Radek Netušil

Cryptochrome 2 mediates directional magnetoreception in cockroaches

Significance The photosensitive protein Cryptochrome (Cry) is involved in the detection of magnetic fields (MFs) in Drosophila. However, Cry-dependent responses to natural MF intensities and to the direction of the MF vector have not been demonstrated previously in any insect. Birds, monarch butterflies, and many other species perceive the direction of geomagnetic field (GMF) lines, but the involvement of Cry has not been rigorously proven using genetic tools. In this study, by combining behavioral and genetic approaches, we provide the first unambiguous evidence to our knowledge of a Cry-dependent sensitivity to the direction of GMF in two cockroach species. Furthermore, by eye-covering experiments and by immunolocalization of a crucial mammalian-type Cry2 under the retina, we clearly show that the eye is an indispensable organ for the directional GMF response. The ability to perceive geomagnetic fields (GMFs) represents a fascinating biological phenomenon. Studies on transgenic flies have provided evidence that photosensitive Cryptochromes (Cry) are involved in the response to magnetic fields (MFs). However, none of the studies tackled the problem of whether the Cry-dependent magnetosensitivity is coupled to the sole MF presence or to the direction of MF vector. In this study, we used gene silencing and a directional MF to show that mammalian-like Cry2 is necessary for a genuine directional response to periodic rotations of the GMF vector in two insect species. Longer wavelengths of light required higher photon fluxes for a detectable behavioral response, and a sharp detection border was present in the cyan/green spectral region. Both observations are consistent with involvement of the FADox, FAD•− and FADH– redox forms of flavin. The response was lost upon covering the eyes, demonstrating that the signal is perceived in the eye region. Immunohistochemical staining detected Cry2 in the hemispherical layer of laminal glia cells underneath the retina. Together, these findings identified the eye-localized Cry2 as an indispensable component and a likely photoreceptor of the directional GMF response. Our study is thus a clear step forward in deciphering the in vivo effects of GMF and supports the interaction of underlying mechanism with the visual system.

How swift is Cry-mediated magnetoreception? Conditioning in an American cockroach shows sub-second response.

Diverse animal species perceive Earth’s magnetism and use their magnetic sense to orientate and navigate. Even non-migrating insects such as fruit flies and cockroaches have been shown to exploit the flavoprotein Cryptochrome (Cry) as a likely magnetic direction sensor; however, the transduction mechanism remains unknown. In order to work as a system to steer insect flight or control locomotion, the magnetic sense must transmit the signal from the receptor cells to the brain at a similar speed to other sensory systems, presumably within hundreds of milliseconds or less. So far, no electrophysiological or behavioral study has tackled the problem of the transduction delay in case of Cry-mediated magnetoreception specifically. Here, using a novel aversive conditioning assay on an American cockroach, we show that magnetic transduction is executed within a sub-second time span. A series of inter-stimulus intervals between conditioned stimuli (magnetic North rotation) and unconditioned aversive stimuli (hot air flow) provides original evidence that Cry-mediated magnetic transduction is sufficiently rapid to mediate insect orientation.