Kinematic diversity suggests expanded roles for fly halteres

Abstract

The halteres of flies are mechanosensory organs that provide information about body rotations during flight. We measured haltere movements in a range of fly taxa during free walking and tethered flight. We find a diversity of wing-haltere phase relationships in flight, with higher variability in more ancient families and less in more derived families. Diverse haltere movements were observed during free walking and were correlated with phylogeny. We predicted that haltere removal might decrease behavioural performance in those flies that move them during walking and provide evidence that this is the case. Our comparative approach reveals previously unknown diversity in haltere movements and opens the possibility of multiple functional roles for halteres in different fly behaviours.

Cross-modal influence of mechanosensory input on gaze responses to visual motion in Drosophila

“…These results also suggest that halteres contribute more to reflexive, 'inner-loop' behaviors than to voluntary 'outer-loop' behaviors (Krapp and Wicklein, 2008;Mureli and Fox, 2015). These differences in head movement behaviors between Drosophila and other flies, in combination with differences in haltere movement behaviors (Hall et al, 2015), also open the possibility that haltere inputs to NMNs might differ significantly between fly taxa. What is the sensory effect of Drosophila head movements on the visual input?…”

“…If haltere oscillations are necessary for visually guided head movements to occur, then Drosophila should only show such head movements during flight, because this is the only behavior in which the halteres are oscillated in this species (Geurten et al, 2014;Hall et al, 2015). By contrast, Calliphora show visually guided head movements during walking behavior, and also oscillate the halteres during walking (Geurten et al, 2014;Hall et al, 2015;Sandeman and Markl, 1980). To determine whether Drosophila show visually guided head movements when not flying, we placed flies in a visual LED arena and stimulated the visual system with wide-field triangle-wave motion, which produces a robust head movement response in flying flies .…”

Representation of Haltere Oscillations and Integration with Visual Inputs in the Fly Central Complex

“…4D) and could signal that the halteres are oscillating at any speed. We note, however, that in blowflies and flesh flies, the halteres oscillate at similar frequencies during both walking and flying (Hall et al, 2015), and thus, a downstream neuron would likely be unable to determine the specific behavioral state from the haltere frequency. Similarly, the neck motoneurons that show gating activity are not selective for specific haltere frequencies; oscillations as low as 10 Hz (well below the biological range of haltere oscillation) are sufficient for action potentials.…”

“…The highest frequency trials in these experiments (150 Hz) were an approximation of self-driven haltere frequency during tethered flight (168 Hz; Hall et al, 2015) and in free walking (173 Hz with variable frequencies; Yarger and Fox, 2018). Because haltere oscillations at the beginning and end of each oscillation bout in both flight and walking are slower and more variable than their peak oscillation frequency, it is possible that frequency encoding neurons of the CX are sensitive to changes in the haltere's oscillation patterns upon changes in behavioral state.…”

Mechanics of the thorax in flies

“…In most Diptera, the wings and halteres beat precisely antiphase (i.e. 180 deg) relative to each other, whereas in some others with higher wingbeat frequencies, the phase relationship may not be 180 deg (Hall et al, 2015). From the perspective of flies, the phase difference is extremely important because any change in the relative phase between wings and halteres is indicative of an aerial maneuver that must be corrected if unintentional; alternatively, the tendency to correct such deviations should be overridden if the maneuver is intentional.…”