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Synopsis Paleozoic skies were ruled by extinct odonatopteran insects called “griffenflies,” some with wingspans 3 times that of the largest extant dragonflies and 10 times that of common extant dragonflies. Previous studies suggested that flight was possible for larger fliers because of higher atmospheric oxygen levels, which would have increased air density. We use actuator disk theory to evaluate this hypothesis. Actuator disk theory gives similar estimates of induced power as have been estimated for micro-air vehicles based on insect flight. We calculate that for a given mass of griffenfly, and assuming isometry, a higher density atmosphere would only have reduced the induced power required to hover by 11%, which would have supported a flyer 3% larger in linear dimensions. Steady-level forward flight would have further reduced induced power but could only account for a flier 5% larger in linear dimensions. Further accounting for the higher power available due to high-oxygen air and assuming isometry, we calculate that the largest flyer hovering would have been only 1.19 times longer than extant dragonflies. We also consider known allometry in dragonflies and estimated allometry in extinct griffenflies. But such allometry only increases flyer size to 1.22 times longer while hovering. We also consider profile and parasite power, but both would have been higher in denser air and thus would not have enhanced the flyability of larger griffenflies. The largest meganeurid griffenflies might have adjusted flight behaviors to reduce power required. Alternatively, the scaling of flight muscle power may have been sufficient to support the power demands of large griffenflies. In literature estimates, mass-specific power output scales as mass0.24 in extant dragonflies. We need only more conservatively assume that mass-specific muscle power scales with mass0, when combined with higher oxygen concentrations and induced power reductions in higher-density air to explain griffenflies 3.4 times larger than extant odonates. Experimental measurement of flight muscle power scaling in odonates is necessary to test this hypothesis. 

Synopsis 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.