Bodybuilding Dragonflies: Costs and Benefits of Maximizing Flight Muscle

Marden, James H.

doi:10.1086/physzool.62.2.30156182

Cited by 223 publications

(163 citation statements)

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“…Our sample of L. pulchella dragonflies included both newly emerged adults whose body masses ranged from 202 to 342 mg and mature adults that ranged up to 751 mg. Much of the maturational change in body mass is attributable to development of the flight muscles (41), which hypertrophy and increase in aerobic metabolic capacity during adult maturation. Previous studies have shown that the fractional cross-sectional area of mitochondria increases from about 0.15 to 0.46 (31,41) between emergence and maturity, whereas the specific activity of an enzyme that is an indicator of aerobic metabolic activity (citrate synthase) increases by approximately 1.6-fold (J.H.M.…”

Section: Resultsmentioning

confidence: 99%

Alternative splicing, muscle calcium sensitivity, and the modulation of dragonfly flight performance

Marden

Fitzhugh

Wolf

et al. 1999

Proc. Natl. Acad. Sci. U.S.A.

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Calcium sensitivity of myosin cross-bridge activation in striated muscles commonly varies during ontogeny and in response to alterations in muscle usage, but the consequences for wholeorganism physiology are not well known. Here we show that the relative abundances of alternatively spliced transcripts of the calcium regulatory protein troponin T (TnT) vary widely in flight muscle of Libellula pulchella dragonflies, and that the mixture of TnT splice variants explains significant portions of the variation in muscle calcium sensitivity, wing-beat frequency, and an index of aerodynamic power output during free flight. Two size-distinguishable morphs differ in their maturational pattern of TnT splicing, yet they show the same relationship between TnT transcript mixture and calcium sensitivity and between calcium sensitivity and aerodynamic power output. This consistency of effect in different developmental and physiological contexts strengthens the hypothesis that TnT isoform variation modulates muscle calcium sensitivity and whole-organism locomotor performance. Modulating muscle power output appears to provide the ecologically important ability to operate at different points along a tradeoff between performance and energetic cost. S triated muscles from a variety of taxa show substantial interand intra-specific variation in the sensitivity of myosin crossbridge activation by calcium (1-6). Within individual animals, calcium sensitivity of muscle activation varies during ontogeny, training, and disease and appears to be one of the primary ways that striated muscles adjust to changes in contractile regimes (7-9). It generally is thought that varying the calcium sensitivity of muscle activation affects recruitment of force-generating cross-bridges during a calcium transient, thereby modulating the rate and amount of force and power output (7-12). However, little is presently known regarding the effects of variation in calcium sensitivity on whole-muscle contractile performance, locomotor ability, and energetics.Variation in muscle calcium sensitivity often involves changes in the molecular composition of the troponin-tropomyosin complex (7-9, 13). This group of molecules constitutes the molecular ''switch'' that turns myosin cross-bridge activity on and off in response to neurally induced calcium signals. Troponin T (TnT), one of the components of the troponin-tropomyosin complex, varies in isoform composition during development (14-17), training (18), and human heart failure (19,20). Changes in TnT isoform composition frequently correlate with variation in the calcium sensitivity of myosin cross-bridge activation (1-9), and experimental manipulations of TnT isoform composition have been shown to affect the calcium sensitivity of actomyosin ATPase (21). Point mutations in human cardiac TnT alter both calcium sensitivity and myosin cross-bridge kinetics (22,23). The emerging picture is that many regions of TnT interact in functionally significant ways with the other troponins, tropomyosin (7-9, 13), and perhaps with m...

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Section: Resultsmentioning

confidence: 99%

Alternative splicing, muscle calcium sensitivity, and the modulation of dragonfly flight performance

Marden

Fitzhugh

Wolf

et al. 1999

Proc. Natl. Acad. Sci. U.S.A.

