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Annual Review of Entomology

Volume 61, 2016

The Genetic Basis of Pheromone Evolution in Moths

Abstract

Moth sexual pheromones are widely studied as a fine-tuned system of intraspecific sexual communication that reinforces interspecific reproductive isolation. However, their evolution poses a dilemma: How can the female pheromone and male preference simultaneously change to create a new pattern of species-specific attraction? Solving this puzzle requires us to identify the genes underlying intraspecific variation in signals and responses and to understand the evolutionary mechanisms responsible for their interspecific divergence. Candidate gene approaches and functional analyses have yielded insights into large families of biosynthetic enzymes and pheromone receptors, although the factors controlling their expression remain largely unexplored. Intra- and interspecific crosses have provided tantalizing evidence of regulatory genes, although, to date, mapping resolution has been insufficient to identify them. Recent advances in high-throughput genome and transcriptome sequencing, together with established techniques, have great potential to help scientists identify the specific genetic changes underlying divergence and resolve the mystery of how moth sexual communication systems evolve.

Keyword(s): divergence, genetic analyses, interspecific variation, intraspecific variation, Lepidoptera, sexual communication
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2016-03-11
2024-04-20
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Literature Cited

  1. Albre J, Liénard MA, Sirey TM, Schmidt S, Tooman LK. 1.  et al. 2012. Sex pheromone evolution is associated with differential regulation of the same desaturase gene in two genera of leafroller moths. PLOS Genet. 8:e1002489 [Google Scholar]
  2. Albre J, Steinwender B, Newcomb RD. 2.  2013. The evolution of desaturase gene regulation involved in sex pheromone production in leafroller moths of the genus Planotortrix. J. Hered. 104:627–38 [Google Scholar]
  3. Allison JD, Cardé RT. 3.  2008. Male pheromone blend preference function measured in choice and no-choice wind tunnel trials with almond moths, Cadra cautella. Anim. Behav. 75:259–66 [Google Scholar]
  4. Allison JD, Roff DA, Cardé RT. 4.  2008. Genetic independence of female signal form and male receiver design in the almond moth, Cadra cautella. J. Evol. Biol. 21:1666–72 [Google Scholar]
  5. Arima R, Takahara K, Kadoshima T, Numazaki F, Ando T. 5.  et al. 1991. Hormonal regulation of pheromone biosynthesis in the silkworm moth, Bombyx mori (Lepidoptera, Bombycidae). Appl. Entomol. Zool. 26:137–47 [Google Scholar]
  6. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL. 6.  et al. 2008. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLOS ONE 3:e3376 [Google Scholar]
  7. Baker TC, Quero C, Ochieng SA, Vickers NJ. 7.  2006. Inheritance of olfactory preferences II. Olfactory receptor neuron responses from Heliothis subflexa×Heliothis virescens hybrid male moths. Brain Behav. Evol. 68:75–89 [Google Scholar]
  8. Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P. 8.  et al. 2007. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25:1322–26 [Google Scholar]
  9. Baxter SW, Davey JW, Johnston JS, Shelton AM, Heckel DG. 9.  et al. 2011. Linkage mapping and comparative genomics using next-generation RAD sequencing of a non-model organism. PLOS ONE 6:e19315 [Google Scholar]
  10. Benton R, Vannice KS, Vosshall LB. 10.  2007. An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450:289–93 [Google Scholar]
  11. Berg B, Zhao XC, Wang G. 11.  2014. Processing of pheromone information in related species of heliothine moths. Insects 5:742–61 [Google Scholar]
  12. Bjostad LB, Wolf WA, Roelofs WL. 12.  1987. Pheromone biosynthesis in lepidopterans: desaturation and chain shortening. Pheromone Biochemistry GD Prestwich, GJ Blomquist 77–117 Orlando, FL: Academic [Google Scholar]
  13. Butlin RK. 13.  1995. Reinforcement—an idea evolving. Trends Ecol. Evol. 10:432–34 [Google Scholar]
