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PLOS ONE  2014 

Transient and Permanent Experience with Fatty Acids Changes Drosophila melanogaster Preference and Fitness

DOI: 10.1371/journal.pone.0092352

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Food and host-preference relies on genetic adaptation and sensory experience. In vertebrates, experience with food-related cues during early development can change adult preference. This is also true in holometabolous insects, which undergo a drastic nervous system remodelling during their complete metamorphosis, but remains uncertain in Drosophila melanogaster. We have conditioned D. melanogaster with oleic (C18:1) and stearic (C18:0) acids, two common dietary fatty acids, respectively preferred by larvae and adult. Wild-type individuals exposed either during a transient period of development–from embryo to adult–or more permanently–during one to ten generation cycles–were affected by such conditioning. In particular, the oviposition preference of females exposed to each fatty acid during larval development was affected without cross-effect indicating the specificity of each substance. Permanent exposure to each fatty acid also drastically changed oviposition preference as well as major fitness traits (development duration, sex-ratio, fecundity, adult lethality). This suggests that D. melanogaster ability to adapt to new food sources is determined by its genetic and sensory plasticity both of which may explain the success of this generalist-diet species.


[1]  Cattin MF, Bersier LF, Banasek-Richter C, Baltensperger R, Gabriel JP (2004) Phylogenetic constraints and adaptation explain food-web structure. Nature 427: 835–839. doi: 10.1038/nature02327
[2]  Milo R, Hou JH, Springer M, Brenner MP, Kirschner MW (2007) The relationship between evolutionary and physiological variation in hemoglobin. Proceedings of the National Academy of Sciences of the United States of America 104: 16998–17003. doi: 10.1073/pnas.0707673104
[3]  Kent CF, Daskalchuk T, Cook L, Sokolowski MB, Greenspan RJ (2009) The Drosophila foraging gene mediates adult plasticity and Gene-Environment Interactions in behaviour, metabolites, and gene expression in response to food deprivation. PLoS Genet. 5(8): e1000609. doi: 10.1371/journal.pgen.1000609
[4]  Fricke C, Arnqvist G (2007) Rapid adaptation to a novel host in a seed beetle (Callosobruchus maculatus): the role of sexual selection. Evolution 61: 440–454. doi: 10.1111/j.1558-5646.2007.00038.x
[5]  Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, et al. (2007) Diet and the evolution of human amylase gene copy number variation. Nature Genetics 39: 1256–1260. doi: 10.1038/ng2123
[6]  Schaal B, Hummel T, Soussignan R (2004) Olfaction in the fetal and premature infant: functional status and clinical implications. Clinics in Perinatology 31: 261–+.
[7]  Glendinning JI (1994) Is the bitter rejection response always adaptive. Physiology & Behavior 56: 1217–1227. doi: 10.1016/0031-9384(94)90369-7
[8]  Phillips WM (1977) Modification of feeding ‘preference’ in the flea-beetle, Haltica lythri (Coleoptera, Chrysomelidae). Entomologia Experimentalis et Applicata 21: 71–80. doi: 10.1111/j.1570-7458.1977.tb02658.x
[9]  Akhtar Y, Isman MB (2003) Larval exposure to oviposition deterrents alters subsequent oviposition behavior in generalist, Trichoplusia ni and specialist, Plutella xylostella moths. Journal of Chemical Ecology 29: 1853–1870.
[10]  Blackiston DJ, Casey ES, Weiss MR (2008) Retention of memory through metamorphosis: can a moth remember what it learned as a caterpillar? PLoS One 3(3), e1736.
[11]  Alloway TM (1972) Learning and memory in insects. Annual Review of Entomology 17: 43–56. doi: 10.1146/annurev.en.17.010172.000355
[12]  Barron AB, Corbet SA (1999) Preimaginal conditioning in Drosophila revisited. Animal Behaviour 58: 621–628. doi: 10.1006/anbe.1999.1169
[13]  Burns JG, Svetec N, Rowe L, Mery F, Dolan MJ, et al. (2012) Gene-environment interplay in Drosophila melanogaster: Chronic food deprivation in early life affects adult exploratory and fitness traits. Proceedings of the National Academy of Sciences of the United States of America 109: 17239–17244. doi: 10.1073/pnas.1121265109
[14]  Hoffmann AA (1988) Early adult experience in Drosophila melanogaster. Journal of Insect Physiology 34: 197–204. doi: 10.1016/0022-1910(88)90050-9
