O'Brien, K.R. et al. 2013. The intensity of selection acting on the couch potato gene spatial-temporal variation in a diapause cline. Evolution 68: 538–548.
12. Dembeck, L.M., Borocz, K. & Huang, W. 2015. Genetic architecture of natural variation in cuticular hydrocarbon composition in Drosophila melanogaster. Elife 4: e09861.
13. Edney, E.B. & Nagy, K.A. 1976. Water balance and excretion. In: Environmental physiology of animals (J. Bligh, J.L. Cloudsley-Thompson, A.G. Macdonald, eds), pp. 106–132. Blackwell, Oxford.
14. Etges, W.J. & de Oliveira, C.C. 2014. Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. X. Age-specific dynamics of adult epicuticular hydrocarbon expression in response to different host plants. Ecol. Evol. 4: 2033–2045.
15. Everaerts, C., Farine, J.P., Cobb, M. & Ferveur, J.F. 2010. Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PLoS One 5: e9607.
16. Fabian, D.K., Kapun, M., Nolte, V., Koflere, R., Schmidt, P.S., Schlotterer, C. et al. 2012. Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America. Mol. Ecol. 21: 4748–4769.
17. Fedina, T.Y., Kuo, T.H., Dreisewerd, K., Dierick, H.A., Yew, J.Y. & Pletcher, S.D. 2012. Dietary effects on cuticular hydrocarbons and sexual attractiveness in Drosophila. PLoS One 7: e49799.
18. Ferveur, J.F. 2005. Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav. Genet. 35: 279–295.
19. Foley, B., Chenoweth, S.F., Nuzhdin, S.V. & Blows, M.W. 2007. Natural genetic variation in cuticular hydrocarbon expression in male and female Drosophila melanogaster. Genetics 175: 1465-1477.
20. Frentiu, F.D. & Chenoweth, S.E. 2010. Clines in cuticular hydrocarbons in two Drosophila species with independent population histories. Evolution 64: 1784–1794.
21. Gershman, S., Delcourt, M. & Rundle, H.D. 2014. Sexual selection on Drosophila serrata male pheromones does not vary with female age or mating status. J. Evol. Biol. 27: 1279–1286.
22. Gibbs, A.G. 1998. Water-proofing properties of cuticular lipids. Am. Zool. 38: 471–482.
23. Gibbs, A.G. 2002a. Lipid melting and cuticular permeability: new insights into an old problem. J. Insect Physiol. 48: 391–400.
24. Gibbs, A.G. 2002b. Water balance in desert Drosophila: lessons from non-charismatic microfauna. Comp. Biochem. Physiol. 133: 781–789.
25. Gibbs, A. & Pomonis, J.G. 1995. Physical properties of insect cuticular hydrocarbons: model mixtures lipid interactions. Comp. Biochem. Physiol. 112B: 667–672.
26. Gibbs, A. & Rajpurohit, S. 2010. Cuticular lipids and water balance. In: Insect hydrocarbons: Biology, Biochemistry, and Chemical Ecology (G.J. Blomquist & A.G. Bagneres, eds), pp. 100–120. Cambridge University Press, Cambridge.
27. Gibbs, A.G., Chippindale, A.K. & Rose, M.R. 1997. Physiological mechanisms of evolved desiccation resistance in Drosophila melanogaster. J. Exp. Biol. 200: 1821–1832.
28. Gibbs, A.G., Louie, A.K. & Ayala, J.A. 1998. Effects of temperature on cuticular lipids and water balance in a desert Drosophila: is thermal acclimation beneficial? J. Exp. Biol. 201: 71–80.
29. Gilchrist, G.W., Jeffers, L.M., West, B., Folk, D.G., Suess, J. & Huey, R.B. 2008. Clinal patterns of desiccation and starvation resistance in ancestral and invading populations of Drosophila subobscura. Evol. Appl. 1: 513–523.
30. Grillet, M., Everaerts, C., Houot, B., Ritchie, M.G., Cobb, M. & Ferveur, J.-F. 2012. Incipient speciation in Drosophila melanogaster involves chemical signals. Sci. Rep. 2: 244.
31. Hadley, N.F. 1977. Epicuticular lipids of the desert tene-brionid beetle, Eleodes armata: seasonal and acclimatory effects on composition. Insect Biochem. 7: 277–283.
32. Hadley, N.F. 1994. Water Relations of Terrestrial Arthropods. Academic Press, San Diego, CA.
33. Hedrick, P.W., Ginevan, M.E. & Ewing, E.P. 1976. Genetic polymorphism in heterogeneous environments. Annu. Rev. Ecol. Evol. Syst. 7: 1–32.
