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Response to comment on "Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans"

  1. Andres Vidal-Gadea  Is a corresponding author
  2. Chance Bainbridge
  3. Ben Clites
  4. Bridgitte E Palacios
  5. Layla Bakhtiari
  6. Vernita Gordon
  7. Jonathan Pierce-Shimomura  Is a corresponding author
  1. Illinois State University, United States
  2. University of Texas at Austin, United States
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Cite as: eLife 2018;7:e31414 doi: 10.7554/eLife.31414

Abstract

Many animals can orient using the earth’s magnetic field. In a recent study, we performed three distinct behavioral assays providing evidence that the nematode Caenorhabditis elegans orients to earth-strength magnetic fields (Vidal-Gadea et al., 2015). A new study by Landler et al. suggests that C. elegans does not orient to magnetic fields (Landler et al., 2018). They also raise conceptual issues that cast doubt on our study. Here, we explain how they appear to have missed positive results in part by omitting controls and running assays longer than prescribed, so that worms switched their preferred migratory direction within single tests. We also highlight differences in experimental methods and interpretations that may explain our different results and conclusions. Together, these findings provide guidance on how to achieve robust magnetotaxis and reinforce our original finding that C. elegans is a suitable model system to study magnetoreception.

https://doi.org/10.7554/eLife.31414.001

Introduction

We recently asked whether the nematode Caenorhabditis elegans was capable of magnetic orientation (Vidal-Gadea et al., 2015). C. elegans has proven historically important for the discovery of molecules used to sense odors, mechanical force, osmolarity, and humidity (Sengupta et al., 1996; O'Hagan et al., 2005; Colbert et al., 1997; Russell et al., 2014). Notably, each of these molecules share conserved functions in higher animals (Tobin and Bargmann, 2004; Arnadóttir and Chalfie, 2010; Filingeri, 2015). If C. elegans displays magnetoreception, potentially conserved molecular bases for this sensory modality may be studied using similar approaches. Using three distinct behavioral assays, we discovered that this tiny worm could orient its movement to artificial magnets or to the earth’s magnetic field (Vidal-Gadea et al., 2015).

More recently, Landler et al., 2018 performed additional sets of behavioral experiments to confirm whether C. elegans orients to magnetic fields. They reported negative results for all three experiments and conclude that C. elegans is not a suitable model system to study the molecular basis for magnetoreception. On first inspection, the experiments done by Landler et al., 2018 resemble those from our study with additional levels of control. However, there are important differences in their experimental methods, controls, and execution which might have contributed to their negative results.

Landler et al., 2018 also raised conceptual issues with our findings and interpretations. First, they suggest that C. elegans should not be able to orient to the strong magnetic field used in our magnetotaxis assay. Second, they suggest that a tentative explanatory hypothesis that we put forward– that C. elegans strains isolated from different locations on the globe may migrate at a specific angle to the magnetic field, perhaps as a way to orient optimally up or downwards when burrowing is infeasible. We address the first issue by showing that the magnetic field provides directional information in our magnetotaxis assay, allowing us to predict the unusual tracks they made in our original 2015 study. We finish by identifying plausible mechanisms for how worms may use the directional information provided by a magnetic field to migrate along a specific vector.

Results and discussion

Overt differences in experimental methods

Landler et al. attempted to reproduce our results with British worms by performing modified versions of three of our experiments. These modifications included worthwhile control measures and analysis that differed slightly from our original study. Unfortunately, it appears many of these experiments deviated from our described methods. For each experiment, they found negative results concluding that C. elegans may not orient to magnetic fields. Below, we discuss differences in experimental methods, analysis, and interpretation that may explain their failure to match our results.

Animal satiation states

One of the major differences between our methods and theirs was in the duration of the assays. In Vidal-Gadea et al., 2015 we experimentally determined and reported that 30 min away from food was sufficient to flip the magnetotaxis behavior of the worms from positive to negative. This was initially unexpected, because C. elegans does not flip its orientation preference after 30 min away from food for other orientation behaviors including chemotaxis to benzaldehyde. We therefore described this time as sufficient to induce the ‘starved’ state in animals, and went on to perform several experiments with worms in the ‘fed’ or ‘starved’ states. For ‘starved’ assays, we ensured that worms were away from food for 30 min prior to starting an experiment. From reading Landler et al., 2018 it is now clear that we did not explicitly mention that this definition of starvation implied that for worms to be tested in the ‘fed’ state, animals would need to complete their assay within 30 min.

With practice, we found that we could run our behavioral assays to near completion within this 30 min time window and did not need to immediately tally immobilized animals. This allowed us to run many assays in parallel without having to stop to conduct the time-consuming tallying step for each pipette or plate before starting the next. Tallying animals in the magnetotaxis assay, however, was a much simpler (and faster) procedure, which we could do at the 30 min mark. Therefore, it is important to note that we ran assays so that worms migrated to a particular direction within 30 min of initial removal from seeded growth plate.

It is clear from Landler et al., 2018 that they decided to modify our magnet assay to last 60 min rather than 30 min precisely because they continued to see moving animals all the way until this time point (see their Methods). Unfortunately, this also implies that many worms participating in the assay (which they described was a sufficiently large number to make them deviate from our protocol) would have transitioned to the ‘starved’ state. By our described definition of ‘fed’ and ‘starved’ (also adopted by Landler et al.) they report testing animals under both ‘fed’ (first half of the assay), and ‘starved’ (second half of the assay) conditions. This issue may have been obviated when Landler et al. tested pre-starved worms (their Figure 3B); however, no-magnet controls and horizontal-oriented tube controls for these assays were not reported (see below). We believe this singular, and crucial, difference might explain their different results.

Animal rearing

A second major difference between our methods involved the rearing conditions for our animals. Like many C. elegans labs, our worms were grown in laboratories maintained at 20°C. We deliberately kept animals away from artificial magnetic fields (generated by electrical equipment or wiring). Landler et al. grew their animals in incubators. This attempt at controlled culturing could have accidentally grown their animals under extreme magnetic and electric fields conditions generated by their incubators. This is not trivial. Recent studies demonstrated that extreme magnetic inhomogeneities are produced within these type of devices (Makinistian and Belyaev, 2018). For example, animals cultured mere centimeters apart would be exposed to fields differing by up to a factor of 36. This includes hypomagnetic field areas, where the absence of magnetic fields might affect the development of magnetic organs. Therefore, it appears that while rearing animals at 20°C Landler et al. might have unintentionally cultured animals under wildly variable magnetic conditions. This method might also produce preferences for a cultivation temperature in animals that could confound behavior when they are tested in a chamber with a different ambient temperature. We are not certain of what effect these conditions might produce in the magnetic machinery or behavior of worms, however we think it prudent to control magnetic exposure of animals to be used in magnetic studies.

