Aging Enhances Indirect Flight Muscle Fiber Performance yet Decreases Flight Ability in Drosophila

Abstract

We investigated the effects of aging on Drosophila melanogaster indirect flight muscle from the whole organism to the actomyosin cross-bridge. Median-aged (49-day-old) flies were flight impaired, had normal myofilament number and packing, barely longer sarcomeres, and slight mitochondrial deterioration compared with young (3-day-old) flies. Old (56-day-old) flies were unable to beat their wings, had deteriorated ultrastructure with severe mitochondrial damage, and their skinned fibers failed to activate with calcium. Small-amplitude sinusoidal length perturbation analysis showed median-aged indirect flight muscle fibers developed greater than twice the isometric force and power output of young fibers, yet cross-bridge kinetics were similar. Large increases in elastic and viscous moduli amplitude under active, passive, and rigor conditions suggest that median-aged fibers become stiffer longitudinally. Small-angle x-ray diffraction indicates that myosin heads move increasingly toward the thin filament with age, accounting for the increased transverse stiffness via cross-bridge formation. We propose that the observed protein composition changes in the connecting filaments, which anchor the thick filaments to the Z-disk, produce compensatory increases in longitudinal stiffness, isometric tension, power and actomyosin interaction in aging indirect flight muscle. We also speculate that a lack of MgATP due to damaged mitochondria accounts for the decreased flight performance.

The effects of age and lifetime flight behavior on flight capacity inDrosophila melanogaster

“…The senescence of flight ability in aged insects is well established (Le Bourg and Minois, 1999;Magwere et al, 2006;Simon et al, 2006;Miller et al, 2008), and the results of this study expand the understanding of this process by demonstrating that variation in lifetime flight behavior, in addition to age, affects the onset and pace of flight senescence. Elevated flight frequency in the IF group moderately hastened the onset of flight senescence compared with the VF group, and the pace of flight senescence in the VF and IF flies between 35 and 65 days of age was the most rapid over any time period in the study.…”

“…Flight performance, WBF and metabolic rate decreased in older flies, and such trends are well documented for Drosophila and other insects (Le Bourg and Minois, 1999;Tofilski, 2000;Simon et al, 2006;Miller at al., 2008;Williams et al, 2008;Vance et al, 2009). …”

“…The Journal of Experimental Biology (2014) In the Oregon R strain of D. melanogaster, flight performance and WBF decrease after 28 and 42 days of age, respectively (Miller et al, 2008). Exploratory activity (distance travelled away from a central location per unit time), the proportion of time spent flying and negative geotaxis also decrease with age in D. melanogaster (Le Bourg and Minois, 1999;Gargano et al, 2005;Magwere et al, 2006;Simon et al, 2006).…”

“…The flight muscles lose antioxidant capacity and accrue oxidative damage to lipids, proteins and DNA (Yan and Sohal, 2000;Magwere et al, 2006;Seehuus et al, 2006;Williams et al, 2008), and such damage possibly underlies the age-based impairment of glycolytic and electron transport chain enzymes (Schippers et al, 2006;Schippers et al, 2010) and the ultrastructural degeneration of flight muscle mitochondria and sarcomeres (Sacktor and Shimada, 1972;Fernandez-Winckler and da Cruz-Landim, 2008;Miller et al, 2008), which in turn might explain the lower metabolic rates of aged flies in the VF and IF groups. Flight muscle mass decreases steadily with age in certain insects (Ready and Josephson, 1982;Stjernholm and Karlsson, 2008), although this effect did not occur in our study (Fig.…”

Variations in the ultrastructure of the flight muscles of the polymorphic cricket, Gryllus firmus (Orthoptera: Gryllidae)

“…Decreases in flight performance are due to reduced ATP availability and myosin kinetics in isolated fibers, which results in a decrease in wing-beat frequency and might indicate that differences in flight directly reflect the number of mitochondria (Molloy et al, 1997;Swank et al, 2006;Miller et al, 2008). 584 Fig.…”