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Inheritance of central neuroanatomy and physiology related to pheromone preference in the male European corn borer

BACKGROUND: The European corn borer (ECB), Ostrinia nubilalis, is a textbook example of pheromone polymorphism. Males of the two strains (Z and E) prefer opposite ratios of the two pheromone components, Z11- and E11-tetradecenyl acetate, with a sex-linked factor underlying this difference in prefere...

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Autores principales: Kárpáti, Zsolt, Olsson, Shannon, Hansson, Bill S, Dekker, Teun
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2949874/
https://www.ncbi.nlm.nih.gov/pubmed/20846426
http://dx.doi.org/10.1186/1471-2148-10-286
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author Kárpáti, Zsolt
Olsson, Shannon
Hansson, Bill S
Dekker, Teun
author_facet Kárpáti, Zsolt
Olsson, Shannon
Hansson, Bill S
Dekker, Teun
author_sort Kárpáti, Zsolt
collection PubMed
description BACKGROUND: The European corn borer (ECB), Ostrinia nubilalis, is a textbook example of pheromone polymorphism. Males of the two strains (Z and E) prefer opposite ratios of the two pheromone components, Z11- and E11-tetradecenyl acetate, with a sex-linked factor underlying this difference in preference. The male antennal lobes of the two strains contain a pheromone sensitive macroglomerular complex (MGC) that is identical in morphology, but reversed in functional topology. However, hybrids prefer intermediate ratios. How a topological arrangement of two glomeruli can accommodate for an intermediate preference was unclear. Therefore we studied the neurophysiology of hybrids and paternal backcrosses to see which factors correlated with male behavior. RESULTS: Projection neuron (PN) recordings and stainings in hybrids and backcrosses show a dominance of the E-type MGC topology, notwithstanding their intermediate preference. Apparently, the topological arrangement of glomeruli does not directly dictate preference. However, two other factors did correlated very well with preference. First, volumetric measurements of MGC glomeruli demonstrate that, whereas in the parental strains the medial MGC glomerulus is more than 2 times larger than the lateral, in hybrids they are intermediate between the parents, i.e. equally sized. Paternal backcrosses showed that the volume ratio is sex-linked and co-dominant. Second, we measured the summed potential difference of the antennae in response to pheromone stimulation using electroantennogram recordings (EAG). Z-strain antennae responded 2.5 times stronger to Z11 than to E11-14:OAc, whereas in E-strain antennae the ratio was approximately equal. Hybrid responses were intermediate to the parents, and also here the antennal response of the paternal backcrosses followed a pattern similar to the behavioral phenotype. We found no differences in frequency and types of projection and local interneurons encountered between the two strains and their hybrids. CONCLUSIONS: Male pheromone preference in the ECB strains serves as a strong prezygotic reproductive isolation mechanism, and has contributed to population divergence in the field. Our results demonstrate that male pheromone preference is not directly affected by the topological arrangement of olfactory glomeruli itself, but that male preference may instead be mediated by an antennal factor, which causes the MGC glomeruli to be differentially sized. We postulate that this factor affects readout of blend information from the MGC. The results are an illustration of how pheromone preference may be 'spelled out' in the ALs, and how evolution may modulate this.
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spelling pubmed-29498742010-10-06 Inheritance of central neuroanatomy and physiology related to pheromone preference in the male European corn borer Kárpáti, Zsolt Olsson, Shannon Hansson, Bill S Dekker, Teun BMC Evol Biol Research Article BACKGROUND: The European corn borer (ECB), Ostrinia nubilalis, is a textbook example of pheromone polymorphism. Males of the two strains (Z and E) prefer opposite ratios of the two pheromone components, Z11- and E11-tetradecenyl acetate, with a sex-linked factor underlying this difference in preference. The male antennal lobes of the two strains contain a pheromone sensitive macroglomerular complex (MGC) that is identical in morphology, but reversed in functional topology. However, hybrids prefer intermediate ratios. How a topological arrangement of two glomeruli can accommodate for an intermediate preference was unclear. Therefore we studied the neurophysiology of hybrids and paternal backcrosses to see which factors correlated with male behavior. RESULTS: Projection neuron (PN) recordings and stainings in hybrids and backcrosses show a dominance of the E-type MGC topology, notwithstanding their intermediate preference. Apparently, the topological arrangement of glomeruli does not directly dictate preference. However, two other factors did correlated very well with preference. First, volumetric measurements of MGC glomeruli demonstrate that, whereas in the parental strains the medial MGC glomerulus is more than 2 times larger than the lateral, in hybrids they are intermediate between the parents, i.e. equally sized. Paternal backcrosses showed that the volume ratio is sex-linked and co-dominant. Second, we measured the summed potential difference of the antennae in response to pheromone stimulation using electroantennogram recordings (EAG). Z-strain antennae responded 2.5 times stronger to Z11 than to E11-14:OAc, whereas in E-strain antennae the ratio was approximately equal. Hybrid responses were intermediate to the parents, and also here the antennal response of the paternal backcrosses followed a pattern similar to the behavioral phenotype. We found no differences in frequency and types of projection and local interneurons encountered between the two strains and their hybrids. CONCLUSIONS: Male pheromone preference in the ECB strains serves as a strong prezygotic reproductive isolation mechanism, and has contributed to population divergence in the field. Our results demonstrate that male pheromone preference is not directly affected by the topological arrangement of olfactory glomeruli itself, but that male preference may instead be mediated by an antennal factor, which causes the MGC glomeruli to be differentially sized. We postulate that this factor affects readout of blend information from the MGC. The results are an illustration of how pheromone preference may be 'spelled out' in the ALs, and how evolution may modulate this. BioMed Central 2010-09-16 /pmc/articles/PMC2949874/ /pubmed/20846426 http://dx.doi.org/10.1186/1471-2148-10-286 Text en Copyright ©2010 Kárpáti et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Kárpáti, Zsolt
Olsson, Shannon
Hansson, Bill S
Dekker, Teun
Inheritance of central neuroanatomy and physiology related to pheromone preference in the male European corn borer
title Inheritance of central neuroanatomy and physiology related to pheromone preference in the male European corn borer
title_full Inheritance of central neuroanatomy and physiology related to pheromone preference in the male European corn borer
title_fullStr Inheritance of central neuroanatomy and physiology related to pheromone preference in the male European corn borer
title_full_unstemmed Inheritance of central neuroanatomy and physiology related to pheromone preference in the male European corn borer
title_short Inheritance of central neuroanatomy and physiology related to pheromone preference in the male European corn borer
title_sort inheritance of central neuroanatomy and physiology related to pheromone preference in the male european corn borer
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2949874/
https://www.ncbi.nlm.nih.gov/pubmed/20846426
http://dx.doi.org/10.1186/1471-2148-10-286
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