Unbiased analysis of C. elegans behavior reveals the use of distinct turning strategies during magneticorientation

Abstract

To successfully navigate their surroundings, animals detect and orient to environmental stimuli possessing unique physical properties. Most animals can derive directional information from spatial or temporal changes in stimulus intensity (e.g. chemo- and thermo-taxis). However, some biologically relevant stimuli have constant intensity at most organismal scales. The gravitational and magnetic fields of the earth are examples of uniform stimuli that remain constant at most relevant scales. While devoid of information associated with intensity changes, the vectorial nature of these fields intrinsically encodes directional information. While much is known about behavioral strategies that exploit changes in stimulus intensity (gradients), less is understood about orientation to uniform stimuli. Nowhere is this truer than with magnetic orientation. While many organisms are known to orient to the magnetic field of the earth, how these animals extract information from the earths magnetic field remains unresolved.\n\nHere we use the nematode C. elegans to investigate behavioral strategies for orientation to magnetic fields, and compare our findings to the better characterized chemical and thermal orientation strategies. We used an unbiased cluster analysis to categorize, quantify, and compare behavioral components underlying different orientation strategies as a way to quantify and compare animal orientation to distinct stimuli. We find that in the presence of an earth-like magnetic field, worms perform acute angle turns (140-171{degrees}) that significantly improved their alignment with the direction of an imposed magnetic vector. In contrast, animals performed high amplitude turns (46-82{degrees}) that significantly increased alignment of their trajectory with the preferred migratory angle. We conclude that C. elegans orients to earth-strength magnetic fields using two independent behavioral strategies, in contrast to orientation strategies to graded stimuli. Understanding how C. elegans detects and orients to magnetic fields will provide useful insight into how many species across taxa accomplish this fascinating sensory feat.