Adult Drosophila muscle morphometry through microCT reveals dynamics during ageing

Abstract

Indirect flight muscles (IFMs) in adult Drosophila provide the key power stroke for wing beating. They also serve as a valuable model for studying muscle development. An age-dependent decline in Drosophila free flight has been documented, but its relation to gross muscle structure has not yet been explored satisfactorily. Such analyses are impeded by conventional histological preparations and imaging techniques that limit exact morphometry of flight muscles. In this study, we employ microCT scanning on a tissue preparation that retains muscle morphology under homeostatic conditions. Focusing on a subset of IFMs called the dorsal longitudinal muscles (DLMs), we find that DLM volumes increase with age, partially due to the increased separation between myofibrillar fascicles, in a sex-dependent manner. We have uncovered and quantified asymmetry in the size of these muscles on either side of the longitudinal midline. Measurements of this resolution and scale make substantive studies that test the connection between form and function possible. We also demonstrate the application of this method to other insect species making it a valuable tool for histological analysis of insect biodiversity.

Distinct Aging-Vulnerable and -Resilient Trajectories of Specific Motor Circuit Functions in Oxidation- and Temperature-StressedDrosophila

“…1 D , F , 7 B 7 ), suggesting the presence of effective homeostatic adjustments to overcome aging-associated changes in biomechanical properties of flight muscles and thoracic case. As previously reported ( Miller et al, 2008 ), WBF is stable beyond the median life span despite marked changes in muscle structure and stiffness (see also Chaturvedi et al, 2019 ). Despite the nearly invariant WBFs, we found the flight pattern generator circuit driving DLM displayed a clear and largely monotonic increase in firing rate with age ( Figs.…”

“…with stable WBFs (Figure 1D, F; Figure 7B-7), suggesting the presence of effective homeostatic adjustments to overcome aging-associated changes in biomechanical properties of flight muscles and thoracic case. As previously reported (Miller et al, 2008), WBF is stable beyond the median lifespan in spite of marked changes in muscle structure and stiffness (see also Chaturvedi et al, 2019). Despite the nearly invariant WBFs, we found the flight pattern generator circuit driving DLM displayed a clear and largely monotonic increase in firing rate with age (Figure 1E, Figure namely, increasing the firing rate of muscle Ca 2+ action potential to retain appropriate intracellular Ca 2+ levels for powering sustained flight in myogenic stretch-activated DLMs (Gordon & Dickinson, 2006;Lehmann et al, 2013;Pringle, 1978).…”

Heterogeneous distribution of mRNAs within flight muscle fibers, and implications for function

“…Six pairs of DLMs are visible on either side of the mid-line (marked by star), which are guarded by DVMs (another subset of indirect flight muscles, marked by circle) and TDT/jump muscle (marked by triangle) at the sides (Fig1B). We speculated that differences in the proximity to tendons, innervation and tracheation, apart from hitherto unannotated internal cytological differences along the length of DLMs (~500-800μm long) may contribute to a possible difference in mRNA localization [22,25]. In the absence of obvious landmarks separating DLMs into lengthwise sections, we chose to define regions by cross-sectional planes separating the three pairs of legs.…”

Development of the indirect flight muscles of Aedes aegypti, a main arbovirus vector

“…These results coincide with our observations where the number of DLM fascicles was constant, but in DVMs in the groups 1 and 2, and despite the small number of samples analyzed, variations in myotube numbers were seen [ 56 ]. The regulation of muscle size and number during IFMs formation in D. melanogaster is controlled by a balance between fusion and proliferation during larval and pupal stages [ 56 , 62 – 64 ].…”