Scaling of animal musculoskeletal performance. One of the most clearly established facts in muscle physiology is that the maximum force exerted by a muscle is determined by its cross-sectional area, i.e. the number of actomyosin cross-bridges working in parallel. Because of this relationship and the general shape similarity of most muscles, muscle force output scales consistently as muscle mass^0.67, or as muscle cross-sectional area, among animals that vary greatly in body size.

This suggests that as animals increase in size, they would experience a force deficit, since the body weight that requires support by muscles increases “faster” than the force output attainable by muscles (i.e., muscles of larger animals would need to produce more force per cross-sectional area, but may not be able to). However, muscles rarely exert their forces directly on the external environment without some form of mechanical linkage in which lever arms and their associated mechanical advantage either enhance or reduce the forces generated by muscles. Moreover, few musculoskeletal systems move organisms using their maximum force generation capacity. So, force output by intact musculoskeletal systems may be quite different than that of individual muscles, and the scaling of this force output may differ markedly from mass^0.67, especially during locomotion.

We have previously examined this question in flying dragonflies (see here), but they are not the only organisms that transmit force output by single muscles via musculoskeletal linkages (tendons and other skeletal components). Internal musculoskeletal dynamics and force distribution mechanisms inside animals are often unknown or at best understudied. We continue to investigate such mechanisms and dynamics in different types of animal motors, for one to establish to what extent the dragonfly “solution” (see again here) to unequal scaling of muscle force output and body weight support requirements is unique or more general among animals.

Body weight sensation. A long term goal of the lab is to determine if animals know at a physiological level how much they weigh, and, if so, how they make homeostatic adjustments in response to changes in body weight. Skeletal muscle is a likely source tissue for this type of plasticity as well as for the location of required sensors, as weight-bearing muscles receive mechanical feedback regarding body weight and consume ATP in order to generate forces sufficient to (at least) counteract gravity.

We know that skeletal muscle can respond to increased and decreased load by hypertrophy and atrophy, but the molecular and biochemical mechanisms that muscles use to sense and adjust to changes in body weight are poorly understood. We focus our work in this area on the regulation of expression of sarcomere genes encoding proteins that function at the interface between thin and thick filaments. Specifically, we work on mechanisms controlling expression of the troponin complex, and within that, of troponin T. These thin filament regulatory proteins play a large role in regulating muscle force output and energy consumption by controlling the calcium sensitivity of actomyosin cross-bridge activation. The troponin T gene is alternatively spliced and gives rise to several splice variants that differ in way they encode troponin T proteins.

We have made some progress examining mechanisms involved in body weight sensation in rodents (see here), fruit flies (see here) and are currently extending this project using cockroaches as the study system.

Metabolic disease in nature. We are conducting long-term studies on the ecophysiology of dragonfly flight performance. A significant amount of standing variation in male flight performance is apparent in several natural populations of dragonflies that surround the Penn State University main campus. Such variation may be somewhat surprising given that it is likely that high performing males should be selected for in the population. This is because females tend to mate with males that are capable of acquiring and successfully defending a territory, as well as successfully guarding a mated female from being grabbed by another male while she is laying eggs. The presence of this variation indicates that male flight performance may not be set for any particular individual and that gene-by-environment interactions may affect male flight physiology in important ways.

We have discovered that one environmental factor is parasitic infection. Dragonflies are commonly infected with gregarine (Protozoa: Apicomplexa) parasites which infect most invertebrate groups, but are especially common in arthropods and annelids. Dragonflies are likely infected by drinking water and eating prey that may containing infectious spores that produce sporozoites which attach to the intestinal epithelium.

Infected dragonflies typically show no obvious external symptoms but perform poorly in territorial contests in the field and therefore have low mating success. Since these traits are mainly determined by flight performance, we previously examined how gregarine infection affects aspects of flight muscle physiology and metabolism in these dragonflies. We showed that gregarine infection impairs flight muscle energetics and causes a loss of endocrine control of carbohydrate metabolism and significant lipid accumulation (see here). Together these features comprise a set of symptoms associated with what in vertebrates is known as the metabolic syndrome but had not previously been described in other animal taxa.

We also showed that muscle contractile phenotypes associated with parasitic infection in dragonflies are highly similar to those of obese mammals (see here), and are currently using other insect systems to explore the generality of our findings in dragonflies.