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Journal of Molecular Evolution

, Volume 79, Issue 1–2, pp 21–39 | Cite as

Molecular Evolution of the Odorant and Gustatory Receptor Genes in Lepidopteran Insects: Implications for Their Adaptation and Speciation

  • Patamarerk Engsontia
  • Unitsa Sangket
  • Wilaiwan Chotigeat
  • Chutamas Satasook
Original Article

Abstract

Lepidoptera (comprised of butterflies and moths) is one of the largest groups of insects, including more than 160,000 described species. Chemoreception plays important roles in the adaptation of these species to a wide range of niches, e.g., plant hosts, egg-laying sites, and mates. This study investigated the molecular evolution of the lepidopteran odorant (Or) and gustatory receptor (Gr) genes using recently identified genes from Bombyx mori, Danaus plexippus, Heliconius melpomene, Plutella xylostella, Heliothis virescens, Manduca sexta, Cydia pomonella, and Spodoptera littoralis. A limited number of cases of large lineage-specific gene expansion are observed (except in the P. xylostella lineage), possibly due to selection against tandem gene duplication. There has been strong purifying selection during the evolution of both lepidopteran odorant and gustatory genes, as shown by the low ω values estimated through CodeML analysis, ranging from 0.0093 to 0.3926. However, purifying selection has been relaxed on some amino acid sites in these receptors, leading to sequence divergence, which is a precursor of positive selection on these sequences. Signatures of positive selection were detected only in a few loci from the lineage-specific analysis. Estimation of gene gains and losses suggests that the common ancestor of the Lepidoptera had fewer Or genes compared to extant species and an even more reduced number of Gr genes, particularly within the bitter receptor clade. Multiple gene gains and a few gene losses occurred during the evolution of Lepidoptera. Gene family expansion may be associated with the adaptation of lepidopteran species to plant hosts, especially after angiosperm radiation. Phylogenetic analysis of the moth sex pheromone receptor genes suggested that chromosomal translocations have occurred several times. New sex pheromone receptors have arisen through tandem gene duplication. Positive selection was detected at some amino acid sites predicted to be in the extracellular and transmembrane regions of the newly duplicated genes, which might be associated with the evolution of the new pheromone receptors.

Keywords

Odorant receptor Gustatory receptor Molecular evolution Lepidoptera Chemoreception 

Notes

Acknowledgments

We would like to thank Hugh Robertson from the University of Illinois, Urbana Champaign, for the BmGr DNA sequences; Shui Zhan and Stephen Reppert from the University of Massachusetts Medical School, for the DpOR and DpGR protein sequences. Fillipe Vieira and Julio Rozas from the University of Barcelona for suggestion for the use of BadiRate. We thank the editor and the three anonymous reviewers for giving constructive suggestions for the improvement of this paper. This study was financially supported by the Graduate School and the Department of Biology, Faculty of Science, Prince of Songkla University.

Supplementary material

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Supplementary material 1 (XLS 486 kb)
239_2014_9633_MOESM2_ESM.doc (5.4 mb)
Supplementary material 2 (DOC 5525 kb)

