Evolution of Flight Muscle Contractility and Energetic Efficiency

Abstract

The powered flight of animals requires efficient and sustainable contractions of the wing muscles of various flying species. Despite their high degree of phylogenetic divergence, flight muscles in insects and vertebrates are striated muscles with similarly specialized sarcomeric structure and basic mechanisms of contraction and relaxation. Comparative studies examining flight muscles together with other striated muscles can provide valuable insights into the fundamental mechanisms of muscle contraction and energetic efficiency. Here, we conducted a literature review and data mining to investigate the independent emergence and evolution of flight muscles in insects, birds, and bats, and the likely molecular basis of their contractile features and energetic efficiency. Bird and bat flight muscles have different metabolic rates that reflect differences in energetic efficiencies while having similar contractile machinery that is under the selection of similar natural environments. The significantly lower efficiency of insect flight muscles along with minimized energy expenditure in Ca 2+ handling is discussed as a potential mechanism to increase the efficiency of mammalian striated muscles. A better understanding of the molecular evolution of myofilament proteins in the context of physiological functions of invertebrate and vertebrate flight muscles can help explore novel approaches to enhance the performance and efficiency of skeletal and cardiac muscles for the improvement of human health.

Oxygen Dependence of Flight Performance in Ageing Drosophila melanogaster

“…All things considered, at this point, we remain far from understanding the precise physiological mechanisms that determine age-related changes in the locomotory performance of insects, especially the relative contribution of neural and muscular processes. Nevertheless, insect leg movements are powered by muscles with synchronous contractions, while wing movements, at least in all flies and many other small insect species, are powered by muscles functioning with asynchronous contractions [ 80 , 81 , 82 ]. In the synchronous muscles, contractions are directly stimulated by impulses arriving from motor nerves, with one impulse per contraction.…”

Cytochrome c Oxidase at Full Thrust: Regulation and Biological Consequences to Flying Insects

“…Despite the lower energy costs of Ca 2+ cycling, the energy demand to sustain such high frequencies of AFM contractions is exceptionally high, with upper limits of mass-specific metabolic rates close to 1000 W/kg [ 36 ]. To accomplish this, AFM oxygen consumption rates usually rise 10–100 fold during rest to flight transition compared to ≈18-fold increase in mammalian muscles [ 37 , 38 , 39 ].…”

Amenability of Maruca vitrata (Lepidoptera: Crambidae) to gene silencing through exogenous administration and host-delivered dsRNA in pigeonpea (Cajanus cajan L.)

“…Though larvae are the most actively feeding stages of M. vitrata, the feeding is stopped during pupation when they undergo resting phase. The myo lament proteins which are conserved in ight muscles are comprised of actin-activated troponin-tropomyosin complex in all the vertebrates and invertebrates (Cao and Jin 2020) An interesting study on annual life-cycle of M. vitrata revealed that the highest ying activity was observed during late August to mid-October (Traore et al 2014). In our study, the collected larvae emerged into adults at the end of October-mid November.…”