Evolution of a high-performance and functionally robust musculoskeletal system in salamanders.

The evolution of ballistic tongue projection in plethodontid salamanders-a high-performance and thermally robust musculoskeletal system-is ideal for examining how the components required for extreme performance in animal movement are assembled in evolution. Our comparative data on whole-organism performance measured across a range of temperatures and the musculoskeletal morphology of the tongue apparatus were examined in a phylogenetic framework and combined with data on muscle contractile physiology and neural control. Our analysis reveals that relatively minor evolutionary changes in morphology and neural control have transformed a muscle-powered system with modest performance and high thermal sensitivity into a spring-powered system with extreme performance and functional robustness in the face of evolutionarily conserved muscle contractile physiology.

Convergently evolved muscle architecture enables high-performance ballistic movement in salamanders.

Elastically powered ballistic movements, such as tongue projection, are common in nature, likely due to benefits such as increased acceleration and distance of movement, and decreased thermal sensitivity imparted by elastic mechanisms. Within Plethodontidae, both muscle-powered and elastically powered ballistic tongue projection occur. Thus, we examine how elastically powered ballistic tongue projection morphology has evolved from muscle powered projection at the level of the projector muscles (m.

Movements of vastly different performance have similar underlying muscle physiology.

Many animals use elastic recoil mechanisms to power extreme movements, achieving levels of performance that would not be possible using muscle power alone. Contractile performance of vertebrate muscle depends strongly on temperature, but the release of energy from elastic structures is far less thermally dependent, thus elastic recoil confers thermal robustness to whole-animal performance. Here we explore the role that muscle contractile properties play in the differences in performance and thermal robustness between elastic and non-elastic systems by examining muscle from two species of plethodontid salamanders that use elastically powered tongue projection to capture prey and one that uses non-elastic tongue projection.

Thermal sensitivity of motor control of muscle-powered versus elastically powered tongue projection in salamanders.

Elastic-recoil mechanisms can improve organismal performance and circumvent the thermal limitations of muscle contraction, yet they require the appropriate motor control to operate. We compare muscle activity during tongue projection in salamanders with elastically powered, ballistic projection with activity of those with muscle-powered, non-ballistic projection across a range of temperatures to understand how motor control is integrated with elastically powered movements, and how this integration contributes to reduced thermal sensitivity. Species with ballistic tongue projection activated and deactivated their projector muscles significantly earlier than non-ballistic species, in a pattern consistent with a mechanism in which the muscle strains elastic tissue that subsequently recoils to power projection.

Extreme Performance and Functional Robustness of Movement are Linked to Muscle Architecture: Comparing Elastic and Nonelastic Feeding Movements in Salamanders.

Muscle-powered movements are limited by the contractile properties of muscles and are sensitive to temperature changes. Elastic-recoil mechanisms can both increase performance and mitigate the effects of temperature on performance. Here, we compare feeding movements in two species of plethodontid salamanders, Bolitoglossa franklini and Desmognathus quadramaculatus, across a range of body temperatures (5-25°C) to better understand the mechanism of elastically powered, thermally robust movements.

Adaptive evolution in locomotor performance: How selective pressures and functional relationships produce diversity.

Despite the complexity of nature, most comparative studies of phenotypic evolution consider selective pressures in isolation. When competing pressures operate on the same system, it is commonly expected that trade-offs will occur that will limit the evolution of phenotypic diversity, however, it is possible that interactions among selective pressures may promote diversity instead. We explored the evolution of locomotor performance in lizards in relation to possible selective pressures using the Ornstein-Uhlenbeck process.

Dynamics and thermal sensitivity of ballistic and non-ballistic feeding in salamanders.

Low temperature reduces the performance of muscle-powered movements, but in movements powered by elastic recoil mechanisms, this effect can be mitigated and performance can be increased. To better understand the morphological basis of high performance and thermal robustness of elastically powered movements, we compared feeding dynamics at a range of temperatures (5-25°C) in two species of terrestrial plethodontid salamanders, Plethodon metcalfi and Ensatina eschscholtzii, which differ in tongue muscle architecture and the mechanism of tongue projection. We found that Ensatina is capable of ballistic projection with a mean muscle mass-specific power of 2100 W kg(-1), revealing an elastic mechanism.

Running for your life or running for your dinner: what drives fiber-type evolution in lizard locomotor muscles?

Despite its role in whole-animal performance, the adaptation of muscle physiology related to terrestrial locomotion remains underexplored. We tested evolutionary models based on predator escape and foraging strategies of lizards to assess whether fiber-type composition of a leg muscle is adaptive for behavior. The best-fitting model for fast-twitch fiber-type evolution was one based on predator-escape strategy, while the foraging-mode model fared poorly (Akaike Information Criterion with small sample size correction; DeltaAICc=29.

Are powerful females powerful enough? Acceleration in gravid green iguanas (Iguana iguana).

One demand placed exclusively on the musculoskeletal system of females is maintaining locomotor performance with an increasing load over the reproductive cycle. Here, we examine whether gravid (i.e.

Adjusting muscle function to demand: joint work during acceleration in wild turkeys.

We measured the net work performed at hind limb joints in running turkeys to determine the source of mechanical power for acceleration. We tested the hypothesis that net mechanical work per step increases in proportion to acceleration at all four major hind limb joints (hip, knee, ankle and tarsometatarsal-phalangeal joint). This hypothesis was based on the idea that all hind limb muscles should contribute mechanical work to maximize performance during accelerations, and a previous study that indicated the mechanical power output of the entire turkey hind limb musculature was remarkably high.

Mechanical power output during running accelerations in wild turkeys.

We tested the hypothesis that the hindlimb muscles of wild turkeys (Meleagris gallopavo) can produce maximal power during running accelerations. The mechanical power developed during single running steps was calculated from force-plate and high-speed video measurements as turkeys accelerated over a trackway. Steady-speed running steps and accelerations were compared to determine how turkeys alter their running mechanics from a low-power to a high-power gait.