Rearrangements in the musculature correlate with jumping behaviour in legless Mediterranean fruit fly larvae Ceratitis capitata (Tephritidae)

Abstract

Larvae of holometabolic insects evolved different crawling strategies depending on the presence or absence of larval legs or life style. A rather unusual mode of locomotion has independently evolved in legless larvae of several dipteran species. Maggots of the Mediterranean fruit fly Ceratitis capitata developed an effective jumping mechanism to increase locomotion speed or to deter predators during the search for suitable pupation sites. Here, we use high-speed videography to visualize even the fastest movements during jump preparation and take-off. Quantification of kinetic and biometric parameters reveal that maggots jump up to 15-fold of their body length from a standing position and gain speed with 27 times the acceleration of gravity. Videos at high spatial resolution show the mechanism of latch formation and release in unprecedented detail. Mouth hooks insert in the caudal segment and raise a cuticular fold that serves as a handle to pressurize the body prior to launch. Since locomotion behaviour should be intrinsically linked to neuromuscular systems, we dissected third instar larvae and determined the precise pattern of abdominal muscles fibres. Compared to non-jumping dipteran larvae, such as Drosophila melanogaster, the overall arrangement is highly similar, but a few muscle fibres show characteristic re-arrangements in orientation and strength that are consistent with a role in bending and jumping. These results suggest that body wall muscles show adaptations to jumping behaviour in Ceratitis larvae, and possibly also in other species with different jumping techniques.