Behavioral Investigation of the Light-Dependent Magnetoreception Mechanism of Drosophila melanogaster
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Abstract
Use of a magnetic compass has been demonstrated in all major classes of vertebrates as well as several classes of invertebrates, and is proposed to involve a photo-induced radical pair mechanism (RPM). My dissertation research consisted of characterizing a magnetic compass in a model species, Drosophila melanogaster. Preliminary experiments were carried out with adult flies, however, due to the behavioral complexity of adult responses a new behavioral assay of magnetic compass orientation was developed using larval Drosophila that elicits a robust magnetic compass response in a trained magnetic direction. This manuscript describes experiments that were conducted showing that larval magnetic compass orientation: 1) demonstrates a complex 3-dimensional pattern of response consistent with a RPM; 2) is consistent with a receptor mechanism that utilizes short- and long-wavelength antagonistic photopigments, proposed to explain wavelength dependent effects in vertebrates (e.g. amphibians and birds); and 3) produces axially symmetrical patterns of response with respect to the geomagnetic field. Additionally, tests of adult Drosophila under low and high intensities of monochromatic long wavelength light revealed a similar behavioral response to varying intensities of monochromatic light as previously reported in migratory birds (E. rubecula). These findings indicate that the magnetic compass of larval Drosophila shares a common functional architecture and similar biophysical mechanism with that of at least some vertebrates (e.g. amphibians and possibly birds), suggesting that the magnetic compass of modern vertebrates may have evolved once in a common ancestor of these three lineages over 450 million years ago. Furthermore, findings indicating a spontaneous preference for magnetic directions in D. melanogaster larvae suggest that a light-dependent magnetoreception mechanism is more widespread in insects than was previously suspected. The development of a behavioral assay to study the light-dependent magnetic compass in an organism with a simple nervous system, a limited behavioral repertoire, and with the possibility of using the full power of modern molecular and genetic techniques holds considerable promise to increase our understanding of the biophysical mechanism(s) and neurophysiological structures underlying magnetic orientation in terrestrial animals.