Reversed functional topology in the antennal lobe of the male European corn borer

Abstract

SUMMARY The European corn borer Ostrinia nubilalis (Hübner) is a model of evolution of sexual communication in insects. Two pheromone strains produce and respond to opposite ratios of the two pheromone components, Z11 and E11-tetradecenylacetate. The Z-strain uses a ratio of 97:3 of Z11:E11 tetradecenylacetate, whereas the E-strain uses a ratio of 1:99. We studied how the difference in male preference correlates with differences in wiring of olfactory input and output neurons in the antennal lobe (AL). Activity-dependent anterograde staining, intracellular recording and immunocytochemistry were used to establish the structure and function of male olfactory receptor neurons (ORNs) and AL projection neurons (PNs). Physiologically characterized neurons were reconstructed using confocal microscopy of α-synapsin stained ALs. The ALs of males and females in both strains had approximately 64 glomeruli. In males the macroglomerular complex (MGC) was morphologically similar in the two strains and consisted of two major compartments, a large, medial compartment folded around a smaller,lateral one. Extensive physiological and morphological analysis revealed that in both strains the major pheromone component-specific ORNs and PNs arborize in the medial MGC glomerulus, whereas those sensitive to the minor pheromone component arborize in the lateral glomerulus. In other words, the two strains have an indistinguishable MGC morphology, but a reversed topology. Apparently,the single-gene-mediated shift that causes a radical change in behavior is located upstream of the antennal lobes, i.e. at the ORN level.

Genetic mapping of male pheromone response in the European corn borer identifies candidate genes regulating neurogenesis

“…In the Z strain, the OSNs that respond to Z11-14:OAc project their axons onto the large, medial glomerulus of the antennal lobe, and the OSNs responding to E11-14:OAc project onto the smaller, lateral glomerulus (57). In the E strain, these connections are reversed (57). In F 1 hybrids, the connections are similar to those in the E strain, but the lateral and medial glomeruli are more similar in size, and glomerular size appears to be Z-linked (58).…”

A rearrangement of the Z chromosome topology influences the sex-linked gene display in the European corn borer, Ostrinia nubilalis

“…The autosomal pheromone perception loci regulate the development of alternative forms of the male pheromone receptor sensilla. The differences in male pheromone perception are associated with the macroglomerular complex (MGC) of male antennal lobes, where MGC morphology is indistinguishable between strains while the behavioral responses to pheromone stimulation are Z-linked and differ between E and Z moths (Karpati et al 2008;Olsson et al 2010). Pheromone perception generates a predictable electrochemical response through neurons connected to the MGC (Kanzaki et al 2003).…”

Early quality assessment lessens pheromone specificity in a moth

“…Because of its high specificity, moth pheromone communication has been important in understanding species recognition and the evolutionary processes underlying signal evolution (1). In addition, owing to its simplicity, moth pheromone communication has been a prime model for odor-mediated behavior, as well as olfactory detection, processing, and blend recognition (2)(3)(4)(5)(6)). …”

“…Two strains exist, the Z and E strains, which produce and prefer opposite ratios of Z11 and E11, 97:3 and 1:99 Z11:E11, respectively. This has made this species a model for neurophysiological and evolutionary studies on blend production and preference (5,6,10). However, despite the reportedly high pheromone specificity of males, strains interbreed in the field, as sympatric populations may consist of up to 15% of hybrids (11,12).…”