Insect Flight: State of the Field and Future Directions.

The evolution of flight in an early winged insect ancestral lineage is recognized as a key adaptation explaining the unparalleled success and diversification of insects. Subsequent transitions and modifications to flight machinery, including secondary reductions and losses, also play a central role in shaping the impacts of insects on broadscale geographic and ecological processes and patterns in the present and future. Given the importance of insect flight, there has been a centuries-long history of research and debate on the evolutionary origins and biological mechanisms of flight. Here, we revisit this history from an interdisciplinary perspective, discussing recent discoveries regarding the developmental origins, physiology, biomechanics, and neurobiology and sensory control of flight in a diverse set of insect models. We also identify major outstanding questions yet to be addressed and provide recommendations for overcoming current methodological challenges faced when studying insect flight, which will allow the field to continue to move forward in new and exciting directions. By integrating mechanistic work into ecological and evolutionary contexts, we hope that this synthesis promotes and stimulates new interdisciplinary research efforts necessary to close the many existing gaps about the causes and consequences of insect flight evolution.

Flies tune the activity of their multifunctional gyroscope.

Members of the order Diptera, the true flies, are among the most maneuverable flying animals. These aerial capabilities are partially attributed to flies' possession of halteres, tiny club-shaped structures that evolved from the hindwings and play a crucial role in flight control. Halteres are renowned for acting as biological gyroscopes that rapidly detect rotational perturbations and help flies maintain a stable flight posture. Additionally, halteres provide rhythmic input to the wing steering system that can be indirectly modulated by the visual system. The multifunctional capacity of the haltere is thought to depend on arrays of embedded mechanosensors called campaniform sensilla that are arranged in distinct groups on the haltere's dorsal and ventral surfaces. Although longstanding hypotheses suggest that each array provides different information relevant to the flight control circuitry, we know little about how the haltere campaniforms are functionally organized. Here, we use in vivo calcium imaging during tethered flight to obtain population-level recordings of the haltere sensory afferents in specific fields of sensilla. We find that haltere feedback from both dorsal fields is continuously active, modulated under closed-loop flight conditions, and recruited during saccades to help flies actively maneuver. We also find that the haltere's multifaceted role may arise from the steering muscles of the haltere itself, regulating haltere stroke amplitude to modulate campaniform activity. Taken together, our results underscore the crucial role of efferent control in regulating sensor activity and provide insight into how the sensory and motor systems of flies coevolved.