  14. Cardé RT, Baker TC. 14.  1984. Sexual communication with pheromones. Chemical Ecology of Insects WJ Bell, RT Cardé 355–83 London: Chapman Hall [Google Scholar]
  15. Cardé RT, Cardé AM, Hill AS, Roelofs WL. 15.  1977. Sex pheromone specificity as a reproductive isolating mechanism among sibling species Archips argyrospilus and A. mortuanus and other sympatric tortricine moths (Lepidoptera, Tortricidae). J. Chem. Ecol. 3:71–84 [Google Scholar]
  16. Carroll D. 16.  2014. Genome engineering with targetable nucleases. Annu. Rev. Biochem. 83:409–39 [Google Scholar]
  17. Chen QM, Cheng DJ, Liu SP, Ma ZG, Tan X, Zhao P. 17.  2014. Genome-wide identification and expression profiling of the fatty acid desaturase gene family in the silkworm, Bombyx mori. Genet. Mol. Res. 13:3747–60 [Google Scholar]
  18. Collins RD, Cardé RT. 18.  1989. Heritable variation in pheromone response of the pink bollworm, Pectinophora gossypiella (Lepidoptera, Gelechiidae). J. Chem. Ecol. 15:2647–59 [Google Scholar]
  19. Coracini M, Bengtsson M, Liblikas I, Witzgall P. 19.  2004. Attraction of codling moth males to apple volatiles. Entomol. Exp. Appl. 110:1–10 [Google Scholar]
  20. Cossé AA, Campbell MG, Glover TJ, Linn CE, Todd JL. 20.  et al. 1995. Pheromone behavioral responses in unusual male European corn borer hybrid progeny not correlated to electrophysiological phenotypes of their pheromone-specific antennal neurons. Experientia 51:809–16 [Google Scholar]
  21. Dasmahapatra KK, Walters JR, Briscoe AD, Davey JW, Whibley A. 21.  et al. 2012. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487:94–98 [Google Scholar]
  22. De Jong MCM, Sabelis MW. 22.  1991. Limits to runaway sexual selection—the wallflower paradox. J. Evol. Biol. 4:637–56 [Google Scholar]
  23. Dekker T, Revadi S, Mansourian S, Ramasamy S, Lebreton S. 23.  et al. 2015. Loss of Drosophila pheromone reverses its role in sexual communication in Drosophila suzukii. Proc. R. Soc. B 282:e20143018 [Google Scholar]
  24. Domingue MJ, Haynes KF, Todd JL, Baker TC. 24.  2009. Altered olfactory receptor neuron responsiveness is correlated with a shift in behavioral response in an evolved colony of the cabbage looper moth, Trichoplusia ni. J. Chem. Ecol. 35:405–15 [Google Scholar]
  25. Domingue MJ, Musto CJ, Linn CE, Roelofs WL, Baker TC. 25.  2007. Altered olfactory receptor neuron responsiveness in rare Ostrinia nubilalis males attracted to the O. furnacalis pheromone blend. J. Insect Physiol. 53:1063–71 [Google Scholar]
  26. Domingue MJ, Musto CJ, Linn CE, Roelofs WL, Baker TC. 26.  2007. Evidence of olfactory antagonistic imposition as a facilitator of evolutionary shifts in pheromone blend usage in Ostrinia spp. (Lepidoptera: Crambidae). J. Insect Physiol. 53:488–96 [Google Scholar]
  27. Dopman EB, Bogdanowicz SM, Harrison RG. 27.  2004. Genetic mapping of sexual isolation between E and Z pheromone strains of the European corn borer (Ostrinia nubilalis). Genetics 167:301–9 [Google Scholar]
  28. El-Sayed EM. 28.  2014. The pherobase: database of pheromones and semiochemicals. http://www.pherobase.com
  29. Eltahlawy H, Buckner JS, Foster SP. 29.  2007. Evidence for two-step regulation of pheromone biosynthesis by the pheromone biosynthesis–activating neuropeptide in the moth Heliothis virescens. Arch. Insect Biochem. Physiol. 64:120–30 [Google Scholar]
  30. Endo K, Aoki T, Yoda Y, Kimura K, Hama C. 30.  2007. Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages. Nat. Neurosci. 10:153–60 [Google Scholar]
  31. Forstner M, Breer H, Krieger J. 31.  2009. A receptor and binding protein interplay in the detection of a distinct pheromone component in the silkmoth Antheraea polyphemus. Int. J. Biol. Sci. 5:745–57 [Google Scholar]
  32. Foster SP, Muggleston SJ, Löfstedt C, Hansson B. 32.  1997. A genetic study on pheromonal communication in two Ctenopseustis moths. Insect Pheromone Research: New Directions RT Cardé, AK Minks 514–24 New York: Chapman Hall [Google Scholar]
