Date: 22.02.2020

What a caterpillar has to know to build its cocoon…

This article explores an intriguing behavioral program enabling the giant silkworm (Hyalophora cecropia) to successfully construct its complex silk cocoon to survive the harsh overwintering conditions.

Photo description: Left: Morphology of the late 5th instar caterpillar spinning apparatus and surrounding tissues. 3D perspective views were obtained by volume rendering of multiple confocal stacks stained by phalloidin (artificially colored – green, blue, yellow) and DAPI (colored in red). Right: Model of the cocoon construction program performed by the 5th instar cecropia caterpillar.

The late 5th instar caterpillar of the cecropia silk moth (Hyalophora cecropia) spins a silken cocoon with a distinct, multilayered architecture. The cocoon construction program consists of a highly ordered sequence of events. We performed behavioral experiments to evaluate the hypothesis that the length of silk that passes through the spinneret controls the orderly execution of each of the discrete events of cocoon spinning. We showed by three-dimensional scanning and quantitative measurements of silk weights that if cocoon construction is interrupted, upon re-spinning, the caterpillar continues the cocoon program from where it left off. We also demonstrated by quantitative measurements of silk weights that cecropia caterpillars will not bypass any of the sections of the cocoon during the construction process, even if presented with a pre-spun section of a cocoon spun by another caterpillar. Blocking silk output inhibits caterpillars from performing normal spinning behaviors used for cocoon construction. Surprisingly, unblocking silk output 24-hr later did not restart the cocoon construction program, suggesting the involvement of a temporally defined interval timer. We confirm with surgical reductions of the silk glands that it is the length of silk itself that matters, rather than the total amount of silk extracted by individuals. We used scanning electron microscopy to directly show that either mono- or dual-filament silk (i.e., equal silk lengths but which vary in their total amount of silk extracted) can be used to construct equivalent cocoons of normal size and that contain all the relevant layers. We propose that our findings strongly support the hypothesis that the caterpillar uses a silk “odometer” to measure the length of silk extracted during cocoon construction but does so in a temporally regulated manner. We further postulate that our examination of the anatomy of the silk spinning apparatus and ablating spinneret sensory output provides evidence that silk length measurement occurs upstream of output from the spinneret.

Sehadova H., Guerra P.A., Sauman I. and Reppert S.M. (2020) A re-evaluation of silk measurement by the cecropia caterpillar (Hyalophora cecropia) during cocoon construction reveals use of an interval timer and a silk odometer. PLoS ONE 15(2): e0228453.

DOI: 10.1371/journal.pone.0228453




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