Additional differences in experimental methods

We next describe additional differences between our experiments that might have further contributed to their observations.

Burrowing assay

Landler et al., 2018 assayed whether N2 worms injected into agar-filled cylinders burrowed up or down. They report no bias for burrowing up or down, with or without an imposed inverted magnetic field.

The magnetic coil systems used in the two studies differ. In our 2015 study, we used three sets of four-coil systems described by Merritt (Merritt et al., 1983) which was reported to produce more stable test fields for larger samples (e.g. 50 vs 20 cm3) than with the Helmholtz loops (Kirschvink, 1992; Magdaleno-Adame et al., 2010) used by Landler et al., 2018. Before we conducted our burrowing assays inside our magnetic coil system, we measured the field properties throughout the test volume to ensure that our system produced a homogeneous field. Landler et al. (2017) did not report such measurements of homogeneity.

Landler et al., 2018 suggested that unintended temperature gradients generated by our coil system may have resulted in our reported observations. However, aware of this possibility, we used high sensitivity thermometers (0.01°C) to quantify temperature changes (in both magnet, and magnetic coil system assays). A two-way ANOVA (N = 5, p=0.123) showed no significant difference in temperature between cancelled field and one-earth field (Figure 2—figure supplement 1 in Vidal-Gadea et al., 2015). As an extra precaution, we regularly rotated the orientation of our magnetic coil system to a random position before each assay, and used a small fan to circulate air through the coil to prevent temperature gradients. While clearly understanding the risk of unintended thermal gradients, Landler et al., 2018 do not describe doing any such controls and they do not present associated temperature measurements. However, from their discussion they seem to believe that the use of double wrapped coils prevents the generation of meaningful temperature gradients. This is incorrect; all current passing through a metal conductor generates heat. Therefore, under both their test and control conditions, heat would be generated by current passing through their system, potentially building up within the small enclosed metal room used to shield worms from foreign magnetic fields. We welcome their additional control of a mu-metal shielded room as an improvement to minimize potential magnetic contamination, but caution that environmental parameters should be controlled further by positioning the coil system at random orientations within the room, and by empirically measuring and mitigating the thermal gradients that must necessarily develop as current powers any coil system as we did in our original study.

Our burrowing experiments tested in the natural earth field showed that worms migrated differentially based on their global site of origin and satiation state. This observation undermines the likelihood of temperature gradients, or magnetite contamination, being responsible for our results. Furthermore, our findings that worms lacking the transduction channel encoded by the tax-4 gene, or by worms with genetically ablated AFD neurons, failed to burrow preferentially up or down in earth’s natural field strongly point to the involvement of these neurons and molecules in this behavior (Vidal-Gadea et al., 2015). None of these results are mentioned in Landler et al., 2018.

Horizontal plate assay

Landler et al., 2018 tested how worms migrate to the edge of a 10 cm diameter plate in a horizontal magnetic field where they were trapped by azide at the edge. Unlike our study, they found no significant degree of orientation in their migration.

In Landler et al., 2018, they point out that we treated each worm as an individual in our horizontal field assays when performing statistical analysis, which could cause a type one error if worms did not act independently. While we believe that the individual timing and trajectory of each worm makes them independent, which justified our choice of statistical analysis, we nevertheless re-analyzed our data averaging the mean heading of worms in each assay as they did. Similar to our previous report, we found that in all but one out of 28 assays, worms displayed a significant migratory preference (Figure 1). The average heading of the assays changed somewhat from the result reported in Vidal-Gadea et al., 2015, but not significantly so.

Reanalysis of population data from horizontal field assay in Vidal-Gadea et al., 2015 confirms strong orientation with respect to imposed magnetic field.

Well-fed N2 worms were placed in the center of a 10 cm diameter plate and allowed to migrate freely for 30 min as an earth-strength magnetic field was imposed across the surface of the plate. Worms were trapped by sodium azide at the perimeter. The vector averages for each of the 28 assays (black lines) are plotted as well as the average of these vectors (red line). Vector average values are listed on right. This analysis found a significantly biased vector average of 94.7° (p<0.0001) that was not statistically different from our previously reported value of 132° based on the analysis of individual worms.

https://doi.org/10.7554/eLife.31414.002

Landler et al., 2018 also noted that all worms in their magnetic field conditions are set by an experimenter not involved in the analysis. This blinding protocol was also the case for our original study, but not explicitly mentioned. Anecdotally, we expected British worms to migrate towards magnetic north, just like magnetotactic bacteria, but remained puzzled for months when our results unexpectedly showed them consistently migrating at a 132° angle with respect to magnetic north. This illustrates how our expectations did not affect our analysis or results. Indeed, we still do not know why worms prefer this particular angle, although we presented a parsimonious explanation that worms may choose a migratory direction based on the inclination of their native field.

Magnetotaxis assay

Landler et al. also performed a modified version of our magnetotaxis assay, reporting that worms exhibited no preference for the magnet when compared with a Wilcoxon signed rank test to a control group (although the control group is not described or plotted in their manuscript). However, Landler et al. chose to extend their assay time. We feel it is unacceptable that they fail to display their control data due to implications described below.

In their manuscript, Landler et al., 2018 offered no actual replication for our magnetotaxis experiments, opting instead for modified protocols. For example, Landler et al. chose to extend their assay time to one hour to include worms that may have switched to a starved state. As described above, it is therefore likely that by testing fed and starved animals alongside one another, they effectively combined and measured positive and negative magnetotaxis.

Landler et al. conducted an additional control in the form of a magnetic assay with worms fed 1% magnetite throughout their cultivation. They reported a barely significant (p<0.04) improvement over chance performance data that they chose not to plot; however, their assay was still not significantly different from animals not fed iron that migrated in the presence of a magnet. Their observation that worms contaminated with magnetite fail to migrate to a magnet as readily as in our assays, coupled with the lack of significant difference between their ‘contaminated’ vs ‘uncontaminated’ samples provides strong evidence that contamination with magnetite is likely not responsible for our observations. However, we take this conclusion with caution since their one-hour assay might have masked potentially significant effects arising from their magnetite enrichment.

