Final Report Summary - EVOLNEUROETHOL (Evolutionary neuroethology of a lepidopteran species)
Insects possess a highly developed sense of smell and live, as far as they are concerned, in a world dominated by odours. The goal of this research project was to study the neuroethological basis and evolution of olfaction in insects, using European corn borer (ECB) as a model, which has two pheromone races producing and detecting opposite ratio of the two pheromone components (Z and E-race). Additionally, this species is an economically important pest in the northern hemisphere. In this project I combined morphological, neuroanatomical, physiological and behavioural methods to understand the shift in pheromone preference. Knowing that the factor underlying the dramatic shift in pheromone preference was located in the periphery, I subsequently performed a detailed analysis using intracellular recordings and neuronal stainings on hybrids and backcrosses of ECB races. 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 the glomeruli (MGC) in the brain, which are responsible for detecting pheromone components, demonstrate that, whereas in the parental races the medial MGC glomerulus is more than two times larger than the lateral, in hybrids they are intermediate between the parents. Paternal backcrosses showed that the volume ratio is sex-linked and co-dominant. Second, I measured the summed potential difference of the antennae in response to pheromone stimulation using electroantennogram recordings. Z-race antennae responded 2.5 times stronger to Z pheromone component than to E, whereas in E-race 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 behavioural phenotype. The 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. My results are an illustration of how pheromone preference may be 'spelled out' in the brain, and how evolution may modulate this.
I also carried out behavioural experiments in the wind tunnel to study the male orientation towards to pheromone. The results show that males of the ECB are not highly sensitive to ratio in every stage of orientation. Although decidedly specific during activation, males that have 'locked on' to a pheromone plume at their preferred ratio readily continue plume following along off-ratio blends. This implies that males generalise pheromone quality after initial contact. Rapid interception of pheromone filaments, such as occurs in turbulent plumes, thus may cause olfactory 'gestalts' to develop within seconds, and induce blend generalisation. The relaxation of specificity observed here may also help explain the substantial and unexpected rates of field hybridisation between two pheromone races of ECB studied whose ratios are diametrically opposite of each other. At high population densities, males that have first encountered filaments of pheromone from their own race may stray into a plume from the other race and then hybridise.
The results have importance for understanding mechanisms and constrains in insect olfaction; with significance within basic research by contributing to our general understanding of the olfactory sense, as well as in future applications within applied research, e.g. when designing biological traps for pest species.