  33. Fujii T, Ito K, Tatematsu M, Shimada T, Katsuma S, Ishikawa Y. 33.  2011. Sex pheromone desaturase functioning in a primitive Ostrinia moth is cryptically conserved in congeners' genomes. PNAS 108:7102–6 [Google Scholar]
  34. Fujii T, Namiki S, Abe H, Sakurai T, Ohnuma A. 34.  et al. 2011. Sex-linked transcription factor involved in a shift of sex-pheromone preference in the silkmoth Bombyx mori. PNAS 108:18038–43 [Google Scholar]
  35. Galizia CG, Rössler W. 35.  2010. Parallel olfactory systems in insects: anatomy and function. Annu. Rev. Entomol. 55:399–420 [Google Scholar]
  36. Gould F, Estock M, Hillier NK, Powell B, Groot AT. 36.  et al. 2010. Sexual isolation of male moths explained by a single pheromone response QTL containing four receptor genes. PNAS 107:8660–65 [Google Scholar]
  37. Goulding SE, zur Lage P, Jarman AP. 37.  2000. Amos, a proneural gene for Drosophila olfactory sense organs that is regulated by lozenge. Neuron 25:69–78 [Google Scholar]
  38. Gries G, Schaefer PW, Gries R, Liska J, Gotoh T. 38.  2001. Reproductive character displacement in Lymantria monacha from northern Japan. J. Chem. Ecol. 27:1163–76 [Google Scholar]
  39. Groot AT, Estock ML, Horovitz JL, Hamilton J, Santangelo RG. 39.  et al. 2009. QTL analysis of sex pheromone blend differences between two closely related moths: insights into divergence in biosynthetic pathways. Insect Biochem. Mol. Biol. 39:568–77 [Google Scholar]
  40. Groot AT, Horovitz JL, Hamilton J, Santangelo RG, Schal C, Gould F. 40.  2006. Experimental evidence for interspecific directional selection on moth pheromone communication. PNAS 103:5858–63 [Google Scholar]
  41. Groot AT, Schofl G, Inglis O, Donnerhacke S, Classen A. 41.  et al. 2014. Within-population variability in a moth sex pheromone blend: genetic basis and behavioral consequences. Proc. R. Soc. B 281:e20133054 [Google Scholar]
  42. Groot AT, Staudacher H, Barthel A, Inglis O, Schofl G. 42.  et al. 2013. One quantitative trait locus for intra- and interspecific variation in a sex pheromone. Mol. Ecol. 22:1065–80 [Google Scholar]
  43. Grosse-Wilde E, Kuebler LS, Bucks S, Vogel H, Wicher D, Hansson BS. 43.  2011. Antennal transcriptome of Manduca sexta. PNAS 108:7449–54 [Google Scholar]
  44. Grosse-Wilde E, Svatos A, Krieger J. 44.  2006. A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem. Senses 31:547–55 [Google Scholar]
  45. Gu S-H, Wu K-M, Guo Y-Y, Pickett JA, Field LM. 45.  et al. 2013. Identification of genes expressed in the sex pheromone gland of the black cutworm Agrotis ipsilon with putative roles in sex pheromone biosynthesis and transport. BMC Genom 14:636 [Google Scholar]
  46. Gu S-H, Zhou J-J, Wang G-R, Zhang Y-J, Guo Y-Y. 46.  2013. Sex pheromone recognition and immunolocalization of three pheromone binding proteins in the black cutworm moth Agrotis ipsilon. Insect Biochem. Mol. Biol. 43:237–51 [Google Scholar]
  47. Gupta BP, Flores GV, Banerjee U, Rodrigues V. 47.  1998. Patterning an epidermal field: Drosophila Lozenge, a member of the AML-1/Runt family of transcription factors, specifies olfactory sense organ type in a dose-dependent manner. Dev. Biol. 203:400–11 [Google Scholar]
  48. Gupta BP, Rodrigues V. 48.  1997. Atonal is a proneural gene for a subset of olfactory sense organs in Drosophila. Genes Cells 2:225–33 [Google Scholar]
  49. Hagström ÅK, Wang H-L, Liénard MA, Lassance J-M, Johansson T, Löfstedt C. 49.  2013. A moth pheromone brewery: production of (Z)-11-hexadecenol by heterologous co-expression of two biosynthetic genes from a noctuid moth in a yeast cell factory. Microb. Cell Fact. 12:125 [Google Scholar]
  50. Han LZ, Gu HN, Zhai BP, Zhang XX. 50.  2009. Genetic effects on flight capacity in the beet armyworm, Spodoptera exigua (Lep., Noctuidae). J. Appl. Entomol. 133:262–71 [Google Scholar]
  51. Hansson BS, Lofstedt C, Foster SP. 51.  1989. Z-linked inheritance of male olfactory response to sex pheromone components in two species of tortricid moths, Ctenopseustis obliquana and Ctenopseustis sp. Entomol. Exp. Appl. 53:137–45 [Google Scholar]