[15]  Hirsch HVB, Barth M, Luo S, Sambaziotis H, Huber M, et al. (1995) Early visual experience affects mate choice of Drosophila melanogaster. Animal Behaviour 50: 1211–1217. doi: 10.1016/0003-3472(95)80038-7
[16]  Svetec N, Cobb M, Ferveur JF (2005) Chemical stimuli induce courtship dominance in Drosophila. Current Biology 15: R790–R792. doi: 10.1016/j.cub.2005.09.034
[17]  Hussein N, Fedorova I, Moriguchi T, Hamazaki K, Kim HY, et al. (2009) Artificial rearing of infant mice leads to n-3 fatty acid deficiency in cardiac, neural and peripheral tissues. Lipids 44: 685–702. doi: 10.1007/s11745-009-3318-2
[18]  Montmayeur J-P, Le Coutre J, editors (2010) Fat dectection: taste, texture, and post ingestive effects. Boca Raton, Florida (United States): CRC Press. 643 p.
[19]  Kris-Etherton PM, Harris WS, Appel LJ, Nutrition C (2002) Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106: 2747–2757. doi: 10.1161/01.cir.0000038493.65177.94
[20]  Rosenberg NA, Pritchard JK, Weber JL, Cann HM, Kidd KK, et al. (2002) Genetic structure of human populations. Science 298: 2381–2385. doi: 10.1126/science.1078311
[21]  Yach D, Stuckler D, Brownell KD (2006) Epidemiologic and economic consequences of the global epidemics of obesity and diabetes. Nature Medicine 12: 367–367. doi: 10.1038/nm0306-367a
[22]  Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, et al. (2008) Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. British Journal of Nutrition 100: 278–282. doi: 10.1017/s0007114507894438
[23]  Burdge GC, Slater-Jefferies J, Torrens C, Phillips ES, Hanson MA, et al. (2007) Dietary protein restriction of pregnant rats in the F-0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F-1 and F-2 generations. British Journal of Nutrition 97: 435–439. doi: 10.1017/s0007114507352392
[24]  Barrozo RB, Lazzari CR (2004) Orientation behaviour of the blood-sucking bug Triatoma infestans to short-chain fatty acids: synergistic effect of L-lactic acid and carbon dioxide. Chemical Senses 29: 833–841. doi: 10.1093/chemse/bjh249
[25]  Bosch OJ, Geier M, Boeckh J (2000) Contribution of fatty acids to olfactory host finding of female Aedes aegypti.. Chemical Senses 25: 323–330. doi: 10.1093/oxfordjournals.chemse.a014042
[26]  Smallegange RC, Qiu YT, Bukovinszkine-Kiss G, Van Loon JJ, Takken W (2009) The effect of aliphatic carboxylic acids on olfaction-based host-seeking of the malaria mosquito Anopheles gambiae sensu stricto. Journal of Chemical Ecology 35: 933–943. doi: 10.1007/s10886-009-9668-7
[27]  Mullens BA, Reifenrath WG, Butler SM (2009) Laboratory trials of fatty acids as repellents or antifeedants against houseflies, horn flies and stable flies (Diptera: Muscidae). Pest management science 65: 1360–1366. doi: 10.1002/ps.1823
[28]  Skinner WA, Tong HC, Maibach HI, Skidmore D (1970) Human skin-surface lipid fatty acids - Mosquito repellents. Experientia 26: 728–730. doi: 10.1007/bf02232510
[29]  Fougeron A, Farine J, Flaven-Pouchon J, Everaerts C, Ferveur J (2011) Fatty-acid preference changes during development in Drosophila melanogaster. PLoS ONE 6(10): e26899. doi: 10.1371/journal.pone.0026899
[30]  Ashburner M (1989) Drosophila: A Laboratory Handbook. USA: Cold Spring Harbor Edition. 1375 p.
[31]  Addinsoft (2012) XLSTAT 2012, Data analysis and statistics with Microsoft Excel. Paris, France.
[32]  Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47: 817–844.
[33]  Davis JM (2008) Patterns of variation in the influence of natal experience on habitat choice. Quarterly Review of Biology 83: 363–380. doi: 10.1086/592851
[34]  Lindstr?m J (1999) Early development and fitness in birds and mammals. Trends in Ecology & Evolution 14: 343–348. doi: 10.1016/s0169-5347(99)01639-0
[35]  Martel V, Schlyter F, Ignell R, Hansson BS, Anderson P (2011) Mosquito feeding affects larval behaviour and development in a moth. PLoS ONE 6: e25658. doi: 10.1371/journal.pone.0025658
[36]  Tremmel M, Muller C (2012) Insect personality depends on environmental conditions. Behavioral Ecology 24: 386–392. doi: 10.1093/beheco/ars175
[37]  Karowe DN (1989) Facultative monophagy as a consequence of prior feeding experience: behavioural and physiological specialisation in Colias philodice larvae. Oecologia 78: 106–111. doi: 10.1007/bf00377204
[38]  Gutierrez-Ibanez C, Villagra CA, Niemeyer HM (2007) Pre-pupation behaviour of the aphid parasitoid Aphidius ervi (Haliday) and its consequences for pre-imaginal learning. Die Naturwissenschaften 94: 595–600. doi: 10.1007/s00114-007-0233-3
