Neural coding merges sex and habitat chemosensory signals in an insect herbivore

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1760, 2013, Pages

  Trona, Federica ^a,b,e   Anfora, Gianfranco ^b   Balkenius, Anna ^a   Bengtsson, Marie ^a   Tasin, Marco ^a,b   Knight, Alan ^c   Janz, Niklas ^d   Witzgall, Peter ^a   Ignell, Rickard ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b RESEARCH AND INNOVATION CENTRE   (Italy)

^c U S DEPARTMENT OF AGRICULTURE   (United States)

^d STOCKHOLM UNIVERSITY   (Sweden)

^e MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Chemical communication; Cydia pomonella; Functional imaging; Intracellular recordings; Magic trait; Reproductive isolation

Indexed keywords

ANTENNA; BRAIN; CHEMICAL CUE; CHEMORECEPTION; FEMALE; HABITAT SELECTION; HERBIVORE; MOTH; NATURAL SELECTION; ODOR; OLFACTION; REPRODUCTIVE ISOLATION; SEX PHEROMONE; SIGNAL;

CYDIA POMONELLA; HEXAPODA; LEPIDOPTERA;

EID: 84878268549     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.0267     Document Type: Article

References (52)

1. Chittka L, Brockmann A. 2005 Perception space: the final frontier. PLoS Biol. 3, 564-568. (doi:10.1371/ journal.pbio.0030137)
2. Masse NY, Turner GC, Jefferis GSXE. 2009 Olfactory information processing in Drosophila. Curr. Biol. 19, R700-R713. (doi:10.1016/j.cub.2009.06.026)
3. Su C-Y, Menuz K, Carlson JR. 2009 Olfactory perception: receptors, cells, and circuits. Cell 139, 45-59. (doi:10.1016/j.cell.2009.09.015)
4. Murthy VN. 2011 Olfactory maps in the brain. Annu. Rev. Neurosci. 34, 233-258. (doi:10.1146/annurev-neuro-061010-113738)
5. White CS, Lambert DM, Foster SP. 1994 Chemical signals and the recognition concept. In Speciation and the recognition concept: theory and application (eds DM Lambert, H Spencer), pp. 301-326. Baltimore, MA: John Hopkins University Press.
6. Smadja C, Butlin RK. 2009 On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102, 77-97. (doi:10. 1038/hdy.2008.55)
7. Mendelson TC, Shaw KL. 2012 The (mis)concept of species recognition. Trends Ecol. Evol. 27, 421-427. (doi:10.1016/j.tree.2012.04.001)
8. Maan ME, Seehausen O. 2011 Ecology, sexual selection and speciation. Ecol. Lett. 14, 591-602. (doi:10.1111/j.1461-0248.2011.01606.x)
9. Servedio MR, Van Doorn GS, Kopp M, Frame AM, Nosil P. 2011 Magic traits in speciation: 'magic' but not rare? Trends Ecol. Evol. 26, 389-397. (doi:10. 1016/j.tree.2011.04.005)
10. Merrill RM, Wallbank RWR, Bull V, Salazar PCA, Mallet J, Stevens M, Jiggins CD. 2012 Disruptive ecological selection on a mating cue. Proc. R. Soc. B 279, 4907-4913. (doi:10.1098/rspb. 2012.1968)
11. Fordyce JA. 2010 Host shifts and evolutionary radiations of butterflies. Proc. R. Soc. B 277, 3735-3743. (doi:10.1098/rspb.2010.0211)
12. Janz N. 2011 Ehrlich and Raven revisited: mechanisms underlying codiversification of plants and enemies. Annu. Rev. Ecol. Evol. Syst. 42, 71-89. (doi:10.1146/annurev-ecolsys-102710-145024)
13. Wyatt TD. 2003 Pheromones and animal behaviour: communication by smell and taste. Cambridge, UK: Cambridge University Press.
14. Johansson BG, Jones TM. 2007 The role of chemical communication in mate choice. Biol. Rev. 82, 265-289. (doi:10.1111/j.1469-185X.2007.00009.x)
15. Landolt PJ, Phillips TW. 1997 Host plant influence on sex pheromone behaviour of phytophagous insects. Annu. Rev. Entomol. 42, 371-391. (doi:10. 1146/annurev.ento.42.1.371)
16. Reddy GVP, Guerrero A. 2004 Interactions of insect pheromones and plant semiochemicals. Trends Plant Sci. 9, 253-261. (doi:10.1016/j.tplants.2004.03.009)
