Pheromone-responsive olfactory interneurons were studied to determine the extent to which their physiological and morphological properties complemented the behavior and peripheral olfactory neurobiology observed in hybrid male moths created by interbreeding two species of heliothine moth, Heliothis virescens and Heliothis subflexa. Complete recordings were made from a total of 33 neurons, and 16 projection neurons (PNs) were subsequently stained with a fluorescent dye. Stained PNs tuned to pheromonal odorants had dendritic arborizations restricted to one of four olfactory glomeruli that together constituted the macroglomerular complex (MGC). As in parental males, PNs tuned to (Z)-11-hexadecenal always had an arbor in the cumulus, the largest of the MGC glomeruli. Previous neurophysiological investigations revealed that PNs with dendritic arbors restricted to the dorso-medial glomerulus (DM) of the MGC responded specifically to either (Z)-9-tetradecenal (Z9–14:Ald; H. virescens males) or (Z)-9-hexadecenal (Z9–16:Ald; H. subflexa males). Hybrid males, which responded equally well in wind tunnel tests to blends containing either Z9–14:Ald or Z9–16:Ald, had DM PNs that responded to both odorants. PNs specific for a third compound, (Z)-11-hexadecenol, required by hybrid males for behavioral activity were localized to the antero-medial MGC glomerulus (AM). Thus, neuronal activity across the cumulus, DM and AM glomeruli represented an attractive blend in hybrid males. Neurons tuned to (Z)-11-hexadecenyl acetate and Z9–14:Ald were restricted to a fourth, ventro-medial glomerulus. The across-glomerular pattern of activity associated with attractive pheromone blends was most similar to that of H. subflexa males, signifying a dominant effect of H. subflexa genes. These results indicate that the behavioral phenotype of hybrid males can be linked to underlying central olfactory characteristics.

Keywords:
Pheromone, Olfaction, Glomerulus, Olfactory coding, Lepidoptera, Noctuidae, Evolution
1.
Anton S, Löfstedt C, Hansson BS (1997) Central nervous processing of sex pheromones in two strains of the European corn borer Ostrinia nubilalis (Lepidoptera: Pyralidae). J Exp Biol 200:1073–1087.
2.
Baker TC (2003) Mechanism for saltational shifts in pheromone communication systems. Proc Natl Acad Sci USA 99:13368–13370.
3.
Baker TC, Ochieng’ SA, Cossé AA, Lee SG, Todd JL, Quero C, Vickers NJ (2004) A comparison of responses from olfactory receptor neurons of Heliothis subflexa and Heliothis virescens to components of their sex pheromone. J Comp Physiol A 190:155–165.
4.
Baker TC, Quero C, Ochieng’ SA, Vickers NJ (2006) Inheritance of olfactory preferences. II. Olfactory receptor neuron responses from Heliothis subflexa × Heliothis virescens hybrid male moths. Brain Behav Evol 68:75–89.
5.
Berg BG, Almaas TJ, Bjaalie JG, Mustaparta H (1998) The macroglomerular complex of the antennal lobe in the tobacco budworm moth Heliothis virescens: specified subdivision in four compartments according to information about biologically significant compounds. J Comp Physiol A 183:669–682.
6.
Berg BG, Galizia CG, Brandt R, Mustaparta H (2002) Digital atlases of the antennal lobe in two species of tobacco budworm moths, the oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female). J Comp Neurol 446:123–134.
7.
Chess A, Simon I, Cedar H, Axel R (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823–834.
8.
Cho S, Mitchell A, Refier JC, Mitter C, Poole RW, Friedlander TP, Zhao S (1995) A highly conserved gene for low-level phylogenetics: elongation factor-1 alpha recovers morphology-based tree for heliothine moths. Mol Biol Evol 12:650–656.
9.
Christensen TA, Mustaparta H, Hildebrand JG (1995) Chemical communication in heliothine moths: Parallel pathways for information processing in the macroglomerular complex of the male tobacco budworm moth Heliothis virescens. J Comp Physiol A 177:545–557.
10.
Fang QQ, Cho S, Regier JC, Mitter C, Matthews M, Poole RW, Friedlander TP, Zhao S (1997) A new nuclear gene for insect phylogenetics: DOPA decarboxylase is informative of relationships within Heliothinae (Lepidoptera:Noctuidae). Syst Biol 46:269–283.
11.
Gadenne C, Picimbon J-F, Becard J-M, Lalanne-Cassou B, Renou M (1997) Development and pheromone communication systems in hybrids of Agrotis ipsilon and Agrotis segetum (Lepidoptera: Noctuidae). J Chem Ecol 23:191–209.
12.
Goldman AL, Van der Goes van Naters W, Lessing D, Warr CG, Carlson JR (2005) Coexpression of two functional odor receptors in one neuron. Neuron 45:661–666.
