Distance and force production during jumping in wild-type and mutantDrosophila melanogaster

Abstract

SUMMARY In many insects renowned for their jumping ability, elastic storage is used so that high forces can be developed prior to jumping. We have combined physiological, behavioural and genetic approaches to test whether elastic energy storage makes a major contribution to jumping in Drosophila. We describe a sensitive strain gauge setup, which measures the forces produced by tethered flies through their mesothoracic legs. The peak force produced by the main jumping muscle of female flies from a wild-type(Canton-S) strain is 101±4.4 μN [and this is indistinguishable from a second wild-type (Texas) strain]. The force takes 8.2 ms to reach its peak. The peak force is not affected significantly by altering the leg angle (femur–tibia joint angle) in the range of 75–120°, but the peak force declines as the leg is extended further. Measurements of jumping ability (distance jumped) showed that female Drosophila (with their wings removed) of two wild-type strains,Canton-S and Texas, produced jumps of 28.6±0.7 and 30.2±1.0 mm(mean ± s.e.m.). For a female wild-type Drosophila, a jump of 30 mm corresponds to a kinetic energy of 200 nJ on take-off (allowing 20% of the energy to overcome air resistance). We develop equations of motion for a linear force–time model of take-off and calculate that the time to take-off is 5.0 ms and the peak force should be 274 μN (137 μN leg–1). We predicted, from the role of octopamine in enhancing muscle tension in several locust muscles, that if stored elastic energy plays no part in force development, then genetic manipulation of the octopaminergic system would directly affect force production and jumping in Drosophila. Using two mutants deficient in the octopaminergic system, TbhnM18(M18) and TyrRhono (hono), we found significantly reduced jumping distances (20.7±0.7 and 20.7±0.4 mm, respectively) and force production (52% and 55%, respectively) compared with wild type. From the reduced distance and force production in M18, a mutant deficient in octopamine synthesis, and in hono, a tyramine/octopamine receptor mutant, we conclude that in Drosophila, as in locusts,octopamine modulates escape jumping. We conclude that the fly does not need to store large quantities of elastic energy in order to make its jump because (1)the measured and calculated forces agree to within 40% and (2) the reduction in distances jumped by the mutants correlates well with their reduction in measured peak force.

Jumping mechanisms and strategies in moths (Lepidoptera)

“…Small flies such as Drosophila use the middle pair of legs (Card and Dickinson, 2008;Zumstein et al, 2004), whilst most other jumping insects from locusts (Bennet-Clark, 1975) to fleas (Bennet-Clark and Lucey, 1967) and jumping bugs (Burrows, 2006) use only the hind legs. The moths analysed here join a small group of diverse insects that includes lacewings (Burrows and Dorosenko, 2014), snow fleas (Boreus hyemalis) (Burrows, 2011), a fly (Hydrophorus alboflorens) (Burrows, 2013) and an ant (Myrmecia nigrocincta) (Tautz et al, 1994) in using both the middle and hind pairs of legs together to propel jumping.…”

Inter-leg coordination in the control of walking speed inDrosophila

“…It is quite conceivable that w 1118 flies walk slower because of visual impairment (Kalmus, 1943 , Tbh nM18 lacks octopamine (Monastirioti et al, 1996), a biogenic amine that plays an important role during various locomotor behaviors in invertebrates. It is known to influence the initiation and maintenance of flight (Brembs et al, 2007) and pre-flight jumps in Drosophila (Zumstein et al, 2004), and is also implicated as a modulator of walking behavior in cockroaches, for example (Gal and Libersat, 2008;Gal and Libersat, 2010). Interestingly, in all of these studies octopamine appears to selectively influence high-level aspects of locomotion, while more low-level aspects, such as leg kinematics, for instance, remain unaffected.…”

Dynamics of escaping flight initiations of Drosophila melanogaster

“…Since leg forces are only active for as long as there is contact with the substrate, first, we consider our initial forces (t = 0 [ms]), which averaged to 97.3±5. [28]. These measurements were made in tethered flies and the results were highly dependent on 'leg angles', which could partially account for our underestimates.…”