Magnetite is pervasive in soils adjacent to the decaying fruit and plant matter where worms live (Stanjek et al., 1994; Moskowitz, 1995; Schulenburg and Félix, 2017; Schulenburg and Félix, 2017). It is likely that worms in their natural habitat may have access to much greater amounts of iron than those provided for them in the lab via a diet of E. coli on an agar surface. If C. elegans does use magnetite to build its own magnetic field detector, it is possible that enrichment of the lab culture conditions may result in increased magnetic indices for adults, or even succeed in enabling larval stage worms to perform this behavior better than what we previously reported (Bainbridge et al., 2016). While we consider this experiment informative, we do not agree with Landler et al., 2018 in their suggestion that ingestion of magnetic particles might confer the ability to migrate within magnetic fields to C. elegans. This would not explain how worms migrate at different angles in a satiety-dependent manner, or that this behavior can be systematically abolished and rescued by cellular and molecular tinkering. To our knowledge, ingestion of magnetite or iron is yet to be demonstrated in any animal to be sufficient to confer the ability to migrate towards and/or away from magnets using their own power. Thus, although exogenous iron has been suggested to contaminate cells proposed to be magnetoreceptors (e.g. Edelman et al., 2015), in contrast to Landler et al., 2018 claim, there is no example of false positives associated with actual magnetoreceptive behavior or physiology displayed by any wild-type animal. Additionally, in our initial study, we tested more than 30 mutants with impairments in a broad range known sensory modalities that C. elegans has been shown to detect (including temperature, electric fields, soluble and volatile chemicals, touch, light, osmolality, acidity, water, CO2, and O2). Only mutants related to AFD function were unable to orient to magnetic fields (Supplementary file 1).

One important control provided in our manuscript but left out in Landler et al., 2018 was the response of worms in the absence of a magnet. In their Figure 3F the authors display results for two assays in which worms are in the presence of a magnet, with the only difference being whether or not their diet was enriched with magnetite. No control assays where worms tested in the absence of a magnet are provided. Additionally, worms tested with a magnet are confusingly labelled ‘baseline’. We find the omission of this no-magnet control, and the nomenclature used, concerning. Based on our experience, fed worms display magnetotaxis indices with high positive values, and starved worms display indices with high negative values. If Landler et al. inadvertently combined in effect starved and fed worms in their assays, then we expect them to observe a broad range of magnetotaxis indices with an average centered at zero. These results would starkly differ from control assays with no magnet, where indices would more tightly cluster around zero (Vidal-Gadea et al., 2015). If their no-magnet control data are significantly more narrowly distributed around zero than their test data, this would suggest that the broad distribution of indices obtained in their magnet assays is likely the result of combining fed and starved animals that are in fact orienting to the magnetic field, but in opposite directions thus resulting in an average calculated index of zero.

To investigate the possibility that Landler et al. had obtained positive results that were masked by testing worms in both fed and starved states, we reanalyzed their data. First, we plotted their original results from Figure 3F in bar format alongside results from our original study including our no-magnet control (Figure 2A). Next, to control for satiation dependent reversals in magnetotaxis preferences, we plotted the absolute value of magnetotaxis indices (Figure 2B). With this alternative analysis, we found that worms migrating in the presence of a magnet displayed a significant migratory bias when compared to worms migrating in the absence of a magnet (Figure 2B). Landler et al., 2018 reported that their magnetite-enriched worms did not migrate significantly better than worms that were not fed magnetite (p=0.652). Our reanalysis confirms their finding, but also shows that their worms in both test conditions displayed a significant difference from our no-magnet control. We also reanalyzed burrowing data plotted in Figure 3B and Figure 3—figure supplement 1 from Landler et al., 2018. Once again, we provided missing controls in the form of worms burrowing in horizontally oriented pipettes and compared these to data from both groups (Figure 2C&D). We found an identical pattern of results where the absolute value of the burrowing index values for all six test group worms were higher than our horizontal control worms with three of the four groups showing significant differences (Figure 2D, Mann-Whitney Rank Sum Test). Importantly, our reanalysis suggests that had no-magnet, or horizontal controls been included and analyzed by Landler et al., they would have obtained positive results for magnetic orientation in C. elegans.

Reanalysis of data suggests that positive results may have been masked in Landler et al., 2018 by testing worms in both fed and starved states and omitting controls.

(A) Comparison of magnetotaxis data reported by Vidal-Gadea et al., 2015 and Landler et al., 2018 obtained by measuring their plots. Figure 3B and F, and Figure 3B, Figure 3—figure supplement 1 were reproduced from Landler et al., 2018; published under the terms of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/4.0/)). Because Landler et al. omitted no-magnet control data, we used no-magnet control data from Vidal-Gadea et al., 2015. We found that Landler et al., 2018 worms fed OP50 bacteria (or OP50 plus 1% magnetite) show no significant orientation versus no-magnet control worms. (B) Under the hypothesis that Landler et al might have combined fed and starved worms because their assays were run for twice as long, we used the absolute value of the magnetotaxis index to reveal evidence that worms display a biased migration in the presence of a magnetic field (irrespective of the towards or away sign of their migration). We found that both magnet treatments in Landler et al., 2018 resulted in significantly biased migration when compared with no-magnet controls. (C) We also analyzed burrowing data from Landler et al., 2018 and used our horizontal controls because they were omitted in Landler et al., 2018. We demonstrate that combining data from fed and starved worm abolished significant burrowing indexes that were otherwise observed from each of these populations. Similarly, comparison of Landler et al., 2018 burrowing indices to our horizontal controls (N = 24) revealed no burrowing bias in their field up results for either fed or starved conditions. (D) However, when we compared the absolute value of burrowing bias we found that our combined fed + starved group, as well as Landler et al.’s ‘fed’ worms now showed significant bias when compared to horizontal controls. All tests based on Mann-Whitney Ranked Sum Tests.

https://doi.org/10.7554/eLife.31414.003
Directional information in magnetic field predicts C. elegans magnetotaxis trajectory.

(A) The direction of iron filings scattered across an assay plate reveals the general shape of magnetic field emanating from a 1.5’ diameter magnet, north-facing up beneath the plate. (B) Side view of magnetic field lines and their vertical and horizontal components across the surface of the agar-filled plate. Magnet and plate shown to scale. Field line strength not to scale. Gray arrowheads denote start location for worms and points where azide was spotted above the magnet and control goals. (C) Top view of horizontal component of magnetic field (red arrows) across the surface of the agar-filled plate. Note that magnetic north points directly away from the center of the magnet everywhere on the plate. Wild-type N2 worms prefer to move at 132° to magnetic north, which predicts the trajectory (purple arrows and line). Field lines not to scale. (D) Strength of the total magnetic field and its vertical and horizontal components across the agar surface. (E) Inclination angle of the magnetic field across the agar surface. (F) Majority of observed trajectories for N2 worms in the magnetotaxis assay arc left of magnet consistent with prediction.

https://doi.org/10.7554/eLife.31414.004

New behavioral experiments support original study

Reproduction by independent labs

Since our initial description of this behavior in C. elegans (Vidal-Gadea and Pierce-Shimomura, 2012a), we are aware of several groups joining the study of magnetic field detection using nematodes. While conducting our original study, Ilan et al. (2013) reported that parasitic nematodes migrated preferentially south over north when placed in a magnetic field. We recently became aware of a group at the University of Quilmes, Argentina who independently reproduced our findings with minor modifications (Vidal-Gadea et al., 2018).