  52. Hansson BS, Löfstedt C, Roelofs WL. 52.  1987. Inheritance of olfactory response to sex pheromone components in Ostrinia nubilalis. Naturwissenschaften 74:497–99 [Google Scholar]
  53. Hansson BS, Tóth M, Löfstedt C, Szöcs G, Subchev M, Löfqvist J. 53.  1990. Pheromone variation among eastern European and a western Asian population of the turnip moth Agrotis segetum. J. Chem. Ecol. 16:1611–22 [Google Scholar]
  54. Heckel DG. 54.  1993. Comparative genetic linkage mapping in insects. Annu. Rev. Entomol. 38:381–408 [Google Scholar]
  55. Hemmann DJ, Allison JD, Haynes KF. 55.  2008. Trade-off between sensitivity and specificity in the cabbage looper moth response to sex pheromone. J. Chem. Ecol. 34:1476–86 [Google Scholar]
  56. Hull JJ, Lee JM, Kajigaya R, Matsumoto S. 56.  2009. Bombyx mori homologs of STIM1 and Orai1 are essential components of the signal transduction cascade that regulates sex pheromone production. J. Biol. Chem. 284:31200–13 [Google Scholar]
  57. Hull JJ, Ohnishi A, Moto K, Kawasaki Y, Kurata R. 57.  et al. 2004. Cloning and characterization of the pheromone biosynthesis activating neuropeptide receptor from the silkmoth, Bombyx mori—significance of the carboxyl terminus in receptor internalization. J. Biol. Chem. 279:51500–7 [Google Scholar]
  58. Ibba I, Angioy AM, Hansson BS, Dekker T. 58.  2010. Macroglomeruli for fruit odors change blend preference in Drosophila. Naturwissenschaften 97:1059–66 [Google Scholar]
  59. Jin X, Ha TS, Smith DP. 59.  2008. SNMP is a signaling component required for pheromone sensitivity in Drosophila. PNAS 105:10996–1001 [Google Scholar]
  60. Johansson BG, Jones TM. 60.  2007. The role of chemical communication in mate choice. Biol. Rev. 82:265–89 [Google Scholar]
  61. Jung CR, Kim Y. 61.  2014. Comparative transcriptome analysis of sex pheromone glands of two sympatric lepidopteran congener species. Genomics 103:308–15 [Google Scholar]
  62. Jurenka R. 62.  2004. Insect pheromone biosynthesis. Chemistry of Pheromones and Other Semiochemicals I S Schulz 97–-132 Berlin: Springer-Verlag [Google Scholar]
  63. Kárpáti Z, Dekker T, Hansson BS. 63.  2008. Reversed functional topology in the antennal lobe of the male European corn borer. J. Exp. Biol. 211:2841–48 [Google Scholar]
  64. Kárpáti Z, Olsson S, Hansson BS, Dekker T. 64.  2010. Inheritance of central neuroanatomy and physiology related to pheromone preference in the male European corn borer. BMC Evol. Biol. 10:286 [Google Scholar]
  65. Kárpáti Z, Tasin M, Cardé RT, Dekker T. 65.  2013. Early quality assessment lessens pheromone specificity in a moth. PNAS 110:7377–82 [Google Scholar]
  66. Kim YJ, Nachman RJ, Aimanova K, Gill S, Adams ME. 66.  2008. The pheromone biosynthesis activating neuropeptide (PBAN) receptor of Heliothis virescens: identification, functional expression, and structure-activity relationships of ligand analogs. Peptides 29:268–75 [Google Scholar]
  67. Knipple DC, Rosenfield CL, Miller SJ, Liu WT, Tang J. 67.  et al. 1998. Cloning and functional expression of a cDNA encoding a pheromone gland–specific acyl-CoA Δ11-desaturase of the cabbage looper moth, Trichoplusia ni. PNAS 95:15287–92 [Google Scholar]
  68. Knipple DC, Rosenfield CL, Nielsen R, You KM, Jeong SE. 68.  2002. Evolution of the integral membrane desaturase gene family in moths and flies. Genetics 162:1737–52 [Google Scholar]
  69. Koutroumpa FA, Kárpáti Z, Monsempes C, Hill SR, Hansson BS. 69.  et al. 2014. Shifts in sensory neuron identity parallel differences in pheromone preference in the European corn borer. Front. Ecol. Evol. 2:e65 [Google Scholar]
  70. Krieger J, Raming K, Dewer YME, Bette S, Conzelmann S, Breer H. 70.  2002. A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. Eur. J. Neurosci. 16:619–28 [Google Scholar]
  71. Kronforst MR, Hansen MEB, Crawford NG, Gallant JR, Zhang W. 71.  et al. 2013. Hybridization reveals the evolving genomic architecture of speciation. Cell Rep. 5:666–77 [Google Scholar]
