Insulin Signaling Mediates Sexual Attractiveness in

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Sexually attractive characteristics are often thought to reflect an individual's condition or reproductive potential, but the underlying molecular mechanisms through which they do so are generally unknown. Insulin/insulin-like growth factor signaling (IIS) is known to modulate aging, reproduction, and stress resistance in several species and to contribute to variability of these traits in natural populations. Here we show that IIS determines sexual attractiveness in Drosophila through transcriptional regulation of genes involved in the production of cuticular hydrocarbons (CHC), many of which function as pheromones. Using traditional gas chromatography/mass spectrometry (GC/MS) together with newly introduced laser desorption/ionization orthogonal time-of-flight mass spectrometry (LDI-MS) we establish that CHC profiles are significantly affected by genetic manipulations that target IIS. Manipulations that reduce IIS also reduce attractiveness, while females with increased IIS are significantly more attractive than wild-type animals. IIS effects on attractiveness are mediated by changes in CHC profiles. Insulin signaling influences CHC through pathways that are likely independent of dFOXO and that may involve the nutrient-sensing Target of Rapamycin (TOR) pathway. These results suggest that the activity of conserved molecular regulators of longevity and reproductive output may manifest in different species as external characteristics that are perceived as honest indicators of fitness potential.

Vyšlo v časopise: Insulin Signaling Mediates Sexual Attractiveness in. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002684
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002684

Souhrn

Zdroje

1. ZahaviA 1975 Mate selection-a selection for a handicap. J Theor Biol 53 205 214

2. Maynard-SmithJHarperD 2003 Animal Signals Oxford Oxford University Press

3. AnderssonM 1994 Sexual Selection Oxford Oxford University Press

4. SearcyWANowickiS 2005 The Evolution of Animal Communication: Reliability and Deception in Signaling Systems Princeton, N. J. Princeton University Press

5. HillGE 2011 Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol Lett 14 625 634

6. FerveurJF 2005 Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 35 279 295

7. GibbsAG 2002 Lipid melting and cuticular permeability: new insights into an old problem. J Insect Physiol 48 391 400

8. HowardRWBlomquistGJ 2005 Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50 371 393

9. CoyneJAOyamaR 1995 Localization of pheromonal sexual dimorphism in Drosophila melanogaster and its effect on sexual isolation. Proc Natl Acad Sci U S A 92 9505 9509

10. FerveurJFSavaritFO'KaneCJSureauGGreenspanRJ 1997 Genetic feminization of pheromones and its behavioral consequences in Drosophila males. Science 276 1555 1558

11. WickerCJallonJM 1995 Hormonal control of sex pheromone biosynthesis in Drosophila melanogaster. Journal of Insect Physiology 41 65 70

12. ChertempsTDuportetsLLabeurCUeyamaMWicker-ThomasC 2006 A female-specific desaturase gene responsible for diene hydrocarbon biosynthesis and courtship behaviour in Drosophila melanogaster. Insect Mol Biol 15 465 473

13. ChertempsTDuportetsLLabeurCUedaRTakahashiK 2007 A female-biased expressed elongase involved in long-chain hydrocarbon biosynthesis and courtship behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 104 4273 4278

14. MarcillacFBousquetFAlabouvetteJSavaritFFerveurJF 2005 A mutation with major effects on Drosophila melanogaster sex pheromones. Genetics 171 1617 1628

15. DalleracRLabeurCJallonJMKnippleDCRoelofsWL 2000 A delta 9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proc Natl Acad Sci U S A 97 9449 9454

16. WuQBrownMR 2006 Signaling and function of insulin-like peptides in insects. Annu Rev Entomol 51 1 24

17. TatarMBartkeAAntebiA 2003 The endocrine regulation of aging by insulin-like signals. Science 299 1346 1351

18. ToivonenJMPartridgeL 2009 Endocrine regulation of aging and reproduction in Drosophila. Mol Cell Endocrinol 299 39 50

19. MukhopadhyayATissenbaumHA 2007 Reproduction and longevity: secrets revealed by C. elegans. Trends Cell Biol 17 65 71

20. HyunJHashimotoC 2011 Physiological effects of manipulating the level of insulin-degrading enzyme in insulin-producing cells of Drosophila. Fly (Austin) 5 53 57

21. JenkinsNLMcCollGLithgowGJ 2004 Fitness cost of extended lifespan in Caenorhabditis elegans. Proc Biol Sci 271 2523 2526

22. NuzhdinSVBrissonJAPickeringAWayneMLHarshmanLG 2009 Natural genetic variation in transcriptome reflects network structure inferred with major effect mutations: insulin/TOR and associated phenotypes in Drosophila melanogaster. BMC Genomics 10 124

23. ChoIHornLFelixTMFosterLGregoryG 2010 Age- and diet-specific effects of variation at S6 kinase on life history, metabolic, and immune response traits in Drosophila melanogaster. DNA Cell Biol 29 473 485

24. PawlikowskaLHuDHuntsmanSSungAChuC 2009 Association of common genetic variation in the insulin/IGF1 signaling pathway with human longevity. Aging Cell 8 460 472

25. GylvinTEkJNolsoeRAlbrechtsenAAndersenG 2009 Functional SOCS1 polymorphisms are associated with variation in obesity in whites. Diabetes Obes Metab 11 196 203