References

  1. Albre J, Liénard MA, Sirey TM, Schmidt S, Tooman LK, Carraher C, Greenwood DR, Löfstedt C, Newcomb RD (2012) Sex pheromone evolution is associated with differential regulation of the same desaturase gene in two genera of leafroller moths. PLoS Genet 8(1):e1002489PubMedCentralCrossRefPubMedGoogle Scholar
  2. Anderson AR, Wanner KW, Trowell SC, Warr CG, Jaquin-Joly E, Zagatti P, Robertson H, Newcomb RD (2009) Molecular basis of female-specific odorant responses in Bombyx mori. Insect Biochem Mol Biol 39(3):189–197CrossRefPubMedGoogle Scholar
  3. Ando T, Yamakawa R (2011) Analyses of lepidopteran sex pheromones by mass spectrometry. Trends Anal Chem 30(7):990–1002CrossRefGoogle Scholar
  4. Anisimova M, Bielawski JP, Yang Z (2001) Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol 18(8):1585–1592CrossRefPubMedGoogle Scholar
  5. Baker TC (2009) Nearest neural neighbors: Moth sex pheromone receptors HR11 and HR13. Chem Senses 34(6):465–468CrossRefPubMedGoogle Scholar
  6. Baker TC, Nishida R, Roelofs WL (1981) Close-range attraction of female oriental fruit moths to herbal scent of male hairpencils. Science 214(4527):1359–1361CrossRefPubMedGoogle Scholar
  7. Bengtsson JM, Trona F, Montagné N, Anfora G, Ignell R, Witzgall P, Jacquin-Joly E (2012) Putative chemosensory receptors of the codling moth, Cydia pomonella, identified by antennal transcriptome analysis. PLoS ONE 7(2):e31620PubMedCentralCrossRefPubMedGoogle Scholar
  8. Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4(2):e20PubMedCentralCrossRefPubMedGoogle Scholar
  9. Briscoe AD, Macias-Muñoz A, Kozak KM, Walters JR, Yuan F, Jamie GA, Martin SH, Dasmahapatra KK, Ferguson LC, Mallet J, Jacquin-Joly E, Jiggins CD (2013) Female behaviour drives expression and evolution of gustatory receptors in butterflies. PLoS Genet 9:e1003620PubMedCentralCrossRefPubMedGoogle Scholar
  10. Butenandt VA, Beckmann R, Stamm D, Hecker E (1959) Über den Sexual-Lockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z Naturforsch 14:283–284Google Scholar
  11. Chapman RF (2003) Contact chemoreception in feeding by phytophagous insects. Annu Rev Entomol 48(1):455–484CrossRefPubMedGoogle Scholar
  12. Chyb S (2004) Drosophila gustatory receptors: from gene identification to functional expression. J Insect Physiol 50(6):469–477CrossRefPubMedGoogle Scholar
  13. Engsontia P, Sanderson AP, Cobb M, Walden KKO, Robertson HM, Brown S (2008) The red flour beetle’s large nose: an expanded odorant receptor gene family in Tribolium castaneum. Insect Biochem Mol Biol 38(4):387–397CrossRefPubMedGoogle Scholar
  14. Felsenstein J (1989) PHYLIP—Phylogeny Inference Package (Version 3.2). Cladistics 5:164–166Google Scholar
  15. Gao Q, Yuan B, Chess A (2000) Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 3(8):780–785CrossRefPubMedGoogle Scholar
  16. Gardiner A, Barker D, Butlin RK, Jordan WC, Ritchie MG (2008) Drosophila chemoreceptor gene evolution: selection, specialization and genome size. Mol Ecol 17(7):1648–1657CrossRefPubMedGoogle Scholar
  17. Gould F, Estock M, Hillier NK, Powell B, Groot AT, Ward CM, Emerson JL, Schal C, Vickers NJ (2010) Sexual isolation of male moths explained by a single pheromone response QTL containing four receptor genes. Proc Natl Acad Sci USA 107(19):8660–8665PubMedCentralCrossRefPubMedGoogle Scholar
  18. Grosse-Wilde E, Gohl T, Bouché E, Breer H, Krieger J (2007) Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur J Neurosci 25(8):2364–2373CrossRefPubMedGoogle Scholar
  19. Grosse-Wilde E, Kuebler LS, Bucks S, Vogel H, Wicher D, Hansson BS (2011) Antennal transcriptome of Manduca sexta. Proc Natl Acad Sci USA 108(18):7449–7454PubMedCentralCrossRefPubMedGoogle Scholar
  20. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321CrossRefPubMedGoogle Scholar