  72. Lassance JM, Bogdanowicz SM, Wanner KW, Löfstedt C, Harrison RG. 72.  2011. Gene genealogies reveal differentiation at sex pheromone olfactory receptor loci in pheromone strains of the European corn borer Ostrinia nubilalis. Evolution 65:1583–93 [Google Scholar]
  73. Lassance JM, Groot AT, Liénard MA, Binu A, Borgwardt C. 73.  et al. 2010. Allelic variation in a fatty-acyl reductase gene causes pheromone divergence in European corn borer races. Nature 466:486–89 [Google Scholar]
  74. Lassance JM, Liénard MA, Antony B, Qian SG, Fujii T. 74.  et al. 2013. Functional consequences of sequence variation in the pheromone biosynthetic gene pgFAR for Ostrinia moths. PNAS 110:3967–72 [Google Scholar]
  75. Leary GP, Allen JE, Bunger PL, Luginbill JB, Linn CE. 75.  et al. 2012. Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. PNAS 109:14081–86 [Google Scholar]
  76. Lee S-G, Vickers NJ, Baker TC. 76.  2006. Glomerular targets of Heliothis subflexa male olfactory receptor neurons housed within long trichoid sensilla. Chem. Senses 31:821–34 [Google Scholar]
  77. Legeai F, Malpel S, Montagné N, Monsempes C, Cousserans F. 77.  et al. 2011. An expressed sequence tag collection from the male antennae of the noctuid moth Spodoptera littoralis: a resource for olfactory and pheromone detection research. BMC Genom. 12:86 [Google Scholar]
  78. Li Q, Ha TS, Okuwa S, Wang Y, Wang Q. 78.  et al. 2013. Combinatorial rules of precursor specification underlying olfactory neuron diversity. Curr. Biol. 23:2481–90 [Google Scholar]
  79. Liénard MA, Hagström ÅK, Lassance JM, Löfstedt C. 79.  2010. Evolution of multicomponent pheromone signals in small ermine moths involves a single fatty-acyl reductase gene. PNAS 107:10955–60 [Google Scholar]
  80. Liénard MA, Lassance J-M, Wang H-L, Zhao C-H, Piskur J. 80.  et al. 2010. Elucidation of the sex-pheromone biosynthesis producing 5,7-dodecadienes in Dendrolimus punctatus (Lepidoptera: Lasiocampidae) reveals Δ11- and Δ9-desaturases with unusual catalytic properties. Insect Biochem. Mol. Biol. 40:440–52 [Google Scholar]
  81. Liénard MA, Strandh M, Hedenström E, Johansson T, Löfstedt C. 81.  2008. Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera. BMC Evol. Biol. 8:270 [Google Scholar]
  82. Linn CE, Bjostad LB, Du JW, Roelofs WL. 82.  1984. Redundancy in a chemical signal—behavioral responses of male Trichoplusia ni to a 6-component pheromone blend. J. Chem. Ecol. 10:1635–58 [Google Scholar]
  83. Linn CE, Musto CJ, Roelofs WL. 83.  2007. More rare males in Ostrinia: response of Asian corn borer moths to the sex pheromone of the European corn borer. J. Chem. Ecol. 33:199–212 [Google Scholar]
  84. Linn CE, O'Connor M, Roelofs W. 84.  2003. Silent genes and rare males: a fresh look at pheromone blend response specificity in the European corn borer moth, Ostrinia nubilalis. J. Insect Sci. 3:15 [Google Scholar]
  85. Linn CE, Roelofs WL. 85.  1983. Effect of varying proportions of the alcohol component on sex pheromone blend discrimination in male oriental fruit moths. Physiol. Entomol. 8:291–306 [Google Scholar]
  86. Linn CE, Young MS, Gendle M, Glover TJ, Roelofs WL. 86.  1997. Sex pheromone blend discrimination in two races and hybrids of the European corn borer moth, Ostrinia nubilalis. Physiol. Entomol. 22:212–23 [Google Scholar]
  87. Liu BH. 87.  1997. Statistical Genomics: Linkage, Mapping, and QTL Analysis Boca Raton, FL: CRC Press
  88. Liu YB, Haynes KF. 88.  1994. Evolution of behavioral responses to sex pheromone in mutant laboratory colonies of Trichoplusia ni. J. Chem. Ecol. 20:231–38 [Google Scholar]
  89. Löfstedt C. 89.  1993. Moth pheromone genetics and evolution. Philos. Trans. R. Soc. B 340:167–77 [Google Scholar]
  90. Löfstedt C, Hansson BS, Roelofs W, Bengtsson BO. 90.  1989. No linkage between genes controlling female pheromone production and male pheromone response in the European corn borer, Ostrinia nubilalis Hubner (Lepidoptera, Pyralidae). Genetics 123:553–56 [Google Scholar]
  91. Löfstedt C, Herrebout WM, Menken SBJ. 91.  1991. Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moths (Yponomeutidae). Chemoecology 2:20–28 [Google Scholar]