Landler et al., 2018 notes that a study by Njus et al., 2015 reported that worms failed to respond to magnetic fields. Njus et al. restricted their study to crawling velocity and omega bends and not orientation. Nevertheless, in Figure 6 of Njus et al., 2015, they show a 10 ± 7% to 90 ± 20% change omega bends when a 5-mT magnetic field was introduced or removed respectively. Such difference in turns would have a significant effect on course trajectory and orientation. Rather than comparing these paired measurements to each other, Njus et al. compared them to the number of worms turning in the absence of a magnetic stimuli for which they report an average of 70 ± 50%. A 50% variability in omega bends is surprising and not consistent with previous reports in the literature (e.g. Vidal-Gadea et al., 2012), or even with the variability they report for the rest of their data (22.5 ± 8%, obtained by measuring and averaging standard deviations from test conditions reported by Njus et al., 2015: Figure 6). Not surprisingly, no test condition was significantly different from such a variable control. Therefore, the Njus et al., 2015 study appears to offer little evidence to counter the idea that C. elegans orients to magnetic fields.

Conceptual issues regarding magnetic orientation in C. elegans

In addition to methodological issues, Landler et al., 2018 raise two conceptual issues regarding our original study that we address below.

Magnetotaxis assay trajectories

How do worms move in our magnetotaxis assay? As described above, worms are placed in the center of an agar-filled Petri plate with a 0.29 T strength, 1.5-inch diameter, neodymium magnet placed north-side facing up 1 cm beneath the agar surface on one side of the plate (Figure 3A–C). Azide is pipetted on magnet and control sides to immobilize worms that reach either location. Landler et al., (2017) correctly point out that the intensity of the magnetic field generated by the magnet is many times stronger than the earth’s field. They ask how could worms orient to this magnetic gradient if they never encountered magnetic fields this size during their course of evolution.

We agree with Landler that the worms are unlikely to distinguish the difference between magnetic field intensities higher than earth strength. This is consistent with our finding that the AFD magnetosensory neurons failed to generate larger responses when presented with larger than earth-strength fields (Vidal-Gadea et al., 2015). Instead, we believe that C. elegans pays attention to the directional information contained in the magnetic field gradient. To help visualize the magnetic field in our magnetotaxis assay, we scattered iron filings across the agar surface of the assay plate (Figure 3A). The filings stand straight up directly above the center of the magnet, indicating that the magnetic field is perpendicular to the agar surface here. Filings tilt at increasingly shallow angles as the distance from the magnet center increases until they become parallel with the plate surface. This simple experiment shows that magnetic field lines pierce the surface of the agar at a variety of angles in a radial pattern which could provide abundant directional information pointing away from the center of the magnet in our, and Landler et al.’s, experiments.

We next calculated the direction and magnitude of the magnetic field across the assay plate. This was done using the online calculator by K and J Magnetics, and validated experimentally with the aid of a magnetometer. We found that the magnetic field was strongest at the center of the magnet and began to strongly dissipate near the inner edge of magnet (Figure 3D). The horizontal component of the field that is parallel to the plate surface was zero at the magnet center and increased away from this point up until near the inner edge of the magnet (red line, Figure 3D). The sign of the horizontal component switched at the center of the magnet reflecting how the field lines point radially away from the magnet center. The angle of field penetration varied across the assay plate as expected from the iron filings (Figure 3A,B&E). The field pierces out of the agar surface at 90° only at the center of the magnet, and starts tilting until it reaches 180° about 21.5 mm from the center of the magnet (Figure 3B&E). Beyond this point, the magnetic field starts to tilt further, piercing into the surface of the agar. Therefore, the magnetic field in the magnetotaxis assay varies in polarity and inclination which we hypothesize worms may use as a cue to orient (Figure 3B&C).

Armed with an empirically validated model of the magnetic field in our plates, we can predict how worms move in the magnetotaxis assay. We previously found that in a uniform horizontal field, N2 worms preferred to migrate approximately 132° away from magnetic north when well fed (Vidal-Gadea et al., 2015). Given this preference, we expect that worms would make a leftward arc when viewing the assay plate from above (Figure 3C). This is because worms started at the center of the assay plate would consistently bear 132° away from the horizontal field lines (purple arrows, Figure 3C). To test this prediction, we retrieved photographs of assay plates from our original 2015 study. We found that a significant portion of well-fed worms migrate towards the magnet along the left side of the plates (Figure 3F). This unusually asymmetric arced trajectory contrasts greatly from the typical symmetric trajectory that worms make when migrating to the peak of an attractant chemical gradient during chemotaxis (e.g. Pierce-Shimomura et al., 1999).

Taken together, this reanalysis of data from our 2015 study unifies the migratory patterns observed in all three behavioral assays and yields new predictions strengthening our original findings.

Magnetic orientation in three-dimensions

In our original study, we observed that different wild C. elegans strains isolated from different locations on the earth migrate at a different particular angle relative to magnetic north. For instance, relative to magnetic north, well-fed worms from Britain accumulate on average at 132°, Australian worms at 302°, and Hawaiian worms at 121°. Moreover, when worms were starved, each strain migrated ~180° relative to the preferred angle when well fed. In our study, we made the parsimonious hypothesis that these different angles may relate to the different inclination angle of the earth’s magnetic field at each location.

Given these results, Landler et al., 2018, and originally Parthasarathy, 2015, suggested that if worms simply migrated at a fixed angle relative to the magnetic field, then a population of worms dispersing from a single point outward would form a cone-shaped trajectory when burrowing in three-dimensional space. The apex angle of the cone would be twice the preferred angle and only one line along the cone would aim correctly up or down.

We were also puzzled how worms migrated at a particular angle to 2D magnetic field in our horizontal plate assay. With our new analysis above, however, this unexpected behavior appears to be consistent across all three of our magnetic orientation assays. It is important to clarify that these results provide evidence demonstrating that worms do not simply migrate at a fixed angle with respect to magnetic north. If worms simply migrated at a fixed angle to the field in a conical trajectory, then worms would have accumulated at two positions symmetrical about magnetic north on the edge of the horizontal plate. Instead, we found in that worms consistently accumulated at only one position. We observed this result in six out of six conditions – three independent wild-type strains in both fed and starved states. Likewise, if worms simply migrated at a fixed angle with respect to magnetic north in the magnetotaxis assay, then they would have moved both towards and away from the magnet in similar proportions based on our new analysis above.

