Although many animals use the Earth's magnetic field for orientation and navigation 1,2 , the precise biophysical mechanisms underlying magnetic sensing have been elusive. One theoretical model proposes that geomagnetic fields are perceived by chemical reactions involving specialized photoreceptors 3 . But the specific photoreceptor involved in such magnetoreception has not been demonstrated conclusively in any animal. Here we show that the UV-A/blue light photoreceptor CRYPTOCHROME (CRY) is necessary for light-dependent magnetosensitive responses in Drosophila melanogaster. In a binary-choice behavioural assay for magnetosensitivity, wild-type flies exhibit significant naïve and trained responses to a magnetic field under full-spectrum light (~300-700 nm) but do not respond to the field when wavelengths in the CRY-sensitive, UV-A/blue part of the spectrum (<420 nm) are blocked. Remarkably, CRY-deficient cry 0 and cry b flies do not show either naïve or trained responses to a magnet field under full-spectrum light. Moreover, CRYdependent magnetosensitivity does not require a functioning circadian clock. Our work provides the first genetic evidence for a CRY-based magnetosensitive system in any animal.The ability of an animal to detect geomagnetic fields has substantial biological relevance as it is used by many invertebrate and vertebrate species for orientation and navigation purposes, including homing, building activity and long-distance migration 2,4 . Three general modes of magnetoreception have been proposed 5 . One mode is electromagnetic induction by the Earth's magnetic field as may occur in electrosensitive marine fish, although there is scant evidence supporting such sensing. The two other modes, for which experimental evidence does exist, are a magnetite-based process 6-8 and chemical-based reactions 9,10 that are modulated by magnetic fields. One chemical model of magnetoreception proposes that magnetic information is transmitted to the nervous system through the light-induced product of magnetically sensitive radical-pair reactions in specialized photoreceptors 3 .CRYs are flavoproteins that have been postulated to generate magnetosensitive radical pairs that could provide a photoinduced electron transfer reaction for the detection of magnetic fields 3 . CRY proteins are best known for their roles in the regulation of circadian clocks 11, 12 and can be categorized into two groups based on current phylogenetic and functional relationships 13,14 . Drosophila-like CRYs are sensitive to light in the UV-A/blue range 15 and function primarily as photoreceptors that synchronize (entrain) circadian clocks. Vertebratelike CRYs, which have also been found in every non-drosophilid insect so far examined 14 , do
Understanding the biophysical basis of animal magnetoreception has been one of the greatest challenges in sensory biology. Recently, it was discovered that the light-dependent magnetic sense of Drosophila melanogaster is mediated by the ultraviolet (UV)-A/blue light photoreceptor Cryptochrome (Cry)1. We now show using a transgenic approach that the photoreceptive, Drosophila-like Type 1 Cry and the transcriptionally repressive, vertebrate-like Type 2 Cry of the monarch butterfly (Danaus plexippus) can both function in the magnetoreception system of Drosophila and require UV-A/blue light (<420nm) to do so. The lack of magnetic responses for both Cry types under wavelengths >420 nm does not fit the widely held view that tryptophan triad-generated radical pairs mediate Cry’s ability to sense a magnetic field. We bolster this assessment using a mutant form of Drosophila and monarch Type 1 Cry and confirm that the tryptophan triad pathway does not play a critical role in magnetic transduction. Together, these results suggest that animal Crys can mediate light-dependent magnetoreception, but do so through an unconventional photochemical mechanism. This work emphasizes the utility of Drosophila transgenesis for elucidating the precise mechanisms of Cry-mediated magnetosensitivity in insects and also in vertebrates, like migrating birds.