  92. Maitani MM, Allara DL, Park KC, Lee S-G, Baker TC. 92.  2010. Moth olfactory trichoid sensilla exhibit nanoscale-level heterogeneity in surface lipid properties. Arthropod Struct. Dev. 39:1–16 [Google Scholar]
  93. Mao YB, Tao XY, Xue XY, Wang LJ, Chen XY. 93.  2011. Cotton plants expressing CYP6AE14 double-stranded RNA show enhanced resistance to bollworms. Transgenic Res. 20:665–73 [Google Scholar]
  94. Matsumoto S, Fonagy A, Yamamoto M, Wang F, Yokoyama N. 94.  et al. 2002. Chemical characterization of cytoplasmic lipid droplets in the pheromone-producing cells of the silkmoth, Bombyx mori. Insect Biochem. Mol. Biol. 32:1447–55 [Google Scholar]
  95. Matsumoto S, Hull JJ, Ohnishi A, Moto K, Fonagy A. 95.  2007. Molecular mechanisms underlying sex pheromone production in the silkmoth, Bombyx mori: characterization of the molecular components involved in bombykol biosynthesis. J. Insect Physiol. 53:752–59 [Google Scholar]
  96. Matsumoto S, Yoshiga T, Yokoyama N, Iwanaga M, Koshiba S. 96.  et al. 2001. Characterization of acyl-CoA-binding protein (ACBP) in the pheromone gland of the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 31:603–9 [Google Scholar]
  97. McElfresh JS, Millar JG. 97.  2001. Geographic variation in the pheromone system of the saturniid moth Hemileuca eglanterina. Ecology 82:3505–18 [Google Scholar]
  98. Millar J. 98.  2014. The devil is in the details. J. Chem. Ecol. 40:517–18 [Google Scholar]
  99. Miura N, Nakagawa T, Touhara K, Ishikawa Y. 99.  2010. Broadly and narrowly tuned odorant receptors are involved in female sex pheromone reception in Ostrinia moths. Insect Biochem. Mol. Biol. 40:64–73 [Google Scholar]
  100. Montagné N, Chertemps T, Brigaud I, François A, François M-C. 100.  et al. 2012. Functional characterization of a sex pheromone receptor in the pest moth Spodoptera littoralis by heterologous expression in Drosophila. Eur. J. Neurosci. 36:2588–96 [Google Scholar]
  101. Moto K, Suzuki MG, Hull JJ, Kurata R, Takahashi S. 101.  et al. 2004. Involvement of a bifunctional fatty-acyl desaturase in the biosynthesis of the silkmoth, Bombyx mori, sex pheromone. PNAS 101:8631–36 [Google Scholar]
  102. Moto K, Yoshiga T, Yamamoto M, Takahashi S, Okano K. 102.  et al. 2003. Pheromone gland–specific fatty-acyl reductase of the silkmoth, Bombyx mori. PNAS 100:9156–61 [Google Scholar]
  103. Neafsey DE, Waterhouse RM, Abai MR, Aganezov SS, Alekseyev MA. 103.  et al. 2015. Highly evolvable malaria vectors: the genomes of 16 Anopheles mosquitoes. Science 347:43 [Google Scholar]
  104. Ohnishi A, Hull JJ, Kaji M, Hashimoto K, Lee JM. 104.  et al. 2011. Hormone signaling linked to silkmoth sex pheromone biosynthesis involves Ca2+/calmodulin-dependent protein kinase II–mediated phosphorylation of the insect PAT family protein Bombyx mori lipid storage droplet protein-1 (BmLsd1). J. Biol. Chem. 286:24101–12 [Google Scholar]
  105. Ohnishi A, Hull JJ, Matsumoto S. 105.  2006. Targeted disruption of genes in the Bombyx mori sex pheromone biosynthetic pathway. PNAS 103:4398–403 [Google Scholar]
  106. Olsson SB, Kesevan S, Groot AT, Dekker T, Heckel DG, Hansson BS. 106.  2010. Ostrinia revisited: evidence for sex linkage in European corn borer Ostrinia nubilalis (Hubner) pheromone reception. BMC Evol. Biol. 10:285 [Google Scholar]
  107. Paterson HEH. 107.  1985. The recognition concept of species. Species and Speciation ES Vrba 21–30 Pretoria, S. Afr.: Transvaal Mus. [Google Scholar]
  108. Phelan PL. 108.  1992. Evolution of sex pheromones and the role of asymmetric tracking. Insect Chemical Ecology: An Evolutionary Approach BD Roitber, MB Isman 265–314 New York: Chapman Hall [Google Scholar]
  109. Poland JA, Rife TW. 109.  2012. Genotyping-by-sequencing for plant breeding and genetics. Plant Genome 5:92–102 [Google Scholar]
  110. Rafaeli A, Bober R, Becker L, Choi MY, Fuers EJ, Jurenka R. 110.  2007. Spatial distribution and differential expression of the PBAN receptor in tissues of adult Helicoverpa spp. (Lepidoptera: Noctuidae). Insect Mol. Biol. 16:287–93 [Google Scholar]
