Magnetoreception-A sense without a receptor

Abstract

Evolution has equipped life on our planet with an array of extraordinary senses, but perhaps the least understood is magnetoreception. Despite compelling behavioral evidence that this sense exists, the cells, molecules, and mechanisms that mediate sensory transduction remain unknown. So how could animals detect magnetic fields? We introduce and discuss 3 concepts that attempt to address this question: (1) a mechanically sensitive magnetite-based magnetoreceptor, (2) a light-sensitive chemical-based mechanism, and (3) electromagnetic induction within accessory structures. In discussing the merits and issues with each of these ideas, we draw on existing precepts in sensory biology. We argue that solving this scientific mystery will require the development of new genetic tools in magnetosensitive species, coupled with an interdisciplinary approach that bridges physics, behavior, anatomy, physiology, molecular biology, and genetics.

Fig 1. Animals that undertake astonishing journeys.

Image of an (A) arctic tern (Sterna paradisaea), (B) a loggerhead turtle (Caretta caretta), and (C) a rock pigeon (Columba livia). (D) Representation of the Earth that shows the journeys undertaken by these 3 species. White tracks show the migratory route of the arctic tern. Greenlandic colonies leave their breeding grounds (white circle) in August and follow migratory routes along the Brazilian coast to spend the austral Winter (December to April) in regions of the Antarctica (white square). Purple tracks show the migratory route of loggerhead turtles) that hatch off the east coast of Florida (purple line), circle the North Atlantic gyre, before returning to the very same stretch of coastline for nesting. Yellow track shows the homing range of a pigeon (approximately 500 km), around the city of Paris, France.

Fig 2. Three mechanisms proposed to underlie the magnetic sense.

(A) Image depicting a mechanically sensitive magnetite-based magnetoreceptor. Magnetite crystals (shown here as a chain) are attached to the plasma membrane via a cytoskeletal linker. This linear arrangement of single-domain crystals attempts to align with the Earth's geomagnetic field (like a compass needle), and thereby exerts a torque force on a mechanosensitive channel (shown in teal). This transiently activates the channel leading to cation influx (red arrow) and membrane depolarization. (B) Diagram showing a light-sensitive chemical-based magnetoreceptor. Blue light (shown with a blue arrow) induces the formation of long-lived radical pairs between Cry and the cofactor FAD. The spin state of these electrons interconverts between an antiparallel (↑↓) or parallel (↓↓) state, depending on the local magnetic environment. This, in turn, influences the biochemical or structural properties of Cry, resulting in the activation of an unknown signaling molecule (X) that modulates ion channel permeability. (C) Magnetoreception based on electromagnetic induction. This hypothesis relies on an accessory structure that transforms magnetic stimuli into an electrical information. Depicted is one semicircular canal of a vertebrate, filled with cation-rich endolymph, and sensory cells located on either side of the cupula (shown in orange). If the animal moves so that rotation occurs around an axis in the plane of a semicircular canal, there will be no displacement of the endolymph but electromagnetic induction could occur. Depending on the intensity and orientation of the external magnetic field, this will induce an electromotive force in the conductive endolymph. This results in the separation of charges within the circuit, inducing cation influx through highly sensitive voltage-gated ion channels (shown in teal). Cry, cryptochrome; FAD, flavin adenine dinucleotide.