  21. Guo S, Kim J (2007) Molecular evolution of Drosophila odorant receptor genes. Mol Biol Evol 24(5):1198–1207Google Scholar
  22. Hahn MW, De Bie T, Stajich JE, Nguyen C, Cristianini N (2005) Estimating the tempo and mode of gene family evolution from comparative genomic data. Genome Res 15(8):1153–1160PubMedCentralCrossRefPubMedGoogle Scholar
  23. Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125(1):143–160CrossRefPubMedGoogle Scholar
  24. Hallem EA, Nicole Fox A, Zwiebel LJ, Carlson JR (2004) Olfaction: mosquito receptor for human-sweat odorant. Nature 427(6971):212–213CrossRefPubMedGoogle Scholar
  25. Heliconius Genome Consortium (2012) Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487(7405):94–98Google Scholar
  26. Howlett N, Dauber K, Shukla A, Morton B, Glendinning J, Brent E, Gleason C, Islam F, Izquierdo D, Sanghavi S, Afroz A, Aslam A, Barbaro M, Blutstein R, Borovka M, Desire B, Elikhis A, Fan Q, Hoffman K, Huang A, Keefe D, Lopatin S, Miller S, Patel P, Rizzini D, Robinson A, Rokins K, Turlik A, Mansfield J (2012) Identification of chemosensory receptor genes in Manduca sexta and knockdown by RNA interference. BMC Genom 13(1):211CrossRefGoogle Scholar
  27. Jacquin E, Nagnan P, Frerot B (1991) Identification of hairpencil secretion from male Mamestra brassicae (L.) (Lepidoptera: Noctuidae) and electroantennogram studies. J Chem Ecol 17(1):239–246CrossRefPubMedGoogle Scholar
  28. Kent L, Robertson H (2009) Evolution of the sugar receptors in insects. BMC Evol Biol 9:41PubMedCentralCrossRefPubMedGoogle Scholar
  29. Knipple DC, Rosenfield CL, Nielsen R, You KM, Jeong SE (2002) Evolution of the integral membrane desaturase gene family in moths and flies. Genetics 162(4):1737–1752PubMedCentralPubMedGoogle Scholar
  30. Krieger J, Raming K, Dewer YME, Bette S, Conzelmann S, Breer H (2002) A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. Eur J Neurosci 16(4):619–628CrossRefPubMedGoogle Scholar
  31. Krieger J, Grosse-Wilde E, Gohl T, Dewer YME, Raming K, Breer H (2004) Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc Natl Acad Sci USA 101(32):11845–11850PubMedCentralCrossRefPubMedGoogle Scholar
  32. Krieger J, Gondesen I, Forstner M, Gohl T, Dewer Y, Breer H (2009) HR11 and HR13 receptor-expressing neurons are housed together in pheromone-responsive sensilla trichodea of male Heliothis virescens. Chem Senses 34(6):469–477CrossRefPubMedGoogle Scholar
  33. Kristensen NP, Scoble MJ, Karsholt O (2007) Lepidoptera phylogeny and systematics: the state of inventorying moth and butterfly diversity. Zootaxa 1668:699–747Google Scholar
  34. Kurtovic A, Widmer A, Dickson BJ (2007) A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446(7135):542–546CrossRefPubMedGoogle Scholar
  35. Lassance J-M, Groot AT, Lienard MA, Antony B, Borgwardt C, Andersson F, Hedenstrom E, Heckel DG, Lofstedt C (2010) Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466(7305):486–489CrossRefPubMedGoogle Scholar
  36. Leary GP, Allen JE, Bunger PL, Luginbill JB, Linn CE, Macallister IE, Kavanaugh MP, Wanner KW (2012) Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. Proc Natl Acad Sci USA 109(35):14081–14086PubMedCentralCrossRefPubMedGoogle Scholar
  37. Legeai F, Malpel S, Montagne N, Monsempes C, Cousserans F, Merlin C, Francois M-C, Maibeche-Coisne M, Gavory F, Poulain J, Jacquin-Joly E (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(1):86CrossRefGoogle Scholar
  38. Li L, Stoeckert CJ Jr, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13(9):2178–2189PubMedCentralCrossRefPubMedGoogle Scholar
  39. Librado P, Vieira FG, Rozas J (2012) BadiRate: estimating family turnover rates by likelihood-based methods. Bioinformatics 28(2):279–281CrossRefPubMedGoogle Scholar