  111. Rafaeli A, Jurenka R. 111.  2003. PBAN regulation of pheromone biosynthesis in female moths. Pheromone Biochemistry and Molecular Biology GJ Blomquist, R Vogt 107–36 London: Elsevier [Google Scholar]
  112. Raina AK, Jaffe H, Kempe TG, Keim P, Blacher RW. 112.  et al. 1989. Identification of a neuropeptide hormone that regulates sex pheromone production in female moths. Science 244:796–98 [Google Scholar]
  113. Ray A, van der Goes van Naters W, Shiraiwa T, Carlson JR. 113.  2007. Mechanisms of odor receptor gene choice in Drosophila. Neuron 53:353–69 [Google Scholar]
  114. Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R. 114.  et al. 2008. The genome of the model beetle and pest Tribolium castaneum. Nature 452:949–55 [Google Scholar]
  115. Rodríguez S, Hao GX, Liu WT, Piña B, Rooney AP. 115.  et al. 2004. Expression and evolution of Δ9 and Δ11 desaturase genes in the moth Spodoptera littoralis. Insect Biochem. Mol. Biol. 34:1315–28 [Google Scholar]
  116. Roelofs W, Glover T, Tang X, Sreng I, Robbins P. 116.  et al. 1987. Sex pheromone production and perception in European corn borer moths is determined by both autosomal and sex-linked genes. PNAS 84:7585–89 [Google Scholar]
  117. Roelofs WL, Liu WT, Hao GX, Jiao HM, Rooney AP, Linn CE. 117.  2002. Evolution of moth sex pheromones via ancestral genes. PNAS 99:13621–26 [Google Scholar]
  118. Rosenfield CL, You KM, Marsella-Herrick P, Roelofs WL, Knipple DC. 118.  2001. Structural and functional conservation and divergence among acyl-CoA desaturases of two noctuid species, the corn earworm, Helicoverpa zea, and the cabbage looper, Trichoplusia ni. Insect Biochem. Mol. Biol. 31:949–64 [Google Scholar]
  119. Sakai R, Fukuzawa M, Nakano R, Tatsuki S, Ishikawa Y. 119.  2009. Alternative suppression of transcription from two desaturase genes is the key for species-specific sex pheromone biosynthesis in two Ostrinia moths. Insect Biochem. Mol. Biol. 39:62–67 [Google Scholar]
  120. Sakurai T, Nakagawa T, Mitsuno H, Mori H, Endo Y. 120.  et al. 2004. Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. PNAS 101:16653–58 [Google Scholar]
  121. Schultze A, Breer H, Krieger J. 121.  2014. The blunt trichoid sensillum of female mosquitoes, Anopheles gambiae: odorant binding protein and receptor types. Int. J. Biol. Sci. 10:426–37 [Google Scholar]
  122. Serra M, Gauthier LT, Fabriàs G, Buist PH. 122.  2006. Δ11 desaturases of Trichoplusia ni and Spodoptera littoralis exhibit dual catalytic behaviour. Insect Biochem. Mol. Biol. 36:822–25 [Google Scholar]
  123. Sheck AL, Groot AT, Ward CM, Gemeno C, Wang J. 123.  et al. 2006. Genetics of sex pheromone blend differences between Heliothis virescens and Heliothis subflexa: a chromosome mapping approach. J. Evol. Biol. 19:600–17 [Google Scholar]
  124. Strandh M, Johansson T, Ahren D, Löfstedt C. 124.  2008. Transcriptional analysis of the pheromone gland of the turnip moth, Agrotis segetum (Noctuidae), reveals candidate genes involved in pheromone production. Insect Mol. Biol. 17:73–85 [Google Scholar]
  125. Strandh M, Johansson T, Löfstedt C. 125.  2009. Global transcriptional analysis of pheromone biosynthesis–related genes in the female turnip moth, Agrotis segetum (Noctuidae) using a custom-made cDNA microarray. Insect Biochem. Mol. Biol. 39:484–89 [Google Scholar]
  126. Symonds MRE, Elgar MA. 126.  2008. The evolution of pheromone diversity. Trends Ecol. Evol. 23:220–28 [Google Scholar]
  127. Tang JD, Wolf WA, Roelofs WL, Knipple DC. 127.  1991. Development of functionally competent cabbage looper moth sex pheromone glands. Insect Biochem. 21:573–81 [Google Scholar]
  128. Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H. 128.  et al. 2011. RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J. Insect Physiol. 57:231–45 [Google Scholar]
  129. Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ. 129.  1999. Insect pheromones—an overview of biosynthesis and endocrine regulation. Insect Biochem. Mol. Biol. 29:481–514 [Google Scholar]
