scholarly journals Flightin maintains myofilament lattice organization required for optimal flight power and courtship song quality in Drosophila

2017 ◽  
Vol 284 (1854) ◽  
pp. 20170431 ◽  
Author(s):  
Samya Chakravorty ◽  
Bertrand C. W. Tanner ◽  
Veronica Lee Foelber ◽  
Hien Vu ◽  
Matthew Rosenthal ◽  
...  

The indirect flight muscles (IFMs) of Drosophila and other insects with asynchronous flight muscles are characterized by a crystalline myofilament lattice structure. The high-order lattice regularity is considered an adaptation for enhanced power output, but supporting evidence for this claim is lacking. We show that IFMs from transgenic flies expressing flightin with a deletion of its poorly conserved N-terminal domain ( fln ΔN62 ) have reduced inter-thick filament spacing and a less regular lattice. This resulted in a decrease in flight ability by 33% and in skinned fibre oscillatory power output by 57%, but had no effect on wingbeat frequency or frequency of maximum power output, suggesting that the underlying actomyosin kinetics is not affected and that the flight impairment arises from deficits in force transmission. Moreover, we show that fln ΔN62 males produced an abnormal courtship song characterized by a higher sine song frequency and a pulse song with longer pulses and longer inter-pulse intervals (IPIs), the latter implicated in male reproductive success. When presented with a choice, wild-type females chose control males over mutant males in 92% of the competition events. These results demonstrate that flightin N-terminal domain is required for optimal myofilament lattice regularity and IFM activity, enabling powered flight and courtship song production. As the courtship song is subject to female choice, we propose that the low amino acid sequence conservation of the N-terminal domain reflects its role in fine-tuning species-specific courtship songs.

2001 ◽  
Vol 204 (20) ◽  
pp. 3457-3470 ◽  
Author(s):  
James H. Marden ◽  
Gail H. Fitzhugh ◽  
Mahasweta Girgenrath ◽  
Melisande R. Wolf ◽  
Stefan Girgenrath

SUMMARYThe flight muscles of Libellula pulchella dragonflies contain a mixture of six alternatively spliced transcripts of a single troponin T (TnT) gene. Here, we examine how intraspecific variation in the relative abundance of different TnT transcripts affects the Ca2+ sensitivity of skinned muscle fibers and the performance of intact muscles during work-loop contraction regimes that approximate in vivo conditions during flight. The relative abundance of one TnT transcript, or the pooled relative abundance of two TnT transcripts, showed a positive correlation with a 10-fold range of variation in Ca2+ sensitivity of skinned fibers (r2=0.77, P<0.0001) and a threefold range in peak specific force (r2=0.74, P<0.0001), specific work per cycle (r2=0.54; P<0.0001) and maximum specific power output (r2=0.48, P=0.0005) of intact muscle. Using these results to reanalyze previously published data for wing kinematics during free flight, we show that the relative abundances of these particular transcripts are also positively correlated with wingbeat frequency and amplitude. TnT variation alone may be responsible for these effects, or TnT variation may be a marker for changes in a suite of co-regulated molecules. Dragonflies from two ponds separated by 16 km differed significantly in both TnT transcript composition and muscle contractile performance, and within each population there are two distinct morphs that showed different maturational trajectories of TnT transcript composition and muscle contractility. Thus, there is broad intraspecific variability and a high degree of population structure for contractile performance phenotypes, TnT ribotypes and ontogenetic patterns involving these traits that affect locomotor performance.


Genetics ◽  
1985 ◽  
Vol 111 (4) ◽  
pp. 845-868
Author(s):  
C C Laurie-Ahlberg ◽  
P T Barnes ◽  
J W Curtsinger ◽  
T H Emigh ◽  
B Karlin ◽  
...  

ABSTRACT The major goal of the studies reported here was to determine the extent to which genetic variation in the activities of the enzymes participating in flight metabolism contributes to variation in the mechanical power output of the flight muscles in Drosophila melanogaster. Isogenic chromosome substitution lines were used to partition the variance of both types of quantitative trait into genetic and environmental components. The mechanical power output was estimated from the wingbeat frequency, wing amplitude and wing morphology of tethered flies by applying the aerodynamic models of Weis-Fogh and Ellington. There were three major results. (1) Chromosomes sampled from natural populations provide a large and repeatable genetic component to the variation in the activities of most of the 15 flight metabolism enzymes investigated and to the variation in the mechanical power output of the flight muscles. (2) The mechanical power output is a sensitive indicator of the rate of flight metabolism (i.e., rate of oxygen consumption during tethered flight). (3) In spite of (1) and (2), no convincing cases of individual enzyme effects on power output were detected, although the number and sign of the significant enzyme-power correlations suggests that such effects are not totally lacking.


