Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 35, 2012, Pages 14081-14086

  Leary, Greg P ^a,b   Allen, Jean E ^a   Bunger, Peggy L ^a   Luginbill, Jena B ^b   Linn, Charles E ^c   Macallister, Irene E ^d   Kavanaugh, Michael P ^b   Wanner, Kevin W ^a  

^a MONTANA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MONTANA   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d U S ARMY ENGINEER RESEARCH AND DEVELOPMENT CENTER   (United States)

Author keywords

Furnacalis; Nubilalis

Indexed keywords

ALANINE; ODORANT RECEPTOR 3; PHEROMONE RECEPTOR; SEX PHEROMONE; THREONINE; UNCLASSIFIED DRUG;

ANTENNA (ORGAN); ARTICLE; EUROPEAN CORN BORER; FEMALE; GENE MUTATION; IN VITRO STUDY; MALE; MOTH; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPECIES DIFFERENCE;

LEPIDOPTERA; OSTRINIA; OSTRINIA NUBILALIS; PAPILIONOIDEA;

EID: 84865546063     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1204661109     Document Type: Article

References (53)

1. Schneider D (1992) 100 years of pheromone research. Naturwissenschaften 79:241-250.
2. Kristensen NP, Scoble MJ, Karsholt OLE (2007) Lepidoptera phylogeny and systematics: The state of inventorying moth and butterfly diversity. Zootaxa 1668:699-747. (Pubitemid 351147617)
3. Cardé RT, Haynes KF (2004) Advances in Insect Chemical Ecology (Cambridge Univ Press, Cambridge, UK), 1st Ed, pp 283-332.
4. Ando T, Inomata SI, Yamamoto M (2004) Lepidopteran sex pheromones. Top Curr Chem 239:51-96.
5. Dopman EB, Robbins PS, Seaman A (2010) Components of reproductive isolation between North American pheromone strains of the European corn borer. Evolution 64:881-902.
6. Butenandt A, Beckmann R, Stamm D, Hecker E (1959) Über den sexuallockstoff des seidenspinners Bombyx mori. Reindarstellung und konstitution. Z Naturforsch B 14:283-284.
7. Dopman EB, Bogdanowicz SM, Harrison RG (2004) Genetic mapping of sexual isolation between E and Z pheromone strains of the european corn Borer (Ostrinia nubilalis). Genetics 167:301-309. (Pubitemid 38736389)
8. Roelofs W, et al. (1987) Sex pheromone production and perception in European corn borer moths is determined by both autosomal and sex-linked genes. Proc Natl Acad Sci USA 84:7585-7589.
9. Gould F, et al. (2010) Sexual isolation of male moths explained by a single pheromone response QTL containing four receptor genes. Proc Natl Acad Sci USA 107:8660-8665.
10. Lassance JM, et al. (2010) Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466:486-489.
11. Krieger J, et al. (2004) Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc Natl Acad Sci USA 101:11845-11850. (Pubitemid 39095382)
12. Nakagawa T, Sakurai T, Nishioka T, Touhara K (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307:1638-1642. (Pubitemid 40354748)
13. 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 40:64-73.
14. Wanner KW, et al. (2010) Sex pheromone receptor specificity in the European corn borer moth, Ostrinia nubilalis. PLoS ONE 5:e8685.
15. Sakurai T, et al. (2011) A single sex pheromone receptor determines chemical response specificity of sexual behavior in the silkmoth Bombyx mori. PLoS Genet 7:e1002115.
16. Fujii T, et al. (2011) Sex-linked transcription factor involved in a shift of sex-pheromone preference in the silkmoth Bombyx mori. Proc Natl Acad Sci USA 108:18038-18043.
17. Ishikawa Y, et al. (1999) Ostrinia spp. in Japan: Their host plants and sex pheromones. Entomol Exp Appl 91:237-244. (Pubitemid 29417008)
18. Frolov AN, Bourguet D, Ponsard S (2007) Reconsidering the taxomony of several Ostrinia species in the light of reproductive isolation: A tale for Ernst Mayr. Biol J Linn Soc Lond 91:49-72. (Pubitemid 46642954)
19. Kim CG, Hoshizaki S, Huang YP, Tatsuki S, Ishikawa Y (1999) Usefulness of mitochondrial COII gene sequences in examining phylogenetic relationships in the Asian corn borer, Ostrinia furnacalis, and allied species (Lepidoptera: Pyralidae). Appl Entomol Zool (Jpn) 34:405-412. (Pubitemid 129333562)
20. Cardé RT, et al. (1978) European corn borer: Pheromone polymorphism or sibling species? Science 199:555-556.
21. Ando T, Saito O, Arai K, Takahashi N (1980) (Z)- and (E)-12-Tetradecenyl acetates: Sex pheromone components of oriental corn borer (Lepidoptera: Pyralidae). Agric Biol Chem 44:2643-2649.
