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 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.