The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection in vertebrates

Abstract

Theoretical models implicating specialized photoreceptors in the detection of the geomagnetic field have been the impetus for studying the effects of light on magnetic compass orientation. Magnetic orientation in flies, amphibians and birds has been found to be influenced by light, and in all these groups a shift of approximately 90 degrees in the direction of magnetic compass orientation has been observed under certain wavelengths and/or intensities of light. In the eastern red-spotted newt Notophthalmus viridescens, wavelength-dependent effects of light on magnetic compass orientation appear to result from an antagonistic interaction between short-wavelength (< or = 450 nm) and long-wavelength (> or = 500 nm) photoreception mechanisms. We have demonstrated that at least the short-wavelength input to the newt's magnetic compass is mediated by extraocular photoreceptors located in or near the pineal organ, and here we present new findings that indicate that the putative long-wavelength mechanism is also associated with pineal photoreceptors. Interestingly, the amphibian pineal organ mediates orientation to both the e-vector of plane-polarized light and the magnetic field. Although the wavelength-dependence of the polarized light orientation in amphibians has not been studied, polarization sensitivity in fishes appears to be mediated by two antagonistic photoreception mechanisms that have similar spectral characteristics to those of the newts' magnetic compass response. These parallels, along with similarities in the types of receptors that are expected to be involved in light-dependent magnetoreception and polarized light detection, suggest that similar photoreception mechanisms may mediate the light-dependent magnetic and polarized light compasses.