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 Ca²⁺ 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.

Keywords: bat; bird; energetic efficiency; flight muscle; insect; molecular evolution; myofilament proteins; striated muscle.

FIGURE 1

Evolutionary emergence of insects, birds, and bats. The phylogenetic tree summarized from literature data (Nelson and Tidwell, 1987; Tokita et al., 2012; Brusatte et al., 2015) illustrates the geological times when the Insecta and Aves classes and Chiroptera order of flying animals emerged. Insects evolved flight around 400 million years ago (Mya), ancient flying birds appeared 150 Mya and bats emerged around 50 Mya. The historical atmospheric oxygen content curve (Dudley, 1998) illustrates the similar hyperoxia environments when analogous aerial locomotion emerged in these flying animals.

FIGURE 2

Direct and indirect insect flight muscles. (Left) Wing movement driven by synchronous direct flight muscles. Larger insects, such as dragonflies and locusts, use direct flight muscle for wing beating during flight. Contraction of elevator muscles pulls wing up, and depressor muscles pull wings down. (Right) Wing movement of fruit fly driven by asynchronous indirect flight muscles. Dorsal vertical muscles (DVM) pull on the thorax roof to produce upstroke of wings while stretching the dorsal longitudinal muscles (DLM). Subsequent contraction of DLM causes shortened anterior and posterior ends of the thorax resulting in downstroke of wings and DVM stretching to induce the next stretch-activated cycle. The illustrations were summarized from literature information (Iwamoto, 2011).

FIGURE 3

Comparison of sarcomere structures of (A) vertebrate and (B) invertebrate flight muscles. Invertebrate and vertebrate flight muscles contain similar sarcomeric structures consisting of overlapping myosin thick filaments and actin thin filaments with homologous but diverged scaffolding proteins. Invertebrate indirect flight muscles (IFM) have longer sarcomeres compared to vertebrate flight muscle and narrower I-bands in comparison with the vertebrate sarcomeres. The illustrations were summarized from literature information (Hooper et al., 2008; Lange et al., 2020).

FIGURE 4

Glu-rich C-terminal extension of insect TnT. Amino acid sequences encoded by exon 11 or exon 12 of representative insect TnT genes are aligned to identify residue similarity and to illustrate the insect-specific C-terminal extension enriched with Glu residues. The Glu contents appear positively correlating to the frequencies of wing beat of these species (Snelling et al., 2012). GenBank accession numbers of the sequences used are: Dragonfly TnT, AAD33604.1; locust TnT, AVCP010016941; Drosophila TnT, NP_525088; Bee TnT, NP_001035348.1.

FIGURE 5

Paired dot plots of amino acid sequence similarities between the Glu-rich segment of insect TnT and sarcoplasmic reticulum histidine-rich calcium binding protein (HRC). Analyzed using DNAStar MegAlign Dotplot software method of pairwise alignment, the C-terminal extension of bee TnT matches with high similarity to segments in human (A) and mouse (B) HRC (indicated with dashed circles), suggesting an analogous function as a myofilament Ca²⁺ reservoir. The matched regions and degree of sequence similarity are indicated by the different colors of the diagonal lines. Shown in the color bar below the panels, red represents the highest similarity while purple shows the least similarity. The GenBank accession numbers for the sequences used are: Human HRC binding protein, AAH94691.1; mouse cardiac HRC protein, AAD42061.1; Bee TnT, PBC29029.1.

FIGURE 6

Paired dot plots of amino acid sequence similarities between TnT from bat fast twitch skeletal muscle, avian pectoral and leg muscles, and mouse fast twitch skeletal muscle. Analyzed using Dotplot method of DNAStar MegAlign software, bat TnT lacks the Glu-rich N-terminal segment found in avian pectoral TnT (A, indicated by the dash circle) whereas it has similar overall structure to that of avian leg muscle TnT (B) and mouse fast TnT (C). Shown in the color bar below the panels, red represents the highest similarity while purple shows the lowest similarity. The GenBank accession numbers for the sequences used are: Bat fast skeletal muscle TnT, XP_028371248.1; avian pectoral fast skeletal TnT, AAG44258.1; avian leg muscle TnT, BAC76600.1; mouse fast skeletal muscle TnT, AAB67285.1.