We still do not understand how or why worms behave this way, and are not wedded to any particular hypothesis. As the first study of magnetic orientation in C. elegans, we do not feel that we must provide a mechanistic explanation for a finding that we do not yet fully understand. We tend to agree with Landler et al. and others in their observation that magnetic orientation alone is unlikely to be the only way worms navigate vertically. In our original study we did not hypothesize that worms orient in three dimensions solely by employing their magnetic sense. Organisms known to use the earth magnetic field in orientation also rely on additional sensory modalities to accomplish their behaviors. This is true of magnetotactic bacteria (which combine magnetotaxis with chemotaxis) and birds (which rely on vision for much of their migrations) (Chen et al., 2010; Muheim et al., 2016). For C. elegans, the AFD sensory neurons are clearly established as thermosensory, but are also involved in humidity, and CO2 detection (Mori and Ohshima, 1995; Bretscher et al., 2011; Russell et al., 2014). As we noted in Vidal-Gadea et al., 2015, these environmental parameters are stratified vertically in the soil, although the direction of their gradients can vary independently for each parameter. Consider for example the reversal of the vertical temperature gradient in the soil during daytime vs nighttime, or reversals in humidity gradients during a rainfall vs following a rain. These complex cues likely provide worms with reliable information about the vertical dimension. However, because each of these cues regularly reverse their gradients, they are less likely to provide reliable orientation information (i.e. which way is up or down). We hypothesize that magnetosensation allows worms to disambiguate directional information associated with other environmental cues.

Conclusion

Magnetic orientation may be challenging to test in C. elegans, but worthwhile to get a foothold in discovering some of the first evidence for cellular and molecular basis for magnetoreception in animals.

Materials and methods

Estimation of magnetic field

We used the K and J Magnetics magnetic field calculator to approximate field strength over distance and validated the resulting field components with our DC milligauss meter model mgm magnetometer (Alphalab, Utah).

Statistics

Vectorial data were analyzed as previously described (Vidal-Gadea et al., 2015) using Circular Toolbox for Matlab (Mathworks). Following Landler et al., (2017), animals were not pooled but each assay was rather treated as a unit. We conducted Rayleigh tests to determine probability of deviation from circular distribution. Non- parametric groups were compared using Mann-Whitney Ranked Sum tests.

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Decision letter

  1. Russ Fernald
    Reviewing Editor; Stanford University, United States

In the interests of transparency, eLife includes the editorial decision letter and accompanying author responses. A lightly edited version of the letter sent to the authors after peer review is shown, indicating the most substantive concerns; minor comments are not usually included.

Thank you for submitting your article "Response to Comment on "Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans"" for consideration by eLife. Your article has been reviewed by three peer reviewers, and the evaluation has been overseen by a Reviewing Editor and Eve Marder as the Senior Editor. The following individuals involved in review of your submission have agreed to reveal their identity: Markus Meister (Reviewer #2); Pavel Nemec (Reviewer #3).

The reviewers have discussed the reviews with one another and the Reviewing Editor has drafted this decision to help you prepare a revised submission.

Summary:

The rebuttal from Vidal-Gadea has three main parts: 1) A specific technical concern regarding Landler's attempt at replication. This is legitimate and Landler could address it with a reasonable bit of additional analysis. 2) A long list of potential reasons why magnetotaxis experiments might fail. This line of argument supports Landler's conclusion that C. elegans magnetotaxis is not a robust effect and thus not a suitable model system. 3) A report on new experiments on the subject that appear to confirm magnetotaxis in C. elegans. These don't directly address the Landler report, they use somewhat different methods, and should be published separately. Thus, the reviewers and BRE feel that a much reduced manuscript that does not introduce new data is now appropriate, and feel that any entirely new experiments belong in a new, separate paper.

Specific comments:

1) In subsection “Magnetotaxis assay”, the authors state (referring to their 2015 paper) "the cGMP-gated cation channel TAX-4 was necessary and sufficient in AFD neurons for magnetic orientation" While they did show TAX-4 was required, they did not show that is was sufficient (i.e. that expression of TAX-4 in a non-magnetically sensitive cell conferred magnetic sensitivity). In fact, TAX-4 is expressed in many sensory neurons (AWB, URX, ASE, AQR….) that are not seemingly involved in magentosensation. This statement needs to be changed.

2) In subsection “Overt differences in experimental methods”: The main technical concern regarding Landler's experiments is that the movement assays were conducted over a longer period of time (60 min vs 30 min). Vidal-Gadea contends that over this period the worms could have changed from "fed" to "starved", leading them to switch the polarity of magnetotaxis. If so, then Landler may have observed a mix of worms moving in opposite directions. Note that this concern applies to some but not all of the Landler experiments, for example the starved worms in their Figure 3B were presumably always starved, and here Landler's results are in direct conflict with Vidal-Gadea's.

3) In the same subsection: A long list of what look like minor differences between the experimental protocols in the two labs. For none of these differences (electrically shielded pipettes, plastic caps vs parafilm, brass vs aluminum for the sham magnet, etc.) is there a plausible argument how they would affect magnetotaxis. If in fact magnetotaxis is real, but so fragile that it depends in some intricate manner on the assay tube material or on large-scale field homogeneity or on minuscule temperature gradients, then one would have to agree with Landler that this just isn't a robust model system for magnetotaxis.

4) In subsection “Additional differences in experimental methods”, the authors cite the requirement for tax-4 and the AFD neurons for as evidence against magnetotaxis being an artifact of temperature gradients. But as the authors must know, AFD neurons are exquisitely sensitive to very small temperature fluctuations, and their temperature responses (which depend on tax-4) are far more robust than their responses to earth-strength magnetic fields. To this reviewer, the involvement of AFD undermines rather than supports their contention that temperature is not involved in the behavior they observe. This section should probably be cut.

5) In subsection “Horizontal plate assay”, indeed, levels of significance reported in the original paper (Vidal-Gadea et al., 2015) were based on an inappropriate number of degrees of freedom. This is because individual worms were used as replicates although they were tested within the same Petri dish and were therefore not independent of one another. Treating them as such violates a key assumption of the statistical tests used and leads to inflated type 1 error. In the response to Lander et al. Vidal-Gadea et al. claim that reanalysis of the data using mean headings of the worms had no major effect on results. They should either refrain from this argument or present the re-analysed data (preferably in from of a supplementary table).

6) In subsection “Magnetotaxis assay, it is stated that " worms in their natural habitat may have access to much greater amounts of iron than those provided for them in the lab…." We don't know what evidence the authors have for this statement. The current view on C. elegans ecology (e.g. Felix and Braendle, 2010) is that it is not a soil-dweller but rather colonizes decaying fruit and plant matter. Please remove this statement.