During their fall migration, Eastern North American monarch butterflies (Danaus plexippus) use a time-compensated sun compass to aid navigation to their overwintering grounds in central Mexico. It has been assumed that the circadian clock that provides time compensation resides in the brain, although this assumption has never been examined directly. Here we show that the antennae are necessary for proper time-compensated sun compass orientation in migratory monarch butterflies, that antennal clocks exist in monarchs, and that they likely provide the primary timing mechanism for sun compass orientation. These unexpected findings pose a novel function for the antennae and open a new line of investigation into clock-compass connections that may extend widely to other insects that use this orientation mechanism.Eastern North American monarch butterflies, Danaus plexippus, undergo one of the most magnificent long-distance migrations observed in animals. Each fall in the northern United States and southern Canada, migratory monarchs travel distances up to 4000 kilometers to arrive at their overwintering grounds in central Mexico (1,2). The navigational abilities of the migrants include the use of a time-compensated sun compass (3-5). Previous studies show that a circadian clock provides the internal timing device that allows the butterflies to correct their flight orientation, relative to skylight parameters, to maintain a southerly flight bearing, as the sun moves across the sky during the day (3-5).The circadian clock mechanism in the monarch butterfly has been recently elucidated (6). It relies on a negative transcriptional feedback loop that involves the transcription factors CLOCK (CLK) and CYCLE (CYC), which drive the expression of period (per), timeless (tim) and a vertebrate-like cryptochrome, designated cry2. The translated PER, TIM and CRY2 proteins form complexes in the cytoplasm and after the appropriate time delay translocate back into the nucleus where CRY2 represses CLK:CYC-mediated transcription (6-8). A Drosophila-like CRY also exists in the butterfly, designated CRY1, which functions as a blue light photoreceptor to synchronize (entrain) the circadian clockwork to the prevailing lightdark conditions (6). Four cells in the dorsolateral region of the central brain (the pars lateralis) house the major circadian clocks in butterfly brain (6,9). # This manuscript has been accepted for publication in Science. This version has not undergone final editing. Please refer to the complete version of record at http://www.sciencemag.org/. The manuscript may not be reproduced or used in any manner that does not fall within the fair use provisions of the Copyright Act without the prior, written permission of AAAS.Correspondence to: Steven M. Reppert. Summary: The antennae contain circadian clocks that provide a timing mechanism for time-compensated sun compass orientation.
Humans are not believed to have a magnetic sense, even though many animals use the Earth's magnetic field for orientation and navigation. One model of magnetosensing in animals proposes that geomagnetic fields are perceived by light-sensitive chemical reactions involving the flavoprotein cryptochrome (CRY). Here we show using a transgenic approach that human CRY2, which is heavily expressed in the retina, can function as a magnetosensor in the magnetoreception system of Drosophila and that it does so in a light-dependent manner. The results show that human CRY2 has the molecular capability to function as a light-sensitive magnetosensor and reopen an area of sensory biology that is ready for further exploration in humans.
Recent studies of the iconic fall migration of monarch butterflies have illuminated the mechanisms behind the navigation south, using a time-compensated sun compass. Skylight cues, such as the sun itself and polarized light, are processed through both eyes and likely integrated in the brain's central complex, the presumed site of the sun compass. Time compensation is provided by circadian clocks that have a distinctive molecular mechanism and that reside in the antennae. Monarchs may also use a magnetic compass, because they possess two cryptochromes that have the molecular capability for light-dependent magnetoreception. Multiple genomic approaches are being utilized to ultimately identify navigation genes. Monarch butterflies are thus emerging as an excellent model organism to study the molecular and neural basis of long-distance migration.
Parasitic infection can influence a variety of behavioural mechanisms in animals, but little is known about the effects of infection on the cognitive processes underlying ecologically relevant behaviours. Here, we examined whether parasitic infection alters cognitive aspects of foraging in a social insect, the bumble-bee (Bombus impatiens). In controlled experiments, we assessed the ability of foraging bees to discriminate rewarding from non-rewarding flowers on the basis of colour and odour. We found that natural and experimental infection by a protozoan parasite (Crithidia bombi, which lives exclusively within the gut tract), impaired the ability of foragers to learn the colour of rewarding flowers. Parasitic infection can thus disrupt central nervous system pathways that mediate cognitive processes in bumble-bees and as a consequence, can reduce their ability to monitor floral resources and make economic foraging decisions. It is postulated that this infection-induced change to cognitive function in bumble-bees is the result of communication between immune and nervous systems. Parasitized animals, including invertebrates, can therefore show subtle behavioural changes that are nonetheless ecologically significant and reflect complex mechanisms.
Convincing evidence that migrant monarch butterflies (Danaus plexippus) use a magnetic compass to aid their fall migration has been lacking from the spectacular navigational capabilities of this species. Here we use flight simulator studies to show that migrants indeed possess an inclination magnetic compass to help direct their flight equatorward in the fall. The use of this inclination compass is light-dependent utilizing ultraviolet-A/blue light between 380 and 420 nm. Notably, the significance of light <420 nm for inclination compass function was not considered in previous monarch studies. The antennae are important for the inclination compass because they appear to contain light-sensitive magnetosensors. For migratory monarchs, the inclination compass may serve as an important orientation mechanism when directional daylight cues are unavailable and may also augment time-compensated sun compass orientation for appropriate directionality throughout the migration.
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