2001 ◽  
Vol 204 (21) ◽  
pp. 3601-3619 ◽  
Author(s):  
Graham N. Askew ◽  
Richard L. Marsh ◽  
Charles P. Ellington

SUMMARYBlue-breasted quail (Coturnix chinensis) were filmed during take-off flights. By tracking the position of the centre of mass of the bird in three dimensions, we were able to calculate the power required to increase the potential and kinetic energy. In addition, high-speed video recordings of the position of the wings over the course of the wing stroke, and morphological measurements, allowed us to calculate the aerodynamic and inertial power requirements. The total power output required from the pectoralis muscle was, on average, 390 W kg–1, which was similar to the highest measurements made on bundles of muscle fibres in vitro (433 W kg–1), although for one individual a power output of 530 W kg–1 was calculated. The majority of the power was required to increase the potential energy of the body. The power output of these muscles is the highest yet found for any muscle in repetitive contractions.We also calculated the power requirements during take-off flights in four other species in the family Phasianidae. Power output was found to be independent of body mass in this family. However, the precise scaling of burst power output within this group must await a better assessment of whether similar levels of performance were measured across the group. We extended our analysis to one species of hawk, several species of hummingbird and two species of bee. Remarkably, we concluded that, over a broad range of body size (0.0002–5 kg) and contractile frequency (5–186 Hz), the myofibrillar power output of flight muscles during short maximal bursts is very high (360–460 W kg–1) and shows very little scaling with body mass. The approximate constancy of power output means that the work output varies inversely with wingbeat frequency and reaches values of approximately 30–60 J kg–1 in the largest species.


Author(s):  
Amy K. Loya ◽  
Sarah K. Van Houten ◽  
Bernadette M. Glasheen ◽  
Douglas M. Swank

A muscle undergoing cyclical contractions requires fast and efficient muscle activation and relaxation to generate high power with relatively low energetic cost. To enhance activation and increase force levels during shortening, some muscle types have evolved stretch activation (SA), a delayed increased in force following rapid muscle lengthening. SA's complementary phenomenon is shortening deactivation (SD), a delayed decrease in force following muscle shortening. SD increases muscle relaxation, which decreases resistance to subsequent muscle lengthening. While it might be just as important to cyclical power output, SD has received less investigation than SA. To enable mechanistic investigations into SD and quantitatively compare it to SA, we developed a protocol to elicit SA and SD from Drosophila and Lethocerus indirect flight muscles (IFM) and Drosophila jump muscle. When normalized to isometric tension, Drosophila IFM exhibited a 118% SD tension decrease, Lethocerus IFM dropped by 97%, and Drosophila jump muscle decreased by 37%. The same order was found for normalized SA tension: Drosophila IFM increased by 233%, Lethocerus IFM by 76%, and Drosophila jump muscle by only 11%. SD occurred slightly earlier than SA, relative to the respective length change, for both IFMs; but SD was exceedingly earlier than SA for jump muscle. Our results suggest SA and SD evolved to enable highly efficient IFM cyclical power generation and may be caused by the same mechanism. However, jump muscle SA and SD mechanisms are likely different, and may have evolved for a role other than to increase the power output of cyclical contractions.


1989 ◽  
Vol 142 (1) ◽  
pp. 17-29 ◽  
Author(s):  
C. J. PENNYCUICK ◽  
M. R. FULLER ◽  
LYNNE McALLISTER

Two Harris' hawks were trained to fly along horizontal and climbing flight paths, while carrying loads of various masses, to provide data for estimating available muscle power during short flights. The body mass of both hawks was about 920 g, and they were able to carry loads up to 630 g in horizontal flight. The rate of climb decreased with increasing all-up mass, as also did the climbing power (product of weight and rate of climb). Various assumptions about the aerodynamic power in low-speed climbs led to estimates of the maximum power output of the flight muscles ranging from 41 to 46 W. This, in turn, would imply a stress during shortening of around 210 kPa. The effects of a radio package on a bird that is raising young should be considered in relation to the food load that the forager can normally carry, rather than in relation to its body mass.