7) In many places the authors state that "worms migrated differently based on their global site of origin" with the specific implication that their internal compass is set to give a consistent up/down migration direction given the location of the population on the globe. These results are too preliminary to firmly draw this conclusion. Although many wild isolates of C. elegans have been described and are available from the stock center, the authors have only tested 3. Moreover, one of these, the N2 lab strain, is not really a good example of a "British" wild strain N2 was grown in liquid culture for many years (in Berkeley) followed by many more years of culture on agar plates before it was frozen. During these thousands of generations of "domestication", it is known to have acquired multiple mutations adapting it to growth in a lab environment. To establish a firm link between the local magnetic field orientation and the preferred migration direction of wild populations, it would be important to sample a wider selection of genuinely wild C. elegans isolates, and ideally cross them to get some insight into how magnetic preference segregates genetically. While this is more a critique of the original 2015 paper than anything else, it is not clear that the somewhat preliminary wild isolates data strengthens the authors' case very much.

8) In subsection “Important experimental variables for magnetic orientation in C. elegans”: An additional long list of environmental factors that could lead magnetotaxis experiments to fail. "Because of these demanding physiological and environmental parameters that the worms must be in before they will orient to magnetic fields, we hesitate to suggest which parameter may have caused trouble in Landler et al., 2018." This raises some fundamental concerns: The claim that experiments "work" only under a very specific constellation of conditions is a feature of what Langmuir once dubbed "pathological science". This belief opens a large number of degrees of freedom that the experimenter can use for data selection. If one day the magnetotaxis assay "didn't work", the student is tempted to look at the hygrometer and conclude that the weather was either too humid or too dry and exclude that data set from analysis. Perhaps Vidal-Gadea and colleagues took special precautions to guard against such risks of self-deception, but emphasizing the fragility and ephemeral nature of magnetotaxis simply supports Landler's argument.

9) Subsection “New behavioral experiments support original study”: These are reports of new studies carried out under different conditions. They don't directly address the Landler report. They should be published separately with proper peer review.

10) Subsection “Magnetic field heading over time”. "…most of the worms appeared starved and displayed a strong heading of 341° (r = 0.35, p = 0.12)." The heading is not significantly different from random. Therefore, interpretation must reflect the non-significance.

11) Subsection “Magnetic orientation in three-dimensions”: Here Vidal-Gadea reiterate their expectation that when traveling in 3D within the soil, a worm can somehow choose one specific direction among the cone of directions that have a constant angle relative to the field. This just doesn't work. In the 2D plate assay this is at least conceptually possible: the horizontal orientation of the plate leaves the worm only two such directions on the cone. And if the worm is left-right asymmetric, one can concoct a way to choose just one of those. However, in the 3D condition in soil there is no horizontal plane for reference and thus selecting one special angle among the many on the cone is not possible in principle. This argument is based on symmetry and holds regardless of how much "vector math" the worms know. If the worms were able to sense a symmetry-breaking cue, like gravity, then one needs to ask why they don't simply follow that cue.

12) Subsection “Physiological evidence for magnetoreception in C. elegans”, This section is redundant with the summary in the Introduction and does not address the Landler report, and so should be omitted here. The authors criticize the Keays manuscript for not discussing the AFD calcium imaging results from their 2015 paper. However, the responses in that paper to earth-strength fields were very small (1-2%∆F/F) and variable (confidence intervals for the average trace overlapping baseline), while they only showed tax-4 and synaptic transmission mutant responses to fields of 100X earth strength. Again, this is mostly a critique of the 2015 paper, but I don't think the results described in this paragraph strengthen the authors' case very much. I think they would be better off cutting this paragraph. The neural imaging results and the ecological conclusions seem much more questionable and preliminary, and should be eliminated from this manuscript.

https://doi.org/10.7554/eLife.31414.009

Author response

Summary:

The rebuttal from Vidal-Gadea has three main parts:

1) A specific technical concern regarding Landler's attempt at replication. This is legitimate and Landler could address it with a reasonable bit of additional analysis.

Thank you for agreeing with our concerns that Landler et al. did not replicate experiments in our 2015 study. When trying to disprove conclusions from a study, we believe that it falls on others to first try and replicate the original experiments before modifying them. Please note that by their own description in the most recent version of their article, Landler et al. still did not replicate our assays, or our controls. We feel this is unacceptable given how our reanalysis of data presented in our Figure 2 suggests that had they run proper controls, they may have found positive results.

2) A long list of potential reasons why magnetotaxis experiments might fail. This line of argument supports Landler's conclusion that C. elegans magnetotaxis is not a robust effect and thus not a suitable model system.

Our goal here was not to provide an unsurmountable list of parameters to be met by experimenters, but rather to enumerate potential variables that may or not impact outcomes. We removed much of the items on this list which we consider to have low likelihood of affecting outcome and left only those which we know to affect this assay.

3) A report on new experiments on the subject that appear to confirm magnetotaxis in C. elegans. These don't directly address the Landler report, they use somewhat different methods, and should be published separately.

As requested, we have removed all new experiments. We only include a reanalysis of data from Landler et al., 2018 and our original 2015 study in three figures. No new data areincluded in this resubmission.

Specific comments:

1) In subsection “Magnetotaxis assay”, the authors state (referring to their 2015 paper) "the cGMP-gated cation channel TAX-4 was necessary and sufficient in AFD neurons for magnetic orientation" While they did show TAX-4 was required, they did not show that is was sufficient (i.e. that expression of TAX-4 in a non-magnetically sensitive cell conferred magnetic sensitivity). In fact, TAX-4 is expressed in many sensory neurons (AWB, URX, ASE, AQR….) that are not seemingly involved in magentosensation. This statement needs to be changed.

Although we did not show or claim that tax-4 was sufficient to convey magnetosensation in other cells, we did provide evidence that tax-4 was sufficient in the AFD neurons for magnetic orientation. This was accomplished by showing that expression of tax-4 only in AFD neurons, and not in any other neuron in a tax-4 null mutant background, was sufficient to rescue magnetic orientation. We do not believe that TAX-4 alone would be sufficient for magnetic orientation. Instead, TAX-4 likely conveys the final depolarization step in a transduction pathwaylike other sensory transduction pathways operate such as in sensing odor, tastant, thermal, and gaseous cues. Nevertheless, we have removed this text to shorten our rebuttal as requested.

