RNAi of the elastomeric protein resilin reduces jump velocity and resilience to damage in locusts

Abstract

Resilin, an elastomeric protein with remarkable physical properties that outperforms synthetic rubbers, is a near-ubiquitous feature of the power amplification mechanisms used by jumping insects. Catapult-like mechanisms, which incorporate elastic energy stores formed from a composite of stiff cuticle and resilin, are frequently used by insects to translate slow muscle contractions into rapid-release recoil movements. The precise role of resilin in these jumping mechanisms remains unclear, however. We used RNAi to reduce resilin deposition in the principal energy-storing springs of the desert locust ( Schistocerca gregaria ) before measuring jumping performance. Knockdown reduced the amount of resilin-associated fluorescence in the semilunar processes (SLPs) by 44% and reduced the cross-sectional area of the tendons of the hind leg extensor-tibiae muscle by 31%. This affected jumping in three ways: First, take-off velocity was reduced by 15% in knockdown animals, which could be explained by a change in the extrinsic stiffness of the extensor-tibiae tendon caused by the decrease in its cross-sectional area. Second, knockdown resulted in permanent breakages in the hind legs of 29% of knockdown locusts as tested by electrical stimulation of the extensor muscle, but none in controls. Third, knockdown locusts exhibited a greater decline in distance jumped when made to jump in rapid succession than did controls. We conclude that stiff cuticle acts as the principal elastic energy store for insect jumping, while resilin protects these more brittle structures against breakage from repeated use.