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“…Because the proportion of unsuccessful predation attempts increases as capture success declines, less successful dragonflies are expending more energy on flight per unit of energy they gain through prey capture. This is likely to limit the amount of body mass they can gain, lowering fecundity and/or mating success (Marden 1989;Anholt 1991). In addition, if less successful hunters engage in more pursuits, in an attempt to compensate for their lower success rate, they may experience higher mortality owing to increased exposure to aerial predators (Anholt 1991).…”

Section: Discussionmentioning

confidence: 99%

“…Aerial predation is the only means by which odonates (dragonflies and damselflies) acquire resources, and is a critical component of fitness. The substantial mass gain that results from hunting contributes to flight muscle mass and mating success in males (Marden 1989), as well as to abdominal mass and fecundity in females (Anholt 1991). However, aerial predation is also a risky business: individuals that forage more and gain more weight have a higher mortality rate, presumably owing to the inherent risk of being preyed upon themselves while pursuing a meal (Anholt 1991).…”

Section: Introductionmentioning

confidence: 99%

Dynamics of animal movement in an ecological context: dragonfly wing damage reduces flight performance and predation success

2010

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Much of our understanding of the control and dynamics of animal movement derives from controlled laboratory experiments. While many aspects of animal movement can be probed only in these settings, a more complete understanding of animal locomotion may be gained by linking experiments on relatively simple motions in the laboratory to studies of more complex behaviours in natural settings. To demonstrate the utility of this approach, we examined the effects of wing damage on dragonfly flight performance in both a laboratory drop-escape response and the more natural context of aerial predation. The laboratory experiment shows that hindwing area loss reduces vertical acceleration and average flight velocity, and the predation experiment demonstrates that this type of wing damage results in a significant decline in capture success. Taken together, these results suggest that wing damage may take a serious toll on wild dragonflies, potentially reducing both reproductive success and survival.

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“…Thus, the unreliable nature of the male signal in this species appears for the most part to depend not on the costs of signal production or maintenance, but on the cost of high-quality muscle production. Indeed, muscle is relatively costly to produce [24] and operate [25,26], and muscle production has been shown to trade-off against other important fitnessrelated phenotypes, such as fecundity [27] and testes size [28] in a variety of invertebrate species. Given these and other life-history trade-offs with physiological traits [26], costs of performance may potentially constrain or otherwise impinge on honest signal production.…”

Section: Introductionmentioning

confidence: 99%

A performance-based cost to honest signalling in male green anole lizards (Anolis carolinensis)

2012

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Sexual signals are considered costly to produce and maintain under the handicap paradigm, and the reliability of signals is in turn thought to be maintained by these costs. Although previous studies have investigated the costly nature of signal production, few have considered whether honesty might be maintained not by the costliness of the signal itself, but by the costs involved in producing the signalled trait. If such a trait is itself costly to produce, then the burden of energetic investment may fall disproportionately on that trait, in addition to any costs of signal maintenance that may also be operating. Under limited resource conditions, these costs may therefore be great enough to disrupt an otherwise reliable signal-to-trait relationship. We present experimental evidence showing that dietary restriction decouples the otherwise honest relationship between a signal (dewlap size) and a whole-organism performance trait (bite force) in young adult male Anolis carolinensis lizards. Specifically, while investment in dewlap size is sustained under low-resource condition relative to the high-resource treatment, investment in bite force is substantially lower. Disruption of the otherwise honest dewlap size to bite force relationship is therefore driven by costs associated with the expression of performance rather than the costs of signal production in A. carolinensis .

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Bodybuilding Dragonflies: Costs and Benefits of Maximizing Flight Muscle

Cited by 223 publications

References 0 publications

Alternative splicing, muscle calcium sensitivity, and the modulation of dragonfly flight performance

Alternative splicing, muscle calcium sensitivity, and the modulation of dragonfly flight performance

Dynamics of animal movement in an ecological context: dragonfly wing damage reduces flight performance and predation success

A performance-based cost to honest signalling in male green anole lizards (Anolis carolinensis)

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