26. EmlenDJSzafranQCorleyLSDworkinI 2006 Insulin signaling and limb-patterning: candidate pathways for the origin and evolutionary diversification of beetle ‘horns’. Heredity (Edinb) 97 179 191

27. ClancyDJGemsDHarshmanLGOldhamSStockerH 2001 Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292 104 106

28. PartridgeLGemsD 2002 Mechanisms of ageing: public or private? Nat Rev Genet 3 165 175

29. SelmanCTulletJMWieserDIrvineELingardSJ 2009 Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 326 140 144

30. ParkerGA 1983 Mate quality and mating decisions. . BatesonPPG Mate Choice Cambridge Cambridge University Press 141 166

31. ParkerGASimmonsLWStockleyPMcCDCharnovEL 1999 Optimal copula duration in yellow dung flies: effects of female size and egg content. Anim Behav 57 795 805

32. ByrnePGRiceWR 2006 Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster. Proc Biol Sci 273 917 922

33. YewJSoltwischJPirklADreisewerdK 2011 Direct laser desorption ionization of endogenous and exogenous compounds from insect cuticles: practical and methodological aspects. J Am Soc Mass Spectrom 22 1273 1284

34. FernandezMPChanYBYewJYBilleterJCDreisewerdK 2011 Pheromonal and behavioral cues trigger male-to-female aggression in Drosophila. PLoS Biol 8 e1000541

35. YewJYDreisewerdKLuftmannHMuthingJPohlentzG 2009 A new male sex pheromone and novel cuticular cues for chemical communication in Drosophila. Curr Biol 19 1245 1254

36. KuoTHYewJYFedinaTYDreisewerdKDierickHA 2012 Aging modulates cuticular hydrocarbons and sexual attractiveness in Drosophila melanogaster. J Exp Biol 215 814 821

37. KimSEChoJYKimKSLeeSJLeeKH 2004 Drosophila PI3 kinase and Akt involved in insulin-stimulated proliferation and ERK pathway activation in Schneider cells. Cell Signal 16 1309 1317

38. GaoXNeufeldTPPanD 2000 Drosophila PTEN regulates cell growth and proliferation through PI3K-dependent and -independent pathways. Dev Biol 221 404 418

39. BohniRRiesgo-EscovarJOldhamSBrogioloWStockerH 1999 Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97 865 875

40. BilleterJCAtallahJKruppJJMillarJGLevineJD 2009 Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461 987 991

41. SiwickiKKRiccioPLadewskiLMarcillacFDartevelleL 2005 The role of cuticular pheromones in courtship conditioning of Drosophila males. Learn Mem 12 636 645

42. FerveurJFSureauG 1996 Simultaneous influence on male courtship of stimulatory and inhibitory pheromones produced by live sex-mosaic Drosophila melanogaster. Proc Biol Sci 263 967 973

43. Wicker-ThomasCGuenachiIKeitaYF 2009 Contribution of oenocytes and pheromones to courtship behaviour in Drosophila. BMC Biochem 10 21

44. LizcanoJMAlrubaieSKielochADeakMLeeversSJ 2003 Insulin-induced Drosophila S6 kinase activation requires phosphoinositide 3-kinase and protein kinase B. Biochem J 374 297 306

45. RadimerskiTMontagneJRintelenFStockerHvan der KaayJ 2002 dS6K-regulated cell growth is dPKB/dPI(3)K-independent, but requires dPDK1. Nat Cell Biol 4 251 255

46. SarbassovDDGuertinDAAliSMSabatiniDM 2005 Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307 1098 1101

47. HennigKMNeufeldTP 2002 Inhibition of cellular growth and proliferation by dTOR overexpression in Drosophila. Genesis 34 107 110

48. UeyamaMChertempsTLabeurCWicker-ThomasC 2005 Mutations in the desat1 gene reduces the production of courtship stimulatory pheromones through a marked effect on fatty acids in Drosophila melanogaster. Insect Biochem Mol Biol 35 911 920

49. GreenbergAJMoranJRCoyneJAWuCI 2003 Ecological adaptation during incipient speciation revealed by precise gene replacement. Science 302 1754 1757

50. WigbySSlackCGronkeSMartinezPCalboliFC 2011 Insulin signalling regulates remating in female Drosophila. Proc Biol Sci 278 424 431

51. TuMPEpsteinDTatarM 2002 The demography of slow aging in male and female Drosophila mutant for the insulin-receptor substrate homologue chico. Aging Cell 1 75 80

52. WeberKJohnsonNChamplinDPattyA 2005 Many P-element insertions affect wing shape in Drosophila melanogaster. Genetics 169 1461 1475

53. BrittonJSLockwoodWKLiLCohenSMEdgarBA 2002 Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev Cell 2 239 249

54. PoonPCKuoTHLinfordNJRomanGPletcherSD 2010 Carbon dioxide sensing modulates lifespan and physiology in Drosophila. PLoS Biol 8 e1000356

55. CoyneJACrittendenAPMahK 1994 Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila. Science 265 1461 1464

56. SavaritFSureauGCobbMFerveurJF 1999 Genetic elimination of known pheromones reveals the fundamental chemical bases of mating and isolation in Drosophila. Proc Natl Acad Sci U S A 96 9015 9020