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. 2011 Aug 9;21(15):1326-30.
doi: 10.1016/j.cub.2011.06.063. Epub 2011 Jul 28.

The C. Elegans Touch Response Facilitates Escape From Predacious Fungi

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Free PMC article

The C. Elegans Touch Response Facilitates Escape From Predacious Fungi

Sean M Maguire et al. Curr Biol. .
Free PMC article

Abstract

Predator-prey interactions are vital determinants in the natural selection of behavioral traits. Gentle touch to the anterior half of the body of Caenorhabditis elegans elicits an escape response in which the animal quickly reverses and suppresses exploratory head movements [1, 2]. Here, we investigate the ecological significance of the touch response in predator-prey interactions between C. elegans and predacious fungi that catch nematodes using constricting hyphal rings. We show that the constricting rings of Drechslerella doedycoides catch early larval stages with a diameter similar to the trap opening. There is a delay between the ring entry and ring closure, which allows the animal to withdraw from the trap before being caught. Mutants that fail to suppress head movements in response to touch are caught more efficiently than the wild-type. This demonstrates that the coordination of motor programs allows C. elegans to smoothly retract from a fungal noose and evade capture. Our results suggest that selective pressures imposed by predacious fungi have shaped the evolution of C. elegans escape behavior.

Figures

Figure. 1
Figure. 1. Constricting fungal rings entrap C. elegans larvae
(A) C. elegans makes exploratory head movements during locomotion [7, 8]. Extent of head movements is outlined. In response to light anterior touch, the animal reverses and suppresses head movements (Figure S1). Nose touch induces a reversal but head movements are suppressed less efficiently. Posterior touch leads to the acceleration of forward locomotion but not the suppression of head movements. Cell bodies and neuronal processes of neurons involved in nose touch (blue: ASH, FLP and OLQ) [24], anterior touch (purple: ALM and AVM) and posterior touch (red: PLM and PVM) [1]. (B) Inner diameter of uninflated constricting rings. D. dactyloides, 12.9 +/- 0.3 μm (n=51); D. brochopaga, 22.1 +/- 1.0 μm (n=25); D. doedycoides, 17.1 +/- 0.4 μm (n=27); D. bembicoides, 9.6 +/- 0.3 μm (n=20). (C) Average diameter of L1: 11.7 +/- 0.2 μm (n=55); L2: 17.0 +/- 0.2 μm (n=49); L3: 22.2 +/- 0.3 μm (n=92); L4: 29.6 +/- 0.6 μm (n=16); Adult: 47.9 +/- 0.8 μm (n=33). (D) Average percentage of worms caught after four hours: L1: 53 +/- 5 % (n=165); L2: 61 +/- 9% (n=1533); L3: 29 +/- 4% (n=1893); L4: 8 +/- 2% (n=499); Adult, 1 +/- 1% (n=461). Error bars represent standard error of the mean (SEM). (E) C. elegans is tapered on both ends. Colored line represents the diameter of an L2 larvae along the anterior-posterior (A-P) axis. Color of the line corresponds to nose (blue), anterior (purple) and posterior (red) regions of the body. Dots represent distance along the A-P axis where the animal is caught by a constricting ring (n=117). L2 larvae are mostly caught at the anterior end (See Movie S1). (F-H) Scanning Electron micrographs: (F) L2 larvae caught in constricting rings of D. doedycoides. (G) A constricting ring prior to inflation. (H) Expanded ring cells of the trap impinging on the cuticle of the worm. Scale bar is 10 μm.
Figure. 2
Figure. 2. C. elegans can escape from constricting rings
(A) Lag time between an animal entering a ring and ring closure of D. doedycoides. The average lag time of trap closure in successful capture events was 5.8 ± 0.5 sec (n=59). Left: Bar diagram shows the percentage of trap closure events in 2 seconds binned intervals. Right: red line shows the cumulative percentage of ring closures. (B) The percentage of L2 larvae that entered and escaped the trap by reversing. Wild type (N2): 81 ± 4% (n=170); mec-4(e1339): 43 ± 8% (n=87), p= 0.0050; osm-9(n1603): 81 +/- 6 %, (n=112) n.s. (p= 0.9804); tdc-1(n3420): 49 ± 10% (n=94), p=0.0482; lgc-55(tm2913): 60 ± 6% (n=125), p=0.0213; unc-4(e120): 59 +/- 7% (n=126), p=0.0289. Error bars represent SEM. Statistical difference from wild type; ** p-value < 0.005; * p-value < 0.05, two-tailed Student’s t-test. (C) Still images of an L2 animal entering and escaping from a constricting ring (See Movie S2). After the animal wedged it self in the ring (entry) the animal reversed and suppressed head movements allowing it to exit the ring just before the ring cells inflate (escape).
Figure. 3
Figure. 3. Tyramine signaling facilitates extraction from a noose
(A) Young adult animals moving through a nylon mesh. Animals make contact with the threads of the mesh when they pass through the 37 μm openings. (B) The time animals spent in a 37 μm opening of a nylon mesh before exiting: : Wild type (N2): 9 +/- 1 s (n=156), lgc-55(tm2913): 23 +/- 4 s (n=274), p=0.0059; Plgc-55∷LGC-55: 10 +/- 1 s (n=418), p=0.1675. Error bars represent SEM. Statistical difference from wild type; ** p-value < 0.005; * p-value < 0.05, two-tailed Student’s t-test.
Figure. 4
Figure. 4. Touch induced suppression of head movements facilitates escape form fungal constricting rings
(A) Animals that fail to suppress head movements are caught more often than the wild type in competition experiments. Genotypes were mixed in a 1:1 ratio and the caught fraction of each genotype was determined. Fluorescent reporters were used to mark the different genotypes. The capture index was calculated by subtracting the weighted fractions of the caught testing genotype from that of the control. A capture index of 0 represents an equal distribution of animals caught between the testing genotype and the wild type. A positive capture index indicates a selective disadvantage compared to the wild type. Wild type (N2): -0.01+/-0.02 (n=14); lgc-55(tm2913): 0.36 +/- 0.02 (n=17); lgc-55; Plgc-55∷LGC-55 rescue: 0.02 +/- 0.02 (n=12); lgc-55; Pmyo-3∷LGC-55 rescue: 0.12 +/- 0.02 (n=17). Error bars represent SEM. Statistical difference as noted; *** p-value < 0.0001, two-tailed Student’s t-test. (See also Figure S4) (B) C. elegans locomotion is accompanied by exploratory head movements. When an animal wedges itself into a constricting ring activation of the anterior touch sensory neurons induces an escape response. Wild-type animals reverse and suppress exploratory head movements allowing a smooth exit from the constricting ring. Tyramine-signaling mutants tdc-1(n3420) and lgc-55(tm2913) reverse but fail to suppress head movements during an escape making it more likely for the animal to activate the ring cells and get caught.

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