17. Namiki S, Iwabuchi S, Kanzaki R. 2008 Representation of a mixture of pheromone and host plant odor by antennal lobe projection neurons of the silkmoth Bombyx mori. J. Comp. Physiol. A 194, 501-515. (doi:10.1007/s00359-008-0325-3)
18. Chaffiol A, Kropf J, Barrozo R, Gadenne C, Rospar JP, Anton S. 2012 Plant odour stimuli reshape pheromonal representation in neurons of the antennal lobe macroglomerular complex of a male moth. J. Exp. Biol. 215, 1670-1680. (doi:10.1242/ jeb.066662)
19. Deisig N et al. 2012 Differential interactions of sex pheromone and plant odour in the olfactory pathway of a male moth. PLoS ONE 7, e33159. (doi:10.1371/journal.pone.0033159)
20. Galizia CG, Rössler W. 2010 Parallel olfactory system in insects: anatomy and function. Annu. Rev. Entomol. 55, 399-420. (doi:10.1146/annurev-ento-112408-085442)
21. Trona F, Anfora G, Bengtsson M, Witzgall P, Ignell R. 2010 Coding and interaction of sex pheromone and plant volatile signals in the antennal lobe of the codling moth Cydia pomonella. J. Exp. Biol. 213, 4291-4303. (doi:10.1242/jeb.047365)
22. Witzgall P, Stelinski L, Gut L, Thomson D. 2008 Codling moth management and chemical ecology. Annu. Rev. Entomol. 53, 503-522. (doi:10.1146/ annurev.ento.53.103106.093323)
23. El-Sayed A, Gödde J, Arn H. 1999 Sprayer for quantitative application of odor stimuli. Environ. Entomol. 28, 947-953.
24. Knight AL, Light DM, Trimble RM. 2011 Identifying (E)-4,8-dimethyl-1,3,7-nonatriene plus acetic acid as a new lure for male and female codling moth (Lepidoptera: Tortricidae). Environ. Entomol. 40, 420-430. (doi:10.1603/EN10283)
25. Carlsson MA, Galizia CG, Hansson BS. 2002 Spatial representation of odors in the antennal lobe of the moth Spodoptera littoralis (Lepidoptera: Noctuidae). Chem. Senses 27, 231-244. (doi:10.1093/chemse/27.3.231)
26. Ochieng SA, Park KC, Baker TC. 2002 Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurons in male Helicoverpa zea. J. Comp. Physiol. A 188, 325-333. (doi:10.1007/s00359-002-0308-8)
27. Pregitzer P, Schubert M, Breer H, Hansson BS, Sachse S, Krieger J. 2012 Plant odorants interfere with detection of sex pheromone signals by male Heliothis virescens. Front. Cell. Neurosci. 6, 42. (doi:10.3389/fncel.2012.00042)
28. Tootoonian S, Laurent G. 2010 Electric times in olfaction. Neuron 67, 903-905. (doi:10.1016/j. neuron.2010.09.011)
29. Witzgall P, Ansebo L, Yang Z, Angeli G, Sauphanor B, Bengtsson M. 2005 Plant volatiles affect oviposition by codling moths. Chemoecology 15, 77-83. (doi:10.1007/s00049-005-0295-7)
30. Witzgall P et al. 2012 "This is not an apple"-yeast mutualism in codling moth. J. Chem. Ecol. 38, 949-957. (doi:10.1007/s10886-012-0158-y)
31. Ramdya P, Benton R. 2010 Evolving olfactory systems on the fly. Trends Genet. 26, 307-316. (doi:10.1016/j.tig.2010.04.004)
32. Bruce TJA, Pickett JA. 2011 Perception of plant volatile blends by herbivorous insects-finding the right mix. Phytochemistry 72, 1605-1611. (doi:10. 1016/j.phytochem.2011.04.011)
33. 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, 2723-2738. (doi:10.1111/ j.1558-5646.2012.01612.x)
34. Bengtsson M, Bäckman A-C, Liblikas I, Ramirez MI, Borg-Karlson A-K, Ansebo L, Anderson P, Läfqvist J, Witzgall P. 2001 Plant odor analysis of apple: antennal response of codling moth females to apple volatiles during phenological development. J. Agric. Food Chem. 49, 3736-3741. (doi:10.1021/ jf0100548)
35. Light DM et al. 2001 A pear-derived kairomone with pheromonal potency that attracts male and female codling moth, Cydia pomonella (L.). Naturwissenschaften 88, 333-338. (doi:10.1007/ s001140100243)