13.
Hansson BS, Löfstedt C, Roelofs WL (1987) Inheritance of olfactory response to sex pheromone components in Ostrinia nubilalis. Naturwissenschaften 74:497–499.
14.
Hansson BS, Almaas TJ, Anton S (1995) Chemical communication in heliothine moths V. Antennal lobe projection patterns of pheromone-detective olfactory receptor neurons in the male Heliothis virescens (Lepidoptera: Noctuidae). J Comp Physiol A 177:535–543.
15.
Haynes KF (1997) Genetics of pheromone communication in the cabbage looper moth, Trichoplusia ni. In: Pheromone Research: New Directions(Cardé RT, Minks AK, eds), pp 525–534. New York: Chapman and Hall.
16.
Jurenka RA, Haynes KF, Adlof RO, Bengtsson M, Roelofs WL (1994) Sex pheromone component ratio in the cabbage looper moth altered by a mutation affecting the fatty-acid chain shortening reactions in the pheromone biosynthesis pathway. Insect Biochem Mol Bio 24:373–381.
17.
Linn CE Jr, Young MS, Gendle M, Glover TJ, Roelofs WL (1997) Sex pheromone blend discrimination in two races and hybrids of the European corn borer moth, Ostrinia nubilalis. Physiol Entomol 22:212–223.
18.
Löfstedt C, Hansson BS, Roelofs W, Bengtsson BO (1989) No linkage between genes controlling female pheromone production and male pheromone response in the European corn borer, Ostrinia nubilalisHübner (Lepidoptera: Pyralidae). Genetics 123:553–556.
19.
Mombaerts P (2004) Odorant receptor gene choice in olfactory sensory neurons: the one receptor-one neuron hypothesis revisited. Curr Opin Neurobiol 14:31–36.
20.
Phelan PL (1992) Evolution of sex pheromones and the role of asymmetric tracking. In: Insect Chemical Ecology: An Evolutionary Approach (Roitberg BD, Isman MB, eds), pp 265–314. New York: Chapman and Hall.
21.
Phelan PL (1997a) Evolution of mate-signaling in moths: phylogenetic considerations and predictions from the asymmetric tracking hypothesis. In: The Evolution of Mating Systems in Insects and Arachnids(Choe JC, Crespi BJ, eds), pp 240–256. Cambridge, UK: Cambridge University Press.
22.
Phelan PL (1997b) Genetic and phylogenetics in the evolution of sex pheromones. In: Pheromone Research: New Directions (Cardé RT, Minks AK), pp 563–579. New York: Chapman and Hall.
23.
Proshold FI, LaChance LE (1974) Analysis of sterility in hybrids from interspecific crosses between Heliothis virescens and H. subflexa. Ann Entomol Soc Am 67:445–449.
24.
Renou M, Gadenne C, Tauban D (1996) Electrophysiological investigations of pheromone-sensitive sensilla in the hybrids between two moth species. J Insect Physiol 42:267–277.
25.
Roelofs WL, Liu W, Hao G, Jiao H, Rooney AP, Linn Jr CE (2003) Evolution of moth sex pheromones via ancestral genes. Proc Natl Acad Sci USA 99:13621–13626.
26.
Roelofs WL, Glover T, Tang X-H, Sreng I, Robbins P, Eckenrode C, Löfstedt C, Hansson BS, Bengtsson BO (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.
27.
Roelofs WL, Hill AS, Carde RT, Baker TC (1974) Two sex pheromone components of the tobacco budworm moth, Heliothis virescens. Life Sci 14:1555–1562.
28.
Tumlinson JH, Hendricks DE, Mitchell ER, Doolittle RE, Brennan MM (1975) Isolation, identification, and synthesis of the sex pheromone of the tobacco budworm. J Chem Ecol 1:203–214.
29.
Vickers NJ (2002) Defining a synthetic pheromone blend attractive to male Heliothis subflexa under wind tunnel conditions. J Chem Ecol 28:1267–1279.
30.
Vickers NJ (2006) Inheritance of olfactory preferences. I. Pheromone-mediated behavioral responses of Heliothis subflexa × Heliothis virescens hybrid male moths. Brain Behav Evol 68:63–74.
31.
Vickers NJ, Baker TC (1997) Chemical communication in heliothine moths: Correlation between diminished responses to point-source plumes and single filaments similarly tainted with a behavioral antagonist. J Comp Physiol A 180:523–536.
32.
Vickers NJ, Christensen TA (2003) Functional divergence of spatially conserved olfactory glomeruli in two related moth species. Chem Senses 28:325–338.
33.
Vickers NJ, Christensen TA, Hildebrand JG (1998) Combinatorial odor discrimination in the brain: attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli. J Comp Neurol 400:35–56.
© 2006 S. Karger AG, Basel
2006
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.