22. Klun JA, et al. (1980) Sex pheromone of the Asian corn borer moth. Life Sci 27:1603-1606. (Pubitemid 11220463)
23. Roelofs WL, Du JW, Tang XH, Robbins PS, Eckenrode CJ (1985) Three European corn borer populations in New York based on sex pheromones and voltinism. J Chem Ecol 11:829-836.
24. Willett CS, Harrison RG (1999) Pheromone binding proteins in the European and Asian corn borers: No protein change associated with pheromone differences. Insect Biochem Mol Biol 29:277-284. (Pubitemid 29196620)
25. Willett CS, Harrison RG (1999) Insights into genome differentiation: Pheromonebinding protein variation and population history in the European corn borer (Ostrinia nubilalis). Genetics 153:1743-1751.
26. Yang Z (1997) PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555-556.
27. Yang Z, Nielsen R (1998) Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol 46:409-418. (Pubitemid 28164945)
28. Sato K, et al. (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002-1006. (Pubitemid 351589615)
29. Wicher D, et al. (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452:1007-1011. (Pubitemid 351589619)
30. Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:e20.
31. Lundin C, et al. (2007) Membrane topology of the Drosophila OR83b odorant receptor. FEBS Lett 581:5601-5604. (Pubitemid 350186005)
32. Smart R, et al. (2008) Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem Mol Biol 38:770-780.
33. Paterson PHEH (1992) Evolution and the Recognition Concept of Species: Collected Writings (The Johns Hopkins Univ Press, Baltimore, MD), 1st Ed.
34. Phelan PL (1997) Evolution of mate signaling in moths: Phylogenetic considerations and predictions from the asymmetric tracking hypothesis. The Evolution of Mating Systems in Insects and Arachnids, eds Choe JC, Crespi BJ (Cambridge Univ Press, Cambridge, UK), pp 240-256.
35. 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 20:115-124.
36. El-Sayed AM (2003) The Pherobase - Database of Insect Pheromones and Semiochemicals (HortResearch, Lincoln, New Zealand).
37. 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 5:319-330.
38. Nielsen R, ed (2005) Statistical Methods in Molecular Evolution (Springer, New York), 1st Ed.
39. Sánchez-Gracia A, Vieira FG, Rozas J (2009) Molecular evolution of the major chemosensory gene families in insects. Heredity (Edinb) 103:208-216.
40. Dobritsa AA, van der Goes van Naters W, Warr CG, Steinbrecht RA, Carlson JR (2003) Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37:827-841.
41. Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117:965-979. (Pubitemid 38798861)
42. Hallem EA, Dahanukar A, Carlson JR (2006) Insect odor and taste receptors. Annu Rev Entomol 51:113-135. (Pubitemid 43107817)
43. Domingue MJ, Musto CJ, Linn CE, Jr., Roelofs WL, Baker TC (2008) Olfactory neuron responsiveness and pheromone blend preference in hybrids between Ostrinia furnacalis and Ostrinia nubilalis (Lepidoptera: Crambidae). J Insect Physiol 54:1261-1270.
44. Domingue MJ, Musto CJ, Linn CE, Jr., Roelofs WL, Baker TC (2010) Homology of olfactory receptor neuron response characteristics inferred from hybrids between Asian and European corn borer moths (Lepidoptera: Crambidae). J Insect Physiol 56:73-80.
45. 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:e18843.
46. Roelofs WL, et al. (2002) Evolution of moth sex pheromones via ancestral genes. Proc Natl Acad Sci USA 99:13621-13626. (Pubitemid 35215430)
47. Linn C, Jr., O'Connor M, Roelofs W (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.
48. Allen JE, Wanner KW (2011) Asian corn borer pheromone binding protein 3, a candidate for evolving specificity to the 12-tetradecenyl acetate sex pheromone. Insect Biochem Mol Biol 41:141-149.
49. Edgar RC (2004) MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113.
50. Suyama M, Torrents D, Bork P (2006) PAL2NAL: Robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34 (Web Server issue):W609-12.
51. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599. (Pubitemid 47236692)
52. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees.Mol Biol Evol 10:512-526. (Pubitemid 23157236)
53. Anisimova M, Bielawski JP, Yang Z (2001) Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol 18:1585-1592. (Pubitemid 32735106)