36. Coracini M, Bengtsson M, Liblikas I, Witzgall P. 2004 Attraction of codling moth males to apple volatiles. Entomol. Exp. Appl. 110, 1-10. (doi:10.1111/j. 0013-8703.2004.00124.x)
37. Hern A, Dorn S. 2004 A female-specific attractant for the codling moth, Cydia pomonella, from apple fruit volatiles. Naturwissenschaften 91, 77-80. (doi:10.1007/s00114-003-0484-6)
38. Phillips PA, Barnes MM. 1975 Host race formation among sympatric apple, walnut, and plum populations of the codling moth, Laspeyresia pomonella. Ann. Entomol. Soc. Am. 68, 1053-1060.
39. Pashley DP, Bush GL. 1979 The use of allozymes in studying insect movement with special reference to the codling moth, Laspeyresia pomonella L. (Olethreutidae). In Movement of highly mobile insects: concepts and methodology in research (eds RL Rabb, GG Kennedy), pp. 333-341. Raleigh, NC: North Carolina State University Press.
40. Thaler R, Brandstätter A, Meraner A, Chabicovski M, Parson W, Zelger R, Dalla Via J, Dallinger R. 2008 Molecular phylogeny and population structure of the codling moth (Cydia pomonella) in central Europe. II. AFLP analysis reflects human-aided local adaptation of a global pest species. Mol. Phylogenet. Evol. 48, 838-849. (doi:10.1016/j. ympev.2008.05.027)
41. Cisneros FH, Barnes MM. 1974 Contribution to the biological and ecological characterization of apple and walnut host races of codling moth, Laspeyresia pomonella L.: moth longevity and oviposition capacity. Environ. Entomol. 3, 402-406.
42. Piskorski R, Dorn S. 2011 How the oligophage codling moth Cydia pomonella survives on walnut despite its secondary metabolite juglone. J. Insect Physiol. 57, 744-750. (doi:10.1016/j.jinsphys.2011. 02.014)
43. Witzgall P et al. 1996 Sex pheromones and attractants in the Eucosmini and Grapholitini (Lepidoptera, Tortricidae). Chemoecology 7, 13-23. (doi:10.1007/BF01240633)
44. Grosjean Y, Rytz R, Farine JP, Abuin L, Cortot J, Jefferis GSXE, Benton R. 2011 An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478, 236-240. (doi:10.1038/ nature10428)
45. Zhang QH, Schlyter F. 2004 Olfactory recognition and behavioural avoidance of angiosperm nonhost volatiles by conifer-inhabiting bark beetles. Agric. Forest Entomol. 6, 1-19. (doi:10.1111/j.1461-9555. 2004.00202.x)
46. Karpati Z, Olsson S, Hansson BS, Dekker T. 2010 Inheritance of central neuroanatomy and physiology related to pheromone preference in the male European corn borer. BMC Evol. Biol. 10, 286. (doi:10.1186/1471-2148-10-286)
47. Lassance JM, 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, 486-489. (doi:10.1038/ nature09058)
48. Malausa T, Bethenod MT, Bontemps A, Bourguet D, Cornuet JM, Ponsard S. 2005 Assortative mating in sympatric host races of the European corn borer. Science 308, 258-260. (doi:10.1126/science. 1107577)
49. Leppik E, Frerot B. 2012 Volatile organic compounds and host-plant specialization in European corn borer E and Z pheromone races. Chemoecology 22, 119-129. (doi:10.1007/s00049-012-0104-z)
50. Witzgall P, Kirsch P, Cork A. 2010 Sex pheromones and their impact on pest management. J. Chem. Ecol. 36, 80-100. (doi:10.1007/s10886-009-9737-y)
51. Cardé RT, Minks AK. 1995 Control of moth pests by mating disruption: successes and constraints. Annu. Rev. Entomol. 40, 559-585. (doi:10.1146/annurev. ento.40.1.559)
52. Miller JR, McGhee PS, Siegert PY, Adams CG, Huang J, Grieshop MJ, Gut LJ. 2010 General principles of attraction and competitive attraction as revealed by large-cage studies of moths responding to sex pheromone. Proc. Natl Acad. Sci. USA 107, 22-27. (doi:10.1073/pnas.0908453107)