The evolution of two distinct strategies of moth flight

Aiello, Brett R.; Sikandar, Usama Bin; Minoguchi, Hajime; Bhinderwala, Burhanuddin; Hamilton, Chris A.; Kawahara, Akito Y.; Sponberg, Simon

doi:10.1098/rsif.2021.0632

Cited by 20 publications

(23 citation statements)

References 60 publications

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“…The flat frequency response of the thorax also has implications for the biomechanical pressures and constraints that apply over evolutionary timescales. Even within closely related subgroups of insects, there is sometimes wide variability in wingbeat frequency, such as in the bombycoid moths, whose wingbeat frequency range spans nearly an order of magnitude from 8 to 64 Hz [53]. A structurally damped thorax may reduce the amount of concomitant neuromuscular and exoskeletal coevolution necessary to evolve different wingbeat frequencies, contributing to the lability of wingbeat frequency as a functional trait.…”

Section: Discussionmentioning

confidence: 99%

Structural damping renders the hawkmoth exoskeleton mechanically insensitive to non-sinusoidal deformations

Wold

Lynch

Gravish

et al. 2023

J. R. Soc. Interface.

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Muscles act through elastic and dissipative elements to mediate movement, which can introduce dissipation and filtering which are important for energetics and control. The high power requirements of flapping flight can be reduced by an insect's exoskeleton, which acts as a spring with frequency-independent material properties under purely sinusoidal deformation. However, this purely sinusoidal dynamic regime does not encompass the asymmetric wing strokes of many insects or non-periodic deformations induced by external perturbations. As such, it remains unknown whether a frequency-independent model applies broadly and what implications it has for control. We used a vibration testing system to measure the mechanical properties of isolated Manduca sexta thoraces under symmetric, asymmetric and band-limited white noise deformations. The asymmetric and white noise conditions represent two types of generalized, multi-frequency deformations that may be encountered during steady-state and perturbed flight. Power savings and dissipation were indistinguishable between symmetric and asymmetric conditions, demonstrating that no additional energy is required to deform the thorax non-sinusoidally. Under white noise conditions, stiffness and damping were invariant with frequency, suggesting that the thorax has no frequency-dependent filtering properties. A simple flat frequency response function fits our measured frequency response. This work demonstrates the potential of materials with frequency-independent damping to simplify motor control by eliminating any velocity-dependent filtering that viscoelastic elements usually impose between muscle and wing.

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Section: Discussionmentioning

confidence: 99%

Structural damping renders the hawkmoth exoskeleton mechanically insensitive to non-sinusoidal deformations

Wold

Lynch

Gravish

et al. 2023

J. R. Soc. Interface.

View full text Add to dashboard Cite

show abstract

“…The flat frequency response of the thorax also has implications for the biomechanical pressures and constraints that apply over evolutionary timescales. Even within closely related subgroups of insects, there is sometimes wide variability in wingbeat frequency, such as in the Bombycoid moths, whose wingbeat frequency range spans nearly an order of magnitude from 8-64 Hz ( 52 ). A structurally damped thorax may reduce the amount of concomitant neuromuscular and exoskeletal coevolution necessary to evolve different wingbeat frequencies, contributing to the lability of wingbeat frequency as a functional trait.…”

Section: Discussionmentioning

confidence: 99%

Structural damping renders the insect exoskeleton mechanically insensitive to non-sinusoidal deformations

Wold

Lynch

Gravish

et al. 2022

Preprint

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Muscles act through elastic and dissipative elements to mediate movement, but these elements can introduce dissipation and filtering which are important for energetics and control. The high power requirements of flapping flight can be reduced by the insect's exoskeleton, which acts as a structurally damped spring under purely sinusoidal deformation. However, this purely sinusoidal dynamic regime does not encompass the asymmetric wing strokes of many insects or non-periodic deformations induced by external perturbations. As such, it remains unknown whether a structural damping model applies broadly and what implications it has for control. We used a vibration testing system to measure the mechanical properties of isolatedManduca sextathoraces under symmetric, asymmetric, and band-limited white noise deformations. We measured a thoracic stiffness of 2980Nm−1at 25 Hz and physiological peak-to-peak amplitude of 0.92 mm. Power savings and dissipation were indistinguishable between symmetric and asymmetric conditions, demonstrating that no additional energy is required to deform the thorax non-sinusoidally. Under white noise conditions, stiffness and damping were invariant with frequency, which is consistent with a structural damping model and suggests the thorax has no frequency-dependent filtering properties. A simple flat frequency response function fits our measured frequency response. This work demonstrates the potential of structurally damped materials to simplify motor control by eliminating any velocity-dependent filtering that viscoelastic elements usually impose between muscle and appendage.

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“…While tails have originated multiple independent times across the Saturniidae family, they are not the norm and aside from Actias, tailed genera are not as speciose as many other non-tailed lineages [10,11]. The origin and proliferation of tails could be limited by other pressures, including flight mechanics [34,35], thermoregulation [36] or pupal metabolic costs [37]. More work parameterizing the flight kinematics of naturally tailed versus non-tailed moths in flight, as well as pre-flight warm-up time or pupal development energetics, etc., will help elucidate the physical limits of tail elongation.…”

Section: Discussionmentioning

confidence: 99%

Testing bird-driven diurnal trade-offs of the moon moth's anti-bat tail

et al. 2023

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Traits are often caught in a dynamic tension of countervailing evolutionary pressures. Trade-offs can be imposed by predators evolutionarily curtailing the conspicuousness of a sexually selected trait, or acting in opposition to another natural selection pressure, for instance, a different predator with a divergent hunting strategy. Some moon moths (Saturniidae) have long hindwing tails that thwart echolocating bat attacks at night, allowing the moth to escape. These long tails may come at a cost, however, if they make the moth's roosting form more conspicuous to visually foraging predators during the day. To test this potential trade-off, we offered wild-caught Carolina wrens ( Thryothorus ludovicianus ) pastry dough models with real Actias luna wings that were either intact or had tails experimentally removed. We video recorded wrens foraging on models and found that moth models with tails did not experience increased detection and attack by birds. Thus, this elaborate trait, while obvious to human observers, does not seem to come at a cost of increased avian predator attention. The evolution of long hindwing tails, likely driven by echolocating predators at night, does not seem to be limited by opposing diurnal constraints. This study demonstrates the importance of testing presumed trade-offs and provides hypotheses for future testing.

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The evolution of two distinct strategies of moth flight

Cited by 20 publications

References 60 publications

Structural damping renders the hawkmoth exoskeleton mechanically insensitive to non-sinusoidal deformations

Structural damping renders the hawkmoth exoskeleton mechanically insensitive to non-sinusoidal deformations

Structural damping renders the insect exoskeleton mechanically insensitive to non-sinusoidal deformations

Testing bird-driven diurnal trade-offs of the moon moth's anti-bat tail

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