  40. McBride CS, Arguello JR (2007) Five drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics 177(3):1395–1416PubMedCentralCrossRefPubMedGoogle Scholar
  41. Mitchell RF, Hughes DT, Luetje CW, Millar JG, Soriano-Agatón F, Hanks LM, Robertson HM (2012) Sequencing and characterizing odorant receptors of the cerambycid beetle Megacyllene caryae. Insect Biochem Mol Biol 42(7):499–505PubMedCentralCrossRefPubMedGoogle Scholar
  42. Miura N, Nakagawa T, Tatsuki S, Touhara K, Ishikawa Y (2009) A male-specific odorant receptor conserved through the evolution of sex pheromones in Ostrinia moth species. Int J Biol Sci 5(4):319–330PubMedCentralCrossRefPubMedGoogle Scholar
  43. Miura N, Nakagawa T, Touhara K, Ishikawa Y (2010) Broadly and narrowly tuned odorant receptors are involved in female sex pheromone reception in Ostrinia moths. Insect Biochem Mol Biol 40(1):64–73CrossRefPubMedGoogle Scholar
  44. Montell C (2009) A taste of the Drosophila gustatory receptors. Curr Opin Neurobiol 19(4):345–353PubMedCentralCrossRefPubMedGoogle Scholar
  45. Nakagawa T, Sakurai T, Nishioka T, Touhara K (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307(5715):1638–1642CrossRefPubMedGoogle Scholar
  46. Niehuis O, Buellesbach J, Gibson JD, Pothmann D, Hanner C, Mutti NS, Judson AK, Gadau J, Ruther J, Schmitt T (2013) Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones. Nature 494(7437):345–348CrossRefPubMedGoogle Scholar
  47. Nozawa M, Nei M (2007) Evolutionary dynamics of olfactory receptor genes in Drosophila species. Proc Natl Acad Sci USA 104:7122–7127PubMedCentralCrossRefPubMedGoogle Scholar
  48. Pelletier J, Hughes DT, Luetje CW, Leal WS (2010) An odorant receptor from the southern house mosquito Culex pipiens quinquefasciatus sensitive to oviposition attractants. PLoS ONE 5(4):e10090PubMedCentralCrossRefPubMedGoogle Scholar
  49. Ramaekers A, Magnenat E, Marin EC, Gendre N, Jefferis GSXE, Luo L, Stocker RF (2005) Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr Biol 15(11):982–992CrossRefPubMedGoogle Scholar
  50. Ramdya P, Benton R (2010) Evolving olfactory systems on the fly. Trends Genet 26(7):307–316CrossRefPubMedGoogle Scholar
  51. Renwick JAA, Chew FS (1994) Oviposition behavior in Lepidoptera. Annu Rev Entomol 39(1):377–400CrossRefGoogle Scholar
  52. Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 16(11):1395–1403PubMedCentralCrossRefPubMedGoogle Scholar
  53. Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci USA 100(Suppl 2):14537–14542PubMedCentralCrossRefPubMedGoogle Scholar
  54. Robertson HM, Gadau J, Wanner KW (2010) The insect chemoreceptor superfamily of the parasitoid jewel wasp Nasonia vitripennis. Insect Mol Biol 19:121–136CrossRefPubMedGoogle Scholar
  55. Roelofs WL, Liu W, Hao G, Jiao H, Rooney AP, Linn CE (2002) Evolution of moth sex pheromones via ancestral genes. Proc Natl Acad Sci USA 99(21):13621–13626PubMedCentralCrossRefPubMedGoogle Scholar
  56. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574CrossRefPubMedGoogle Scholar
  57. Sahara K, Yoshido A, Traut W (2012) Sex chromosome evolution in moths and butterflies. Chromosome Res 20(1):83–94CrossRefPubMedGoogle Scholar
  58. Sakurai T, Nakagawa T, Mitsuno H, Mori H, Endo Y, Tanoue S, Yasukochi Y, Touhara K, Nishioka T (2004) Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci USA 101(47):16653–16658PubMedCentralCrossRefPubMedGoogle Scholar
  59. Sakurai T, Mitsuno H, Haupt SS, Uchino K, Yokohari F, Nishioka T, Kobayashi I, Sezutsu H, Tamura T, Kanzaki R (2011) A Single sex pheromone receptor determines chemical response specificity of sexual behavior in the silkmoth Bombyx mori. PLoS Genet 7:e1002115PubMedCentralCrossRefPubMedGoogle Scholar
  60. Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452(7190):1002–1006CrossRefPubMedGoogle Scholar
