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First published online November 2, 2007
Journal of Experimental Biology 210, 4043-4052 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.006551
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Temperature and food mediate long-term thermotactic behavioral plasticity by association-independent mechanisms in C. elegans

Cynthia A. Chi1,*, Damon A. Clark1,*, Stella Lee1,*, David Biron1,2, Linjiao Luo1, Christopher V. Gabel1, Jeffrey Brown1, Piali Sengupta2 and Aravinthan D. T. Samuel1,3,{dagger}

1 Department of Physics, Harvard University, Cambridge, MA 02138, USA
2 Department of Biology and National Center for Behavioral Genomics, Brandeis University, Waltham, MA 02454, USA
3 Center for Brain Science, Harvard University, Cambridge, MA 02138, USA


Figure 1
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  		Fig. 1. C. elegans crawls towards its set-point (TS) from higher temperatures but not from lower temperatures. (A) Wild-type (WT) worms that were grown overnight at 15°C were initially placed near the middle of a linear thermal gradient spanning 18–22°C across a 9 cm plate, and their instantaneous positions over time were recorded by video microscopy. Each upper panel shows overlaid snapshots of instantaneous worm positions from six independent plates containing ~100 worms in total, with the position of each worm indicated by an open circle. Lower panels show the corresponding histograms of worm positions. The evolution of the worm distributions over time indicates that these worms migrate towards the previous cultivation temperature in what is called cryophilic movement. (B) When wild-type worms that were grown overnight at 25°C were initially placed near the middle of the linear thermal gradient, they exhibit random dispersal.

 

Figure 2
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  		Fig. 2. Starvation inactivates the mechanism for cryophilic movement. (A) When wild-type (WT) worms that were grown overnight at 15°C then starved for 24 h at 15°C are placed near the middle of the linear thermal gradient, they exhibit nearly random dispersal. (B) From snapshots of the temperature positions of individual worms on the spatial thermal gradients, we calculated the mean temperature of the population, and we plotted the mean temperature over time for worms that had been starved for different durations. Worms were initially placed near 20°C, and a subsequent decrease in the mean temperature indicates cryophilic movement. The speed of instantaneous forward-crawling movements exhibited by individual worms in each experiment is indicated in italics (mean ± s.d.), showing that the atactic behavior caused by starvation is not simply due to lack of mobility.

 

Figure 3
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  		Fig. 3. Changes in cryophilic movement are attributed to changes in cryophilic bias. (A) Scatter plots show the correlation between run orientation and run duration of the detailed crawling trajectories exhibited by individual well-fed wild-type (WT) worms navigating a linear spatial thermal gradient at T>TS (upper plot) and at T<TS (lower plot). The starting point of all runs is set to the origin. Each black dot denotes the relative end-point of each run; duration is indicated by distance from the origin (see scale bar) and run orientation is indicated by the angle with respect to the thermal gradient (defined to be 0° for worms crawling up the spatial gradient, shown by the arrow). For wild-type worms tested at T>TS (cultivated at 15°C and allowed to navigate on a gradient between 18–22°C), runs oriented down the gradient are extended, and runs oriented up the gradient are shortened. By contrast, for wild-type worms tested at T<TS (raised at 25°C and allowed to navigate on a gradient between 18–22°C), there is no significant correlation between run orientation and duration. Each scatter plot represents run statistics collected from ~1000 runs exhibited by ~100 worms. (B) Plots of mean run duration as a function of run orientation of wild-type animals, corresponding to the scatter plots in A. Error bars represent 1 s.e.m. Cryophilic bias at T>TS is represented as prolonged runs pointed down the gradient (grey data points, fit to a constant with P<10–5). The weak or undetectable thermotactic response at T<TS is represented as invariance of run duration with run orientation (black data points, fit to a constant with P>0.1). (C) Two measures of cryophilic behavior – the cryophilic bias, calculated using Eqn 1, and the mean of cryophilic migration after 15 min – are plotted for wild-type worms that had been starved for different durations. Errors bars are 1 s.e.m.