34. Hercus, M.J. & Hoffmann, A.A. 2000. Maternal and grand-maternal age influence offspring fitness in Drosophila. Proc. Biol. Sci. 267: 2105–2110.
35. Hine, E., Chenoweth, S.F. & Blows, M.W. 2004. Multivariate quantitative genetics and the lek paradox: genetic variance in male sexually selected traits of Drosophila serrata under field conditions. Evolution 58: 2754–2762.
36. Hoffmann, A.A. & Harshman, L.G. 1999. Desiccation and starvation resistance in Drosophila: patterns of variation at the species, population and intrapopulation levels. Heredity 83: 637–643.
37. Hoffmann, A.A. & Weeks, A.R. 2007. Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia. Genetica 129: 133–147.
38. Hoffmann, A.A., Sgro, C.M. & Lawler, S.H. 1995. Ecological population genetics: the interface between genes and the environment. Annu. Rev. Genet. 29: 349–370.
39. Hoffmann, A.A., Scott, M., Partridge, L. & Hallas, R. 2003. Overwintering in Drosophila melanogaster: outdoor field cage experiments on clinal and laboratory selected populations help to elucidate traits under selection. J. Evol. Biol. 16: 614–623.
40. Hoffmann, A.A., Sgro, C.M. & Weeks, A.R. 2004. Chromosomal inversion polymorphisms and adaptation. Trends Ecol. Evol. 19: 482–488.
41. Hosken, D.J., Stockely, P., Tregenza, T. & Wedell, N. 2009. Monogamy and the battle of the sexes. Annu. Rev. Entomol. 54: 361–378.
42. Howard, R.W. 1993. Cuticular hydrocarbons and chemical communication. In: Insect Lipids: Chemistry, Biochemistry and Biology (D.W. Stanley-Samuelson & D.R. Nelson, eds), pp. 179–226. University of Nebraska Press, Lincoln, NE.
43. Howard, R.W. & Blomquist, G.J. 2005. Ecological, behavioral and biochemical aspects of insect hydrocarbons. Annu. Rev. Ecol. Evol. Syst. 50: 371–393.
44. Howard, R.W., Howard, C.D. & Colquhoun, S. 1995. Ontogenetic and environmentally induced changes in cuticular hydrocarbons of Oryzaephilus surinamensis (Coleoptera: Cucujidae). Ann. Entomol. Soc. Am. 88: 485–495.
45. Ives, P.T. 1970. Further genetic studies of the south Amherst population of Drosophila melanogaster. Evolution 24: 507–518.
46. Jallon, J.-M. 1984. A few chemical words exchanged by Drosophila during courtship and mating. Behav. Genet. 14: 441–478.
47. Jallon, J.-M. & David, J.R. 1987. Variation in cuticular hydrocarbons among the eight species of the Drosophila melanogaster subgroup. Evolution 41: 294–302.
48. Jallon, J., Kunesch, G., Bricard, L. & Pennanec'h, M. 1997. Incorporation of fatty acids into cuticular hydrocarbons of male and female Drosophila melanogaster. J. Insect. Physiol. 43: 1111-1116.
49. Kalra, B., Parkash, R. & Aggarwal, D.D. 2014. Divergent mechanisms for water conservation in Drosophila species. Entomol. Exp. Appl. 151: 43–56.
50. Karan, D., Dahiya, N., Munjal, A.K., Gibert, P., Moreteau, B., Parkash, R. et al. 1998. Desiccation and starvation tolerance of adult Drosophila: opposite latitudinal clines in natural populations of three different species. Evolution 52: 825–831.
51. Knibb, W.R. 1982. Chromosome inversion polymorphisms in Drosophila melanogaster II. Geographic clines and climatic associations in Australasia, North America and Asia. Genetica 58: 213–221.
52. Kolaczkowski, B., Kern, A.D., Holloway, A.K. & Begun, D.J. 2011. Genomic differentiation between temperate and tropical Australian populations of Drosophila melanogaster. Genetics 187: 245–260.
53. Kuo, T.H., Fedina, T.Y., Hansen, I., Dreisewerd, K., Dierick, H.A., Yew, J.Y. et al. 2012. Insulin signaling mediates sexual attractiveness in Drosophila. PLoS Genet. 8: e1002684.