  61. Sato K, Tanaka K, Touhara K (2011) Sugar-regulated cation channel formed by an insect gustatory receptor. Proc Natl Acad Sci USA 108(28):11680–11685PubMedCentralCrossRefPubMedGoogle Scholar
  62. Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struct Dev 34(3):257–299CrossRefGoogle Scholar
  63. Scott K, Brady R Jr, Cravchik A, Morozov P, Rzhetsky A, Zuker C, Axel R (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104(5):661–673CrossRefPubMedGoogle Scholar
  64. Smadja C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102(1):77–97CrossRefPubMedGoogle Scholar
  65. Smadja C, Shi P, Butlin RK, Robertson HM (2009) Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. Mol Biol Evol 26(9):2073–2086CrossRefPubMedGoogle Scholar
  66. Smadja CM, Canback B, Vitalis R, Gautier M, Ferrari J, Zhou JJ, Butlin RK (2012) Large-scale candidate gene scan reveals the role of chemoreceptor genes in host plant specialization and speciation in the pea aphid. Evolution 66(9):2723–2738CrossRefPubMedGoogle Scholar
  67. Smith CD, Zimin A, Holt C, Abouheif E, Benton R, Cash E, Croset V, Currie CR, Elhaik E, Elsik CG, Fave MJ, Fernandes V, Gadau J, Gibson JD, Graur D, Grubbs KJ, Hagen DE, Helmkampf M, Holley JA, Hu H, Viniegra AS, Johnson BR, Johnson RM, Khila A, Kim JW, Laird J, Mathis KA, Moeller JA, Munoz-Torres MC, Murphy MC, Nakamura R, Nigam S, Overson RP, Placek JE, Rajakumar R, Reese JT, Robertson HM, Smith CR, Suarez AV, Suen G, Suhr EL, Tao S, Torres CW, van Wilgenburg E, Viljakainen L, Walden KK, Wild AL, Yandell M, Yorke JA, Tsutsui ND (2011a) Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proc Natl Acad Sci USA 108(14):5673–5678PubMedCentralCrossRefPubMedGoogle Scholar
  68. Smith CR, Smith CD, Robertson HM, Helmkampf M, Zimin A, Yandell M, Holt C, Hu H, Abouheif E, Benton R, Cash E, Croset V, Currie CR, Elhaik E, Elsik CG, Fave MJ, Fernandes V, Gibson JD, Graur D, Gronenberg W, Grubbs KJ, Hagen DE, Viniegra AS, Johnson BR, Johnson RM, Khila A, Kim JW, Mathis KA, Munoz-Torres MC, Murphy MC, Mustard JA, Nakamura R, Niehuis O, Nigam S, Overson RP, Placek JE, Rajakumar R, Reese JT, Suen G, Tao S, Torres CW, Tsutsui ND, Viljakainen L, Wolschin F, Gadau J (2011b) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci USA 108(14):5667–5672PubMedCentralCrossRefPubMedGoogle Scholar
  69. Sun M, Liu Y, Walker WB, Liu C, Lin K, Gu S, Zhang Y, Zhou J, Wang G (2013) Identification and characterization of pheromone receptors and interplay between receptors and pheromone binding proteins in the diamondback moth. PLoS ONE 8:e62098PubMedCentralCrossRefPubMedGoogle Scholar
  70. Swanson WJ, Nielsen R, Yang Q (2003) Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 20(1):18–20CrossRefPubMedGoogle Scholar
  71. Tanaka K, Uda Y, Ono Y, Nakagawa T, Suwa M, Yamaoka R, Touhara K (2009) Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr Biol 19(11):881–890CrossRefPubMedGoogle Scholar
  72. Teal PE, Tumlinson JH (1989) Isolation, identification, and biosynthesis of compounds produced by male hairpencil glands of Heliothis virescens (F.) (Lepidoptera: Noctuidae). J Chem Ecol 15(1):413–427CrossRefPubMedGoogle Scholar
  73. The International Silkworm Genome C (2008) The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem Mol Biol 38(12):1036–1045CrossRefGoogle Scholar
  74. Thompson JN, Pellmyr O (1991) Evolution of oviposition behavior and host preference in Lepidoptera. Annu Rev Entomol 36(1):65–89CrossRefGoogle Scholar
  75. Vásquez GM, Fischer P, Grozinger CM, Gould F (2011) Differential expression of odorant receptor genes involved in the sexual isolation of two Heliothis moths. Insect Mol Biol 20(1):115–124CrossRefPubMedGoogle Scholar
  76. Vieira FG, Rozas J (2011) Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol Evol 3:476–490PubMedCentralCrossRefPubMedGoogle Scholar