  130. Todd JL, Haynes KF, Baker TC. 130.  1992. Antennal neurones specific for redundant pheromone components in normal and mutant Trichoplusia ni males. Physiol. Entomol. 17:183–92 [Google Scholar]
  131. Tsfadia O, Azrielli A, Falach L, Zada A, Roelofs W, Rafaeli A. 131.  2008. Pheromone biosynthetic pathways: PBAN-regulated rate-limiting steps and differential expression of desaturase genes in moth species. Insect Biochem. Mol. Biol. 38:552–67 [Google Scholar]
  132. Ueira-Vieira C, Kimbrell DA, de Carvalho WJ, Leal WS. 132.  2014. Facile functional analysis of insect odorant receptors expressed in the fruit fly: validation with receptors from taxonomically distant and closely related species. Cell. Mol. Life Sci. 71:4675–80 [Google Scholar]
  133. Vickers NJ. 133.  2006. Inheritance of olfactory preferences I. Pheromone-mediated behavioral responses of Heliothis subflexa×Heliothis virescens hybrid male moths. Brain Behav. Evol. 68:63–74 [Google Scholar]
  134. Vickers NJ, Baker TC. 134.  1997. Chemical communication in heliothine moths VII. Correlation between diminished responses to point source plumes and single filaments similarly tainted with a behavioral antagonist. J. Comp. Physiol. A 180:523–36 [Google Scholar]
  135. Vogel H, Heidel AJ, Heckel DG, Groot AT. 135.  2010. Transcriptome analysis of the sex pheromone gland of the noctuid moth Heliothis virescens. BMC Genom. 11:29 [Google Scholar]
  136. Wang G, Vásquez GM, Schal C, Zwiebel LJ, Gould F. 136.  2011. Functional characterization of pheromone receptors in the tobacco budworm Heliothis virescens. Insect Mol. Biol. 20:125–33 [Google Scholar]
  137. Wei W, Xin HH, Roy B, Dai JB, Miao YG, Gao GJ. 137.  2014. Heritable genome editing with CRISPR/Cas9 in the silkworm, Bombyx mori. PLOS ONE 9:e101210 [Google Scholar]
  138. Wilson RC, Doudna JA. 138.  2013. Molecular mechanisms of RNA interference. Annu. Rev. Biophys. 42:217–39 [Google Scholar]
  139. Wu H, Hou C, Huang L-Q, Yan F-S, Wang C-Z. 139.  2013. Peripheral coding of sex pheromone blends with reverse ratios in two Helicoverpa species. PLOS ONE 8:e70078 [Google Scholar]
  140. Xue BY, Rooney AP, Kajikawa M, Okada N, Roelofs WL. 140.  2007. Novel sex pheromone desaturases in the genomes of corn borers generated through gene duplication and retroposon fusion. PNAS 104:4467–72 [Google Scholar]
  141. Yang Z. 141.  2006. Computational Molecular Evolution Oxford, UK: Oxford Univ. Press
  142. Yasukochi Y, Miura N, Nakano R, Sahara K, Ishikawa Y. 142.  2011. Sex-linked pheromone receptor genes of the European corn borer, Ostrinia nubilalis, are in tandem arrays. PLOS ONE 6:e18843 [Google Scholar]
  143. Zhan S, Zhang W, Niitepold K, Hsu J, Haeger JF. 143.  et al. 2014. The genetics of monarch butterfly migration and warning colouration. Nature 514:317–21 [Google Scholar]
  144. Zhang Y-N, Xia Y-H, Zhu J-Y, Li S-Y, Dong S-L. 144.  2014. Putative pathway of sex pheromone biosynthesis and degradation by expression patterns of genes identified from female pheromone gland and adult antenna of Sesamia inferens (Walker). J. Chem. Ecol. 40:439–51 [Google Scholar]
  145. Zhang Y-N, Ye Z-F, Yang K, Dong S-L. 145.  2014. Antenna-predominant and male-biased CSP19 of Sesamia inferens is able to bind the female sex pheromones and host plant volatiles. Gene 536:279–86 [Google Scholar]
  146. Zhu HT, Hummel T, Clemens JC, Berdnik D, Zipursky SL, Luo LQ. 146.  2006. Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe. Nat. Neurosci. 9:349–55 [Google Scholar]
  147. Zhu JW, Chastain BB, Spohn BG, Haynes KF. 147.  1997. Assortative mating in two pheromone strains of the cabbage looper moth, Trichoplusia ni. J. Insect Behav. 10:805–17 [Google Scholar]
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The Genetic Basis of Pheromone Evolution in Moths
Annual Review of Entomology 61, 99 (2016); https://doi.org/10.1146/annurev-ento-010715-023638
/content/journals/10.1146/annurev-ento-010715-023638
/content/journals/10.1146/annurev-ento-010715-023638
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