Abstract
BackgroundThe Radical-Pair-Model postulates that the reception of magnetic compass directions in birds is based on spin-chemical reactions in specialized photopigments in the eye, with cryptochromes discussed as candidate molecules. But so far, the exact subcellular characterization of these molecules in the retina remained unknown.Methodology/Principal FindingsWe here describe the localization of cryptochrome 1a (Cry1a) in the retina of European robins, Erithacus rubecula, and domestic chickens, Gallus gallus, two species that have been shown to use the magnetic field for compass orientation. In both species, Cry1a is present exclusively in the ultraviolet/violet (UV/V) cones that are distributed across the entire retina. Electron microscopy shows Cry1a in ordered bands along the membrane discs of the outer segment, and cell fractionation reveals Cry1a in the membrane fraction, suggesting the possibility that Cry1a is anchored along membranes.Conclusions/SignificanceWe provide first structural evidence that Cry1a occurs within a sensory structure arranged in a way that fulfils essential requirements of the Radical-Pair-Model. Our findings, identifying the UV/V-cones as probable magnetoreceptors, support the assumption that Cry1a is indeed the receptor molecule mediating information on magnetic directions, and thus provide the Radical-Pair-Model with a profound histological background.
Highlights
The magnetic compass of birds was first described in the 1960s for European robins, Erithacus rubecula, a small passerine migrant [1]
For a magnetic compass based on radical pair processes, three crucial requirements must be fulfilled: (1) light has to reach the receptor molecules to induce the formation of radical pairs, (2) the arrangement of the receptor cells has to cover all spatial directions to allow the comparison of the respective singlet or triplet yields, and (3) within any one receptor cell, all receptor molecules have to be aligned in the same direction to act as a functional unit
Double labeling with the cryptochrome 1a (Cry1a) antiserum and the UV/V opsin antiserum showed that this receptor is the UV/V (SWS1) cone, which has a higher population density in robins than in chickens (Fig. 1)
Summary
The magnetic compass of birds was first described in the 1960s for European robins, Erithacus rubecula, a small passerine migrant [1]. Several hypotheses were forwarded; the one presently favored is the Radical Pair Model by Ritz and colleagues [4]: it proposes that photon absorption in specialized receptor molecules leads to an electron transfer and the formation of radical pairs These occur in two states, singlet and triplet, which are in a chemical balance that depends on the alignment of the receptor molecules in the magnetic field. For a magnetic compass based on radical pair processes, three crucial requirements must be fulfilled: (1) light has to reach the receptor molecules to induce the formation of radical pairs, (2) the arrangement of the receptor cells has to cover all spatial directions to allow the comparison of the respective singlet or triplet yields, and (3) within any one receptor cell, all receptor molecules have to be aligned in the same direction to act as a functional unit. The exact subcellular characterization of these molecules in the retina remained unknown
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