  77. Vogt RG, Riddiford LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293(5828):161–163CrossRefPubMedGoogle Scholar
  78. Vosshall LB (2000) Olfaction in Drosophila. Curr Opin Neurobiol 10(4):498–503CrossRefPubMedGoogle Scholar
  79. Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102(2):147–159CrossRefPubMedGoogle Scholar
  80. Wahlberg N, Wheat CW, Peña C (2013) Timing and patterns in the taxonomic diversification of Lepidoptera (butterflies and moths). PLoS ONE 8:e80875PubMedCentralCrossRefPubMedGoogle Scholar
  81. Wang G, Vásquez GM, Schal C, Zwiebel LJ, Gould F (2011) Functional characterization of pheromone receptors in the tobacco budworm Heliothis virescens. Insect Mol Biol 20(1):125–133CrossRefPubMedGoogle Scholar
  82. Wanner KW, Robertson HM (2008) The gustatory receptor family in the silkworm moth Bombyx mori is characterized by a large expansion of a single lineage of putative bitter receptors. Insect Mol Biol 17(6):621–629CrossRefPubMedGoogle Scholar
  83. Wanner KW, Anderson AR, Trowell SC, Theilmann DA, Robertson HM, Newcomb RD (2007) Female-biased expression of odourant receptor genes in the adult antennae of the silkworm. Insect Mol Biol 16(1):107–119CrossRefPubMedGoogle Scholar
  84. Wanner KW, Nichols AS, Allen JE, Bunger PL, Garczynski SF, Linn CE Jr, Robertson HM, Luetje CW (2010) Sex pheromone receptor specificity in the European corn borer moth, Ostrinia nubilalis. PLoS ONE 5(1):e8685PubMedCentralCrossRefPubMedGoogle Scholar
  85. Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452(7190):1007–1011CrossRefPubMedGoogle Scholar
  86. Yang Z (2007) PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586–1591CrossRefPubMedGoogle Scholar
  87. Yang Z, Nielsen R (2002) Codon-Substitution Models for Detecting Molecular Adaptation at Individual Sites Along Specific Lineages. Mol Biol Evol 19(6):908–917CrossRefPubMedGoogle Scholar
  88. Yang Z, Nielsen R, Goldman N, Pedersen A-MK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155(1):431–449PubMedCentralPubMedGoogle Scholar
  89. Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22(4):1107–1118CrossRefPubMedGoogle Scholar
  90. Yasukochi Y, Miura N, Nakano R, Sahara K, Ishikawa Y (2011) Sex-linked pheromone receptor genes of the European corn borer, Ostrinia nubilalis, are in tandem arrays. PLoS ONE 6(4):e18843PubMedCentralCrossRefPubMedGoogle Scholar
  91. You M, Yue Z, He W, Yang X, Yang G, Xie M, Zhan D, Baxter SW, Vasseur L, Gurr GM, Douglas CJ, Bai J, Wang P, Cui K, Huang S, Li X, Zhou Q, Wu Z, Chen Q, Liu C, Wang B, Li X, Xu X, Lu C, Hu M, Davey JW, Smith SM, Chen M, Xia X, Tang W, Ke F, Zheng D, Hu Y, Song F, You Y, Ma X, Peng L, Zheng Y, Liang Y, Chen Y, Yu L, Zhang Y, Liu Y, Li G, Fang L, Li J, Zhou X, Luo Y, Gou C, Wang J, Wang J, Yang H, Wang J (2013) A heterozygous moth genome provides insights into herbivory and detoxification. Nat Genet 45(2):220–225CrossRefPubMedGoogle Scholar
  92. Zhan S, Merlin C, Boore Jeffrey L, Reppert Steven M (2011) The monarch butterfly genome yields insights into long-distance migration. Cell 147(5):1171–1185PubMedCentralCrossRefPubMedGoogle Scholar
  93. Zhang H-J, Anderson AR, Trowell SC, Luo AR, Xiang Z-H, Xia Q-Y (2011) Topological and functional characterization of an insect gustatory receptor. PLoS ONE 6:e24111PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Patamarerk Engsontia
    • 1
  • Unitsa Sangket
    • 2
  • Wilaiwan Chotigeat
    • 2
  • Chutamas Satasook
    • 1
  1. 1.Department of Biology, Faculty of SciencePrince of Songkla UniversitySongklaThailand
  2. 2.The Center for Genomics and Bioinformatics Research, Department of Molecular Biotechnology and Bioinformatics, Faculty of SciencePrince of Songkla UniversitySongklaThailand

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