Complete neuroanatomy of dragonfly wings suggests direct sensing of aeroelastic deformations

Abstract

Fly-by-feel describes how flying animals capture aerodynamic information via their wings' sensory system to implement or enhance flight control. Traditional studies on animal flight emphasized controlling body stability via visual or inertial sensory inputs. In line with this, it has been demonstrated that wing sensory systems can provide inertial state estimation for the body. What about the state estimation of the wings themselves? Little is known about how flying animals utilize their wing sensory systems to monitor the dynamic state of their highly deformable wings. This study is a step toward a comprehensive investigation of how a flying animal senses aerodynamic and aeroelastic features of the wings relevant to flight control. Odonates: dragonflies and damselflies, are a great model for this because they have excellent flight performance and their wing structure has been extensively studied. Here, we developed a strategy to map the entire sensory system of Odonata wings via confocal microscopy. The result is the first complete map of a flying animal's wing sensory system, including both the external sensor morphologies and internal neuroanatomy. This complete search revealed over 750 sensors on each wing for one of the smallest dragonfly species and roughly half for a comparable size damselfly. We found over eight morphological classes of sensors, most of which resembled mechanosensors. Most sensors were innervated by a single neuron with an innervation pattern consistent with minimising wiring length. We further mapped the major veins of 13 Odonate species across 10 families and identified consistent sensor distribution patterns, with sensor count scaling with wing length. To explain the strain sensor density distribution along the major veins, we constructed a high-fidelity finite element model of a dragonfly wing based on micro-CT data. This flapping wing model revealed dynamic strain fields and suggested how increasing sensor count could allow encoding of different wing states. Taken together, the Odonate wing sensory system is well-equipped to implement sophisticated fly-by-feel flight control.

Viscous effects and complex local flow behaviors dominate hemolymph circulation in the living wings of locusts

“…For example, the dragonfly, a highly maneuverable aerial predator, may require relatively fast hemolymph flows to supply the extensive network of sensory structures throughout its wings. 6,10 In comparison, a migratory insect such as a monarch butterfly, which often glides along air currents and needs to maximize energetic efficiency to travel long distances without feeding, may instead benefit from slower wing hemolymph flows, which require less active pumping..In addition, flow speeds are likely to vary widely within insect orders such as Lepidoptera, which display enormous variation in body size.…”

“…12 Recent work has also confirmed that hemolymph circulation is necessary for the scent-producing organs on lepidopteran wings 4 and the hundreds of sensory hairs distributed across dragonfly wings to function properly. 6,10 Despite this wide range of important physiological functions, insect wings have primarily been studied in relation to their mechanical function during flight. Structurally, insect wings are composed of chitinous, tubular veins and thin, membranous regions 13 .…”

“…Hemolypmh circulation in the wing is critical for hydrating tissues, such as the highly elastic resilin 3 that enhances wing flexibility, and for supplying nutrients to living systems, including sensory organs such as scent-producing patches, sound-receiving tympana, and wind-sensing sensilla distributed across the wing. [4][5][6][7] During flight, the presence of hemolymph in the wings reduces aerodynamic instabilities like flutter 8,9 , and faster hemolymph flows are induced by flapping. 10 Despite the critical role of hemolymph circulation in maintaining healthy wing function, wings are often considered "lifeless" cuticle, and most measurements remain qualitative or employ coarse, bulk-flow techniques.…”

The molecular basis of macrochaete diversification highlighted by a single-cell atlas ofBicyclus anynanabutterfly pupal forewings

“…While scale cell color diversity is the most prominent feature of butterfly wings, wings also display a variety of other cell types that differentiate at multiple locations. Innervated sensory cells, often placed on top of veins (Dickerson et al, 2014;Yoshida and Emoto, 2011;Yoshida et al, 2001), are involved in mechanosensory or chemosensory functions (Aiello et al, 2021;Fabian et al, 2022;Hartenstein and Posakony, 1989) and glandular secretory cells are responsible for producing and secreting sex pheromones, mostly in males (Dion et al, 2016). How such wing cell type diversity is genetically and developmentally regulated remains largely unknown.…”