Aimed limb movements in a hemimetabolous insect are intrinsically compensated for allometric wing growth by developmental mechanisms.

Alexandra J Patel,Thomas Matheson

doi:10.1242/jeb.208553

Abstract

ABSTRACTFor aimed limb movements to remain functional, they must be adapted to developmental changes in body morphology and sensory-motor systems. Insects use their limbs to groom the body surface or to dislodge external stimuli, but they face the particular problem of adapting these movements to step-like changes in body morphology during metamorphosis or moulting. Locusts are hemimetabolous insects in which the imaginal moult to adulthood results in a sudden and dramatic allometric growth of the wings relative to the body and the legs. We show that, despite this, hind limb scratches aimed at mechanosensory stimuli on the wings remain targeted to appropriate locations after moulting. In juveniles, the tips of the wings extend less than halfway along the abdomen, but in adults they extend well beyond the posterior end. Kinematic analyses were used to examine the scratching responses of juveniles (fifth instars) and adults to touch of anterior (wing base) and posterior (distal abdomen) targets that develop isometrically, and to wing tip targets that are anterior in juveniles but posterior in adults. Juveniles reach the (anterior) wing tip with the distal tibia of the hind leg using anterior rotation of the thoraco-coxal and coxo-trochanteral (‘hip’) joints and flexion of the femoro-tibial (‘knee’) joint. Adults, however, reach the corresponding (but now posterior) wing tip using posterior rotation of the hip and extension of the knee, reflecting a different underlying motor pattern. This change in kinematics occurs immediately after the adult moult without learning, indicating that the switch is developmentally programmed.

Highlights

Important behaviours such as reaching, stepping, grooming and prey capture all require accurately aimed limb movements
We show that gentle tactile stimulation of the wings elicits aimed hind leg movements in juvenile locusts that closely resemble those of adults
Combinations of joint angles lie on a continuum in joint angle space, allowing the effector to reach anterior targets using joint angle combinations at one end of the continuum, whereas posterior targets are reached using joint angle combinations at the other extreme of the continuum

Summary

Introduction

Important behaviours such as reaching, stepping, grooming and prey capture all require accurately aimed limb movements. *Present address: University of Leicester, Leicester Learning Institute, 103–105 Princess Road East, Leicester LE1 7LG, UK Human infants begin reaching towards targets at age 4–5 months, but the kinematics of their movements change over the first 3 years of life before assuming their adult-like patterns (Konczak and Dichgans, 1997). This reflects continual recalibration of the sensory-motor system as both the peripheral mechanics and the central nervous system develop (Konczak et al, 1997). Striking is triggered at age- and body-size-appropriate distances largely as a result of concomitant changes in the size and shape of the eyes and the size of the body and legs at each moult (Balderrama and Maldonado, 1973; Maldonado et al, 1974; Kral and Poteser, 2009) – so here it seems that experience-dependent ‘recalibration’ is not required

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