 

Figure 4
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  		Fig. 4. Starvation and sustained exposure to new temperatures have separate long-term effects on thermotactic behavior. (A) When wild-type (WT) worms that were grown overnight at 15°C and then starved for 4 h at 25°C are placed near the middle of the linear thermal gradient, they exhibit random dispersal. The movements of (B) wild-type worms and (C) ttx-3(ks5) mutant worms up or down spatial thermal gradients spanning 18–22°C were quantified after they had been grown at 15°C (left-hand panels) or grown at 25°C (right-hand panels). Line colors indicate the temperature of the worms during the 4 h preceding each experiment; blue represents 15°C and red represents 25°C. Solid lines indicate experiments using unstarved worms. Dotted lines indicate experiments in which worms were starved at 15°C or 25°C before each experiment. In each data trace, error bars (±1 s.e.m.) are shown at 10 min intervals. The speed of instantaneous forward-crawling movements exhibited by individual worms in each experiment is indicated in italics, showing that atactic behavior cannot simply be attributed to lack of mobility (mean ± s.d.).

 

Figure 5
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  		Fig. 5. Worms do not specifically avoid the temperature at which they had been starved. When wild-type worms that were grown overnight at 20°C and then starved for 4 h at 20°C are placed near the middle of linear thermal gradients that span 20°C, they exhibit random dispersal. (A) Data from experiments using a gradient spanning 18–22°C over a 9 cm plate. (B) Data from experiments using a gradient spanning 15–25°C over a 9 cm plate. Upper panels show snapshots of instantaneous worm positions. Lower panels show corresponding histograms.

 

Figure 6
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  		Fig. 6. Analysis of hen-1 and tax-6 mutants. The movements of (A) hen-1(tm501) mutant worms and (B) tax-6(p675) mutant worms after they had been grown at 15°C or 25°C (solid lines in each panel) or starved for 4 h at 15°C or 25°C before each experiment (dotted lines in each panel). The speed of instantaneous forward movements exhibited by individual worms in each experiment is indicated in italics (mean ± s.d.), showing that differences in navigational behavior cannot be simply attributed to differences in mobility.

 

Figure 7
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  		Fig. 7. Comparison of cryophilic movement and cryophilic bias of wild-type (WT) and mutant worms. (A) Cryophilic bias and cryophilic migration were calculated for the experiments using wild-type and mutant worms in Figs 4 and 5, in the manner described in Fig. 3C. Error bars represent 1 s.e.m. Cases in which the cryophilic bias indices or amount of cryophilic migration differ from zero are indicated by * (P<0.05) and ** (P<0.005). (B) Linear correlation between all measurements of cryophilic bias index and cryophilic migration, using all data from Fig. 3C and Fig. 7A.

 

Figure 8
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  		Fig. 8. Rate of TS resetting measured by quantifying isothermal tracking in wild-type and hen-1 mutant worms. (A) Isothermal tracks made by wild-type worms grown overnight at 25°C and placed on a steep linear thermal gradient spanning 16–26°C across a 9 cm-diameter plate. Snapshots of the movement of animals on the gradient were digitized and overlaid such that their trajectories were visible. Isothermal tracks, artificially colored yellow, were defined as long vertical trajectories and emerged in a band of temperatures near the previous cultivation temperature. For comparison, a few white trajectories are also shown, representing worms that are not tracking isotherms in the same period of time. The TS is quantified as the mean temperature of isothermal tracks exhibited by a certain population of worms. (B) Isothermal tracks exhibited by hen-1(tm501) worms that were grown overnight at 25°C and placed on steep linear thermal gradients (1°C/cm). (C–F) The time-course of TS resetting of wild-type animals and hen-1(tm501) animals. In C and D, worms were cultivated overnight with bacterial food at 15°C or 25°C, then shifted to a plate containing food at 25°C or 15°C, respectively. In E and F, worms were grown overnight with bacterial food, then shifted to a new plate without food. The circles represent experimental data, and the broken lines depict an exponential fit of the wild-type data. At least two independent plates, 50 worms and 20 isothermal tracks were used for each data point.

 

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© The Company of Biologists Ltd 2007