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Image from Deora et al., 2021

Secrets of the buzzing flies

Image from Deora et al., 2021

Researchers from the National Centre for Biological Sciences (NCBS), Bangalore, have uncovered another fascinating aspect of flight mechanics in flying insects. Their work shows that soldier flies’ wings and halteres (sense organs that provide rapid feedback for balanced and stable flight) function like two independently driven coupled oscillators. Through mechanical linkages in the fly’s thorax, the wings and halteres can synchronize their movements even when they beat at very high frequencies. The study has also examined, in detail, how the system copes when its structural integrity is affected; for example, if one or both wings are damaged.

A buzzing fly is usually an annoyance. But what most of us often fail to see, is that the buzzing fly is a very well-engineered annoyance, honed to near perfection through years of evolution. Scientists are only now beginning to understand—through brief glimpses into its mechanical and neural connections—the fly’s amazingly intricate flight system.

In a new study published in ELife, Sanjay Sane’s team from the National Centre for Biological Sciences (NCBS), Bangalore, has used soldier flies to investigate how mechanical linkages help flies coordinate wing movements especially when the flight system is perturbed. It investigates how wings and halteres (sense organs involved in rapid feedback for fine-tuning flight) continue to synchronize their movements despite asymmetrical damage and finds that the two structures function as two independently powered coupled oscillators. The system is reminiscent of two pendulums connected to each other; even if both are set in motion independently at slightly different frequencies, they begin to synchronize and fall into a rhythm with each other.

The synchronization between wings and halteres is maintained through mechanical linkages in the thorax. The scutellar link couples the two wings with each other, while the sub-epimeral ridge couples each wing with its corresponding haltere. The entire system is tuned to maintain synchronicity even at high frequencies, which for flies, is hundreds of wingbeats per minute.

“But during an insect’s life, wings can get damaged through natural wear and tear, and when this happens, wing surface areas change. While we already know that this impacts insect flight, this recent work looks at how this happens,” says Tanvi Deora from Sanjay Sane’s group at NCBS. The researchers used tethered flies (where flies are held stationary with a stick glued to their backs) to understand how the flight system coped with changes to wing sizes. When both wings were clipped symmetrically, they beat at a higher frequency but remained synchronized. There are two reasons for this increase in wingbeat frequencies. One, which is likely in these experiments, is due to the reduced load on the resonant wing–thorax system—smaller wings are lighter, which causes wingbeat frequencies to increase . The second reason could be a compensation mechanism to maintain lift. Since smaller wings have lower surface areas, the lift they generate will be smaller; so, the insect has to flap faster to stay airborne. .

However, what would happen if only one wing were to be clipped and the other intact? Even slight asymmetries in wing sizes can affect the torque forces acting on the body, upset wing coordination, and therefore maneuverability in flight. Experiments revealed that shortening one wing (even down to less than 50% of its original size) did not increase flapping frequency. Instead, both wings remained coordinated and the beat frequency seemed to be set by the intact wing, proving that the wings are very tightly coupled to each other.

To investigate if this coupling could be disturbed, the researchers broke the mechanical connection between the two wings—the scutellar link. Without this link, the wingbeats of the two wings became wildly unsynchronized with each wing beating at different phases and frequencies.

Next, the study examined how the wings were coupled to the halteres. As wings were clipped to create slight size reductions in a carefully graded manner and wingbeat frequencies increased gradually, so did those of the halteres. But once wingbeat frequencies reached 150% of their normal values, the coupling between wings and halteres failed, and the halteres fell back to their natural frequencies. When the sub-epimeral ridge, which mechanically connects each wing with its corresponding haltere was disrupted, the haltere frequencies no longer mirrored changes in wingbeat frequencies.

While these experiments clearly demonstrated that changes in the wings’ movements can affect haltere movements through mechanical links, it wasn’t clear if the opposite was true—could changes in haltere movement frequencies affect wingbeat frequencies?

“This was a big practical challenge; initially, we weren’t sure if we could perturb both wings and halteres,” says Deora. “With wings, we can clip them gradually to change their beat frequencies steadily. However, with halteres, this is not possible because not only are they tiny, but most of their weight is on their tips. If the tip is cut, a graded change in haltere beating frequencies cannot be achieved,” she adds.

But Deora did find a way to overcome this challenge. Instead of trying to remove something from the halteres to disturb the system, she simply decided to ‘load’ them with tiny glue globs. As the combined weights of the glue and halteres increased beyond a threshold, the haltere beat frequencies began to decrease in discrete steps. But, interestingly, the wingbeat frequencies did not.

This meant that the wing–haltere coupling mechanism is unidirectional. While changes in wingbeat frequencies affect haltere movement, the opposite does not apply.

“In some ways, this is unsurprising,” says Deora. She explains that in most cases, if one component of a coupled system is much larger than the other, like the wings and halteres, the larger component’s effect on the smaller will be much stronger than the smaller one’s effect on the larger. “But I’m glad we were able to experimentally show this,” she adds.

Typically, when one thinks of movement control, neurons and neural circuits come to mind. However, biomechanics – the way that mechanical structures in the body are molded and linked physically – has a huge role to play in modulating and fine-tuning movement, especially when rapid reaction times are necessary.

“This is especially true for small organisms like flies. As a consequence of their small sizes, their wings need to beat really fast to build up enough force for aerodynamic lift. This, in turn, involves the need for rapid sensing to control movements. That’s where evolution has turned to biomechanics for solutions,” says Deora.