54. Kwan, L. & Rundle, H.D. 2009. Adaptation to desiccation fails to generate pre- and postmating isolation in replicate Drosophila melanogaster laboratory populations. Evolution 64: 710–723.
55. Lavington, E., Cogni, R., Kuczynski, K., Koury, S., Behrman, E.L., O'Brien, K.R. et al. 2014. A small system—high resolution study of metabolic adaptation in the central metabolic pathway to temperate climates in Drosophila melanogaster. Mol. Biol. Evol. 31: 2032–2041.
56. Liimatainen, J.O. & Jallon, J.M. 2007. Genetic analysis of cuticular hydrocarbons and their effect on courtship in Drosophila virilis and D. lummei. Behav. Genet. 37: 713–725.
57. Lockey, K.H. 1988. Lipids of the insect cuticle: origin, composition and function. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 89: 595–645.
58. McColl, G. & McKechnie, S.W. 1999. The Drosophila heat shock hsr-omega gene: an allele frequency cline detected by quantitative PCR. Mol. Biol. Evol. 16: 1568–1574.
59. Nelson, D.R. & Lee, R.E. 2004. Cuticular lipids and desiccation resistance in overwintering larvae of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephirtidae). Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 138: 313–320.
60. Ohtsu, T., Kimura, M.T. & Katagiri, C. 1988. How Drosophila species acquire cold tolerance qualitative changes of phospholipids. Eur. J. Biochem. 252: 608–611.
61. Paaby, A.B., Blacket, M.J., Hoffmann, A.A. & Schmidt, P.S. 2010. Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents. Mol. Ecol. 19: 760–774.
62. Pardy, J.A. 2012. The genetic basis of cuticular hydrocarbon production in Drosophila melanogaster and D. simulans. Electronic Thesis and Dissertation Repository. http://ir.lib.uwo.ca/etd/832.
63. Parkash, R. 2010. Testing the melanism-desiccation hypothesis: a case study in Darwinian evolution. In: Nature at Work: Ongoing Saga of Evolution (V.P. Sharma, ed.), pp. 279–306. Springer, India.
64. Parkash, R. & Ranga, P. 2013. Divergence for tolerance to thermal-stress related traits in two Drosophila species of immigrans group. J. Therm. Biol 38: 396–406.
65. Parkash, R., Kalra, B. & Sharma, V. 2008. Changes in cuticular lipids, water loss and desiccation resistance in a tropical drosophilids: analysis of within population variation. Fly (Austin) 2: 189–197.
66. Parkash, R., Sharma, V. & Kalra, B. 2009. Impact of body melanization on desiccation resistance in montane populations of D. melanogaster. Analysis of seasonal variation. J. Insect Physiol. 10: 898–908.
67. Parkash, R., Sharma, V. & Kalra, B. 2010. Sexual dimorphism for water balance mechanisms in montane populations of Drosophila kikkawai. Biol. Lett. 6: 570–574.
68. Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A.R., Bender, D. et al. 2007. PLINK: a toolset for whole-genome association and population-based linkage analysis. Am. J. Hum. Genet. 81: 559–575.
69. R Core Team. 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
70. Rajpurohit, S. & Nedved, O. 2013. Clinal variation in fitness related traits in tropical drosophilids of the Indian subcontinent. J. Therm. Biol 38: 345–354.
71. Rajpurohit, S., Nedved, O. & Gibbs, A.G. 2013. Meta-analysis of geographical clines in desiccation tolerance of Indian drosophilids. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 164: 391–398.
72. Roff, D.A. 2002. Life History Evolution, Vol. 7. Sinauer Associates, Sunderland.
73. Romer, F. 1991. The oenocytes of insects: differentiation, changes during molting, and their possible involvement in the secretion of moulting hormone. In: Morphogenetic Hormones of Arthropods (A.P. Gupta, ed.), pp. 542–566. Rutgers University Press, New Brunswick, NJ.
74. Rouault, J.-D., Capy, P. & Jallon, J.M. 2000. Variations of male cuticular hydrocarbons with geoclimatic variables: an adaptive mechanism in Drosophila melanogaster? Genetica 110: 117–130.
75. Rouault, J.D., Marican, C., Wicker-Thomas, C. & Jallon, J.M. 2004. Relations between cuticular hydrocarbon (HC) polymorphism, resistance against desiccation and breeding temperature; a model for HC evolution in D. melanogaster and D. simulans. Genetica 120: 195–212.
76. Rourke, B.C. 2000. Geographic and altitudinal variation in water balance and metabolic rate in a California grasshopper, Melanopus sanguinipes. J. Exp. Biol. 203: 2699–2712.