2) In subsection “Overt differences in experimental methods”: The main technical concern regarding Landler's experiments is that the movement assays were conducted over a longer period of time (60 min vs 30 min). Vidal-Gadea contends that over this period the worms could have changed from "fed" to "starved", leading them to switch the polarity of magnetotaxis. If so, then Landler may have observed a mix of worms moving in opposite directions. Note that this concern applies to some but not all of the Landler experiments, for example the starved worms in their Figure 3B were presumably always starved, and here Landler's results are in direct conflict with Vidal-Gadea's.

We have adjusted the text to acknowledge this.

3) In the same subsection: A long list of what look like minor differences between the experimental protocols in the two labs. For none of these differences (electrically shielded pipettes, plastic caps vs parafilm, brass vs aluminum for the sham magnet, etc.) is there a plausible argument how they would affect magnetotaxis. If in fact magnetotaxis is real, but so fragile that it depends in some intricate manner on the assay tube material or on large-scale field homogeneity or on minuscule temperature gradients, then one would have to agree with Landler that this just isn't a robust model system for magnetotaxis.

We agree that some of these factors are unlikely to influence differences in our results. To shorten our rebuttal, we have removed this discussion. We also would like to point out that magnetic orientation in C. elegans is not as robust a behavior as chemotaxis or touch avoidance. We have never claimed that the behavior is robust, merely that it is real and achievable by experienced researchers. Landler et al., however, argue that magnetotaxis is not real or even theoretically plausible. This is a claim that data from our labs, and the labs of others, do not support.

4) In subsection “Additional differences in experimental methods”, the authors cite the requirement for tax-4 and the AFD neurons for as evidence against magnetotaxis being an artifact of temperature gradients. But as the authors must know, AFD neurons are exquisitely sensitive to very small temperature fluctuations, and their temperature responses (which depend on tax-4) are far more robust than their responses to earth-strength magnetic fields. To this reviewer, the involvement of AFD undermines rather than supports their contention that temperature is not involved in the behavior they observe. This section should probably be cut.

We have removed this section to shorten the text as requested.

5) In subsection “Horizontal plate assay”, indeed, levels of significance reported in the original paper (Vidal-Gadea et al., 2015) were based on an inappropriate number of degrees of freedom. This is because individual worms were used as replicates although they were tested within the same Petri dish and were therefore not independent of one another. Treating them as such violates a key assumption of the statistical tests used and leads to inflated type 1 error. In the response to Lander et al. Vidal-Gadea et al. claim that reanalysis of the data using mean headings of the worms had no major effect on results. They should either refrain from this argument or present the re-analysed data (preferably in from of a supplementary table).

We addressed this issue in our rebuttal and plot all data in Figure 1. With the new way of analysis, we still find statistically significant results.

6) In subsection “Magnetotaxis assay”, it is stated that " worms in their natural habitat may have access to much greater amounts of iron than those provided for them in the lab…." We don't know what evidence the authors have for this statement. The current view on C. elegans ecology (e.g. Felix and Braendle, 2010) is that it is not a soil-dweller but rather colonizes decaying fruit and plant matter. Please remove this statement.

We adjusted the language to read that iron is abundant in soil surrounding decaying fruit and plant matter.

7) In many places the authors state that "worms migrated differently based on their global site of origin" with the specific implication that their internal compass is set to give a consistent up/down migration direction given the location of the population on the globe. These results are too preliminary to firmly draw this conclusion. Although many wild isolates of C. elegans have been described and are available from the stock center, the authors have only tested 3. Moreover, one of these, the N2 lab strain, is not really a good example of a "British" wild strain N2 was grown in liquid culture for many years (in Berkeley) followed by many more years of culture on agar plates before it was frozen. During these thousands of generations of "domestication", it is known to have acquired multiple mutations adapting it to growth in a lab environment. To establish a firm link between the local magnetic field orientation and the preferred migration direction of wild populations, it would be important to sample a wider selection of genuinely wild C. elegans isolates, and ideally cross them to get some insight into how magnetic preference segregates genetically. While this is more a critique of the original 2015 paper than anything else, it is not clear that the somewhat preliminary wild isolates data strengthens the authors' case very much.

Our finding that in six out of six conditions – 3 independent wild-type strains (N2, AB1, CB) in both fed and starved states, migrated at predicted angles that associate with the angle of inclination of their native site of isolation, and in four out of four conditions – 2 independent wild-type strains (N2 and AB1) in both fed and starved states, migrated in predicted directions in vertically aligned agar tubes supports our hypothesis. We agree that future work should address the basis for this phenomenon, but respectfully disagree that it should not be mentioned because it strongly supports our conclusions.

8) In subsection “Important experimental variables for magnetic orientation in C. elegans”: An additional long list of environmental factors that could lead magnetotaxis experiments to fail. "Because of these demanding physiological and environmental parameters that the worms must be in before they will orient to magnetic fields, we hesitate to suggest which parameter may have caused trouble in Landler et al., 2018." This raises some fundamental concerns: The claim that experiments "work" only under a very specific constellation of conditions is a feature of what Langmuir once dubbed "pathological science". This belief opens a large number of degrees of freedom that the experimenter can use for data selection. If one day the magnetotaxis assay "didn't work", the student is tempted to look at the hygrometer and conclude that the weather was either too humid or too dry and exclude that data set from analysis. Perhaps Vidal-Gadea and colleagues took special precautions to guard against such risks of self-deception, but emphasizing the fragility and ephemeral nature of magnetotaxis simply supports Landler's argument.

We overcame this concern by including all data with optimal and suboptimal conditions baring extreme ones detailed in our methods (e.g. sick worms). The wide field of behavior research is familiar with the difficulty of studying certain behaviors in lab conditions. e.g. seasonal differences in behavioral responses, effects of artificial substrate, unnatural temperature and lighting, etc.. Our goal for this rebuttal was to help other labs avoid these pitfalls by recognizing these factors. We have reduced the length of our rebuttal to describe only the factors that we feel are critical to replicate robust experiments.

9) Subsection “New behavioral experiments support original study”: These are reports of new studies carried out under different conditions. They don't directly address the Landler report. They should be published separately with proper peer review.

Without our knowledge, Carlos Caldart and Diego Golombek at the National University of Quilmes, Argentina independently reproduced our finding that C. elegans orients to an artificial magnet and that this orientation required cyclic-nucleotide-gated ion channel subunit TAX-2. These positive results directly address Landler et al’s concerns that our experiments cannot be reproduced. Nevertheless, we agree that they would provide stronger support if published in a separately and have thus removed them.

10) Subsection “Magnetic field heading over time”. "…most of the worms appeared starved and displayed a strong heading of 341° (r = 0.35, p = 0.12)." The heading is not significantly different from random. Therefore, interpretation must reflect the non-significance.

We have removed all new experiments as requested. Therefore, our live-tracking experiment that showed how the preferred direction of orientation changes over time from away from magnetic north, to random, and finally weakly towards magnetic north has been removed.