2020 ◽  
Vol 223 (21) ◽  
pp. jeb225839 ◽  
Author(s):  
Joseph W. Bahlman ◽  
Vikram B. Baliga ◽  
Douglas L. Altshuler

ABSTRACTBirds that use high flapping frequencies can modulate aerodynamic force by varying wing velocity, which is primarily a function of stroke amplitude and wingbeat frequency. Previous measurements from zebra finches (Taeniopygia guttata) flying across a range of speeds in a wind tunnel demonstrate that although the birds modulated both wingbeat kinematic parameters, they exhibited greater changes in stroke amplitude. These two kinematic parameters contribute equally to aerodynamic force, so the preference for modulating amplitude over frequency may instead derive from limitations of muscle physiology at high frequency. We tested this hypothesis by developing a novel in situ work loop approach to measure muscle force and power output from the whole pectoralis major of zebra finches. This method allowed for multiple measurements over several hours without significant degradation in muscle power. We explored the parameter space of stimulus, strain amplitude and cycle frequencies measured previously from zebra finches, which revealed overall high net power output of the muscle, despite substantial levels of counter-productive power during muscle lengthening. We directly compared how changes to muscle shortening velocity via strain amplitude and cycle frequency affected muscle power. Increases in strain amplitude led to increased power output during shortening with little to no change in power output during lengthening. In contrast, increases in cycle frequency did not lead to increased power during shortening but instead increased counter-productive power during lengthening. These results demonstrate why at high wingbeat frequency, increasing wing stroke amplitude could be a more effective mechanism to cope with increased aerodynamic demands.


1995 ◽  
Vol 198 (6) ◽  
pp. 1259-1273 ◽  
Author(s):  
B Tobalske

Electromyographic (EMG) and kinematic data were collected from European starlings (Sturnus vulgaris) flying at a range of speeds from 8 to 18 m s-1 in a variable-speed windtunnel. Their flight at all speeds consisted of alternating flapping and non-flapping phases. Wing postures during non-flapping phases included glides, partial-bounds and bounds. Glides were performed proportionally more often within each speed and were longer in duration than either of the other two non-flapping postures, but the percentage of bounds increased markedly with increasing flight speed. The shift from flap-gliding at slow speeds towards flap-bounding at fast speeds was consistent with reducing mean power output relative to continuous flapping. The starlings often combined more than one non-flapping posture within a single non-flapping period. Transitions between non-flapping postures, as well as transitions between bounds and subsequent flapping, were classified as 'pull-outs'. Pull-outs consisted of an increase in wingspan but no change in wingtip elevation. The pectoralis and supracoracoideus exhibited electrical activity during glides but not during bounds. The scapulohumeralis caudalis was not active during glides, but this muscle and the supracoracoideus were typically active during partial-bounds and pull-out phases. The scapulohumeralis caudalis occasionally showed activity during bounds, which may reflect its role as a humeral retractor. The frequency and duration of non-flapping intervals in starlings were less during EMG experiments than during non-implanted flights. During flapping phases, relative intensity and duration of EMG signal and wingbeat frequency increased with flight speed, whereas flapping or non-flapping cycle duration, the percentage of a cycle spent flapping and the number of wingbeats in a cycle were all greatest at 8 m s-1. Wingbeat amplitude was smaller at intermediate speeds, but differences among speeds were not significant. These variables allowed indirect estimates of power output and suggested that minimum power speed for starlings was near 12 m s-1 and that power output increased at both slower and faster speeds. Within windtunnel speeds, muscle activity changed in relation to wingspan at mid-upstroke, wingtip excursion, wingbeat frequency, acceleration, velocity, altitude and horizontal position.


2021 ◽  
Author(s):  
Pravin Kumar ◽  
Erin Schexnaydre ◽  
Karim Rafie ◽  
Ilya Terenin ◽  
Vasili Hauryliuk ◽  
...  

Nonstructural protein 1 (Nsp1) is a major pathogenicity factor of SARS-CoV-2. It inhibits host-cell translation, primarily through a direct interaction between its C-terminal domain and the mRNA entry channel of the 40S small ribosomal subunit, with an N-terminal β-barrel domain fine-tuning the inhibition and promoting selective translation of viral mRNA. SARS-CoV-2 nsp1 is a target of recurring deletions, some of which are associated with altered COVID-19 disease progression. To provide the biochemical basis for this, it is essential to characterize the efficiency of translational inhibition by the said protein variants. Here, we use an in vitro translation system to investigate the translation inhibition capacity of a series of clinically observed Nsp1 deletion variants. We find that a frequently observed deletion of residues 79-89 destabilized the N-terminal domain (NTD) and severely reduced the capacity of Nsp1 to inhibit translation. Interestingly, shorter deletions in the same region have been reported to effect the type I interferon response but did not affect translation inhibition, indicating a possible translation-independent role of the Nsp1 NTD in interferon response modulation. Taken together, our data provide a mechanistic basis for understanding how deletions in Nsp1 influence SARS-CoV-2 induction of interferon response and COVID-19 progression.


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