77. Savolainen, O., Lascoux, O.M. & Merilä, J. 2013. Ecological genomics of local adaptation. Nat. Rev. Genet. 14: 807–820.
78. Schal, C., Sevala, V.L., Young, H.P. & Bachmann, J.A.S. 1998. Sites of synthesis and transport pathways of insect hydrocarbons: cuticle and ovary as target tissues. Am. Zool. 38: 382–393.
79. Schmidt, P.S. & Conde, D.R. 2006. Environmental heterogeneity and the maintenance of genetic variation for reproductive diapause in Drosophila melanogaster. Evolution 60: 1602–1611.
80. Schmidt, P.S. & Paaby, A.B. 2008. Reproductive diapause and life history clines in North American populations of Drosophila melanogaster. Evolution 62: 1204–1215.
81. Schmidt, P.S., Matzkin, L.M., Ippolito, M. & Eanes, W.F. 2005. Geographic variation in diapause incidence, life history traits and climatic adaptation in Drosophila melanogaster. Evolution 59: 1721–1732.
82. Sezgin, E., Duvernell, D.D., Matzkin, L.M., Duan, Y.H., Zhu, C.T., Verrelli, B.C. et al. 2004. Single-locus latitudinal clines and their relationship to temperate adaptation in metabolic genes and derived alleles in Drosophila melanogaster. Genetics 168: 923–931.
83. Sharma, M.D., Mitchell, C., Hunt, J., Tregenza, T. & Hosken, D.J. 2012. The genetics of cuticular hydrocarbon profiles in the fruit fly Drosophila simulans. J. Hered. 103: 230–239.
84. Šmilauer, P. & Lepš, J. 2014. Multivariate Analysis of Ecological Data using Canoco5. Cambridge University Press, Cambridge.
85. Stearns, S.C. 1992. The Evolution of Life Histories. Oxford University Press, London.
86. Takahashi, A., Fujiwara-Tsujii, N., Yamaoka, R., Itoh, M., Ozaki, M. & Takano-Shimizu, T. 2012. Cuticular hydrocarbon content that affects male mate preference of Drosophila melanogaster from West Africa. Int. J. Evol. Biol. 2012: 1–10.
87. Toolson, E.C. 1982. Effects of rearing temperature on cuticle permeability and epicuticular lipid composition in Drosophila pseudoobscura. J. Exp. Zool. 222: 249–253.
88. Toolson, E.C. & Hadley, N.F. 1979. Seasonal effects on cuticular permeability and epicuticular lipid composition in Centruroides sculpturatus Ewing 1928 (Scorpiones: Buthidae). J. Comp. Physiol. B. 129: 319–325.
89. Toolson, E.V. & Kuper-Simbron, R. 1989. Laboratory Evolution of epicuticular hydrocarbon composition and cuticular permeability in Drosophila pseudoobscura: effects on sexual dimorphism and thermal acclimation ability. Evolution 43: 468–473.
90. Turchin, M.C., Chiang, C.W.K., Palmer, C.D., Sankararaman, S., Reich, D., GIANT Consortium, Hirschhorn, J.N. 2012. Evidence of widespread selection on standing variation in Europe at height-associated SNPs. Nat. Genet. 44: 1015–1019.
91. Venard, R. & Jallon, J.-M. 1980. Evidence for an aphrodisiac pheromone of female Drosophila. Experientia 36: 211–213.
92. Wicker-Thomas, C. 2007. Pheromonal communication involved in courtship behavior in Diptera. J. Insect Physiol. 53: 1089–1100.
93. Wicker-Thomas, C., Garrido, D., Bontonou, G., Napal, L., Mazuras, N., Denis, B., et al. 2015. Flexible origin of hydrocarbon/pheromone precursors in Drosophila melanogaster. J. Lipid. Res. 56: 2094-2101.
94. Wigglesworth, V.B. 1948. The insect cuticle. Biol. Rev. 23: 408–445.
95. Yeaman, S. & Jarvis, A. 2006. Regional heterogeneity and gene flow maintain variance in a quantitative trait within populations of lodgepole pine. Proc. Biol. Sci. 273: 1587–1593.
96. Zhao, X., Bergland, A.O., Behrman, E.L., Gregory, B.D., Petrov, D.A. & Schmidt, P.S. 2015. Global transcriptional profiling of diapause and climatic adaptation in Drosophila melanogaster. Mol. Biol. Evol. 33: 707-720.