11) Subsection “Magnetic orientation in three-dimensions”: Here Vidal-Gadea reiterate their expectation that when traveling in 3D within the soil, a worm can somehow choose one specific direction among the cone of directions that have a constant angle relative to the field. This just doesn't work. In the 2D plate assay this is at least conceptually possible: the horizontal orientation of the plate leaves the worm only two such directions on the cone. And if the worm is left-right asymmetric, one can concoct a way to choose just one of those. However, in the 3D condition in soil there is no horizontal plane for reference and thus selecting one special angle among the many on the cone is not possible in principle. This argument is based on symmetry and holds regardless of how much "vector math" the worms know. If the worms were able to sense a symmetry-breaking cue, like gravity, then one needs to ask why they don't simply follow that cue.

We agree with the reviewer that worms need to use another cue other than the magnetic field to help break the symmetry. We have adjusted our text to focus on this hypothesis. As to why worms need to sense magnetic field if they can sense these other cues? The same question might be asked of other animals. Like other animals that orient to the magnetic field, the other cues might be unreliable. For instance, birds orient using visual cues, but rely more on magnetic cue in the absence of visual landmarks. Worms might rely on moisture, thermal or gaseous gradients to detect the vertical dimension as an allothetic cue. However, in a rotting compost pile, these gradients may not consistently reflect up versus down directions during certain conditions (e.g. rain, weather events, and decomposition). In these circumstances, the worm may rely more on magnetic cues to decide which way to move vertically.

12) Subsection “Physiological evidence for magnetoreception in C. elegans”, This section is redundant with the summary in the Introduction and does not address the Landler report, and so should be omitted here. The authors criticize the Keays manuscript for not discussing the AFD calcium imaging results from their 2015 paper. However, the responses in that paper to earth-strength fields were very small (1-2%∆F/F) and variable (confidence intervals for the average trace overlapping baseline), while they only showed tax-4 and synaptic transmission mutant responses to fields of 100X earth strength. Again, this is mostly a critique of the 2015 paper, but I don't think the results described in this paragraph strengthen the authors' case very much. I think they would be better off cutting this paragraph. The neural imaging results and the ecological conclusions seem much more questionable and preliminary, and should be eliminated from this manuscript.

From our 2015 study, average responses did not overlap with baseline and were all significantly different from baseline for 6 out of 6 experimental conditions (Figure 7C-H, K). We showed wild-type responses to 100x earth strength in Figure 7C,D,K. We also reported changes in fluorescence of 20% in our 2015 supplementary methods for partially restrained worms. Our finding that worms did not respond higher to 1x versus 100x field strength is consistent with the idea that worms have not evolved in the presence of stronger than earth magnetic fields. Nevertheless, to shorten our rebuttal as requested, we have removed this section.

https://doi.org/10.7554/eLife.31414.010

Article and author information

Author details

  1. Andres Vidal-Gadea

    School of Biological Sciences, Illinois State University, Normal, United States
    Contribution
    Supervision, Writing—original draft, Writing—review and editing, oversaw project; analyzed data; helped with conceptualization; developed novel methods; conducted experiments; wrote original and final draft
    For correspondence
    avidal@ilstu.edu
    Competing interests
    No competing interests declared
    ORCID icon 0000-0001-5981-5528
  2. Chance Bainbridge

    School of Biological Sciences, Illinois State University, Normal, United States
    Contribution
    Writing—original draft, Helped with conceptualization; Developed novel methods; Conducted experiments; edited original draft
    Competing interests
    No competing interests declared
  3. Ben Clites

    Department of Physics, University of Texas at Austin, Austin, United States
    Contribution
    Writing—review and editing, Helped with conceptualization; Developed novel methods; Conducted experiments; Edited original draft
    Competing interests
    No competing interests declared
  4. Bridgitte E Palacios

    1. Department of Physics, University of Texas at Austin, Austin, United States
    2. Department of Neuroscience, University of Texas at Austin, Austin, United States
    Contribution
    Conducted experiments
    Competing interests
    No competing interests declared
  5. Layla Bakhtiari

    Department of Neuroscience, University of Texas at Austin, Austin, United States
    Contribution
    Helped with conceptualization; Edited original draft
    Competing interests
    No competing interests declared
  6. Vernita Gordon

    Department of Neuroscience, University of Texas at Austin, Austin, United States
    Contribution
    Helped with conceptualization; Edited original draft
    Competing interests
    No competing interests declared
  7. Jonathan Pierce-Shimomura

    Department of Physics, University of Texas at Austin, Austin, United States
    Contribution
    Software, Supervision, Writing—original draft, Writing—review and editing, Oversaw project; Analyzed data; Helped with conceptualization; Ddeveloped novel methods; Conducted experiments; Wrote original and final draft
    For correspondence
    jonps@austin.utexas.edu
    Competing interests
    No competing interests declared
    ORCID icon 0000-0002-9619-4713

Funding

National Institutes of Health (R15AR068583)

  • Andres Vidal-Gadea

National Institutes of Health (R01NS075541)

  • Jonathan Pierce-Shimomura

National Institutes of Health (1RF1AG057355)

  • Jonathan Pierce-Shimomura

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Acknowledgements

We wish to acknowledge the Caenorhabditis Genetics Center which is supported by the National Institutes of Health, as well as NIH grants to AV-G (R15AR068583) and JP (R01NS075541 and 1RF1AG057355).

Reviewing Editor

  1. Russ Fernald, Stanford University, United States

Publication history

  1. Received: August 21, 2017
  2. Accepted: March 19, 2018
  3. Version of Record published: April 13, 2018 (version 1)

Copyright

© 2018, Vidal-Gadea et al.

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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Further reading

    1. Neuroscience
    Andrés Vidal-Gadea et al.
    Research Article Updated

    Many organisms spanning from bacteria to mammals orient to the earth's magnetic field. For a few animals, central neurons responsive to earth-strength magnetic fields have been identified; however, magnetosensory neurons have yet to be identified in any animal. We show that the nematode Caenorhabditis elegans orients to the earth's magnetic field during vertical burrowing migrations. Well-fed worms migrated up, while starved worms migrated down. Populations isolated from around the world, migrated at angles to the magnetic vector that would optimize vertical translation in their native soil, with northern- and southern-hemisphere worms displaying opposite migratory preferences. Magnetic orientation and vertical migrations required the TAX-4 cyclic nucleotide-gated ion channel in the AFD sensory neuron pair. Calcium imaging showed that these neurons respond to magnetic fields even without synaptic input. C. elegans may have adapted magnetic orientation to simplify their vertical burrowing migration by reducing the orientation task from three dimensions to one.

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