[39]  Peralta Quesada PC, Schausberger P (2012) Prenatal chemosensory learning by the predatory mite Neoseiulus californicus. PLoS One 7: e53229. doi: 10.1371/journal.pone.0053229
[40]  Radziute S, Buda V (2013) Host feeding experience affects host plant odour preference of the polyphagous leafminer Liriomyza bryoniae. Entomologia Experimentalis et Applicata 146: 286–292. doi: 10.1111/eea.12028
[41]  Prokopy RJ, Averil AL, Cooley SS, Roitberg CA (1982) Associative learning in egg laying site selection by apple maggot flies. Science 218: 76–77. doi: 10.1126/science.218.4567.76
[42]  Shikano I, Isman MB (2009) A sensitive period for larval gustatory learning influences subsequent oviposition choice by the cabbage looper moth. Animal Behaviour 77: 247–251. doi: 10.1016/j.anbehav.2008.08.033
[43]  Anderson P, Sadek MM, Larsson M, Hansson BS, Th?ming G (2013) Larval host plant experience modulates both mate finding and oviposition choice in a moth. Animal Behaviour 85: 1169–1175. doi: 10.1016/j.anbehav.2013.03.002
[44]  Kruidhof HM, de Rijk M, Hoffmann D, Harvey JA, Vet LEM, et al. (2013) Effect of belowground herbivory on parasitoid associative learning of plant odours. Oikos 122: 1094–1100. doi: 10.1111/j.1600-0706.2012.00142.x
[45]  Colomb J, Grillenzoni N, Stocker RF, Ramaekers A (2007) Complex behavioural changes after odour exposure in Drosophila larvae. Animal Behaviour 73: 587–594. doi: 10.1016/j.anbehav.2006.04.016
[46]  Gerber B, Stocker RF (2007) The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chemical Senses 32: 65–89. doi: 10.1093/chemse/bjl030
[47]  Barron AB, Corbet SA (2000) Behavioural induction in Drosophila: timing and specificity Entomologia Experimentalis et Applicata. 94: 159–171. doi: 10.1046/j.1570-7458.2000.00616.x
[48]  Barron AB (2001) The Life and Death of Hopkins’ Host-Selection Principle. Journal of Insect Behaviour 14: 725–737.
[49]  Thorpe WH (1939) Further studies on pre-imaginal olfactory conditioning in insects. Proceedings of the Royal Society B 127: 424–433. doi: 10.1098/rspb.1939.0032
[50]  Hershberger WA, Smith MP (1967) Conditioning in Drosophila melanogaster. Animal Behaviour 15: 259–262. doi: 10.1016/0003-3472(67)90008-5
[51]  Manning A (1967) Pre-imaginal conditioning in Drosophila. Nature 216: 338–340. doi: 10.1038/216338a0
[52]  Jaenike J (1983) Induction of host preference in Drosophila melanogaster. Oecologia 58: 320–325. doi: 10.1007/bf00385230
[53]  Vet L (1983) Host-habitat location through olfactory cues by Leptopilina clavipes (Hartig) (Hym, Eucoilidae), a parasitoid of fungivorous Drosophila - the influence of conditioning. Netherlands Journal of Zoology 33: 225–248. doi: 10.1163/002829683x00101
[54]  Jaenike J (1982) Environmental modification of oviposition behavior in Drosophila. American Naturalist 119: 784–802. doi: 10.1086/283955
[55]  Jaenike J (1988) Effects of early adult experience on host selection in insects: some experimental and theoretical results. Journal of Insect Behaviour 1: 3–15. doi: 10.1007/bf01052500
[56]  Yang CH, Belawat P, Hafen E, Jan LY, Jan N (2008) Drosophila egg-laying site selection as a system to study simple decision-making processes. Science 319: 1679–1683. doi: 10.1126/science.1151842
[57]  Montel C (2009) A taste of the Drosophila gustatory receptor. Current Opinion in Neurobiology 19: 345–353. doi: 10.1016/j.conb.2009.07.001
[58]  Reaume CJ, Sokolowski MB (2006) The nature of Drosophila melanogaster. Current biology : CB 16: R623–628. doi: 10.1016/j.cub.2006.07.042
[59]  King-Jones K, Charles JP, Lam G, Thummel CS (2005) The ecdysone-induced DHR4 orphan nuclear receptor coordinates growth and maturation in Drosophila. Cell 121: 773–784. doi: 10.1016/j.cell.2005.03.030
[60]  Grishkevich V, Ben-Elazar S, Hashimshony T, Schott DH, Hunter CP, et al. (2012) A genomic bias for genotype-environment interactions in C. elegans. Molecular Systems Biology 8: 587. doi: 10.1038/msb.2012.19
[61]  Ingleby FC, Hosken DJ, Flowers K, Hawkes MF, Lane SM, et al. (2013) Genotype-by-environment interactions for cuticular hydrocarbon expression in Drosophila simulans. Journal of Evolutionary Biology 26: 94–107. doi: 10.1111/jeb.12030
[62]  Smith EN, Kruglyak L (2008) Gene-environment interaction in yeast gene expression. PLoS Biology 6: e83. doi: 10.1371/journal.pbio.0060083


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