Gastrocnemius Muscle Structural and Functional Changes Associated with Domestication in the Turkey.

Selection for increased muscle mass in domestic turkeys has resulted in muscles twice the size of those found in wild turkeys. This study characterizes muscle structural changes as well as functional differences in muscle performance associated with selection for increased muscle mass. We compared peak isometric force production, whole muscle and individual fiber cross-sectional area (CSA), connective tissue collagen concentration and structure of the lateral gastrocnemius (LG) muscle in wild and adult domestic turkeys. We also explored changes with age between juvenile and adult domestic turkeys. We found that the domestic turkey's LG muscle can produce the same force per cross-sectional area as a wild turkey; however, due to scaling, domestic adults produce less force per unit body mass. Domestic turkey muscle fibers were slightly smaller in CSA (3802 ± 2223 µm2) than those of the wild turkey (4014 ± 1831 µm2, p = 0.013), indicating that the absolutely larger domestic turkey muscles are a result of an increased number of smaller fibers. Collagen concentration in domestic turkey muscle (4.19 ± 1.58 µg hydroxyproline/mg muscle) was significantly lower than in the wild turkeys (6.23 ± 0.63 µg/mg, p = 0.0275), with visible differences in endomysium texture, observed via scanning electron microscopy. Selection for increased muscle mass has altered the structure of the LG muscle; however, scaling likely contributes more to hind limb functional differences observed in the domestic turkey.

Diversity of extracellular matrix morphology in vertebrate skeletal muscle.

Existing data suggest the extracellular matrix (ECM) of vertebrate skeletal muscle consists of several morphologically distinct layers: an endomysium, perimysium, and epimysium surrounding muscle fibers, fascicles, and whole muscles, respectively. These ECM layers are hypothesized to serve important functional roles within muscle, influencing passive mechanics, providing avenues for force transmission, and influencing dynamic shape changes during contraction. The morphology of the skeletal muscle ECM is well described in mammals and birds; however, ECM morphology in other vertebrate groups including amphibians, fish, and reptiles remains largely unexamined. It remains unclear whether a multilayered ECM is a common feature of vertebrate skeletal muscle, and whether functional roles attributed to the ECM should be considered in mechanical analyses of non-mammalian and non-avian muscle. To explore the prevalence of a multilayered ECM, we used a cell maceration and scanning electron microscopy technique to visualize the organization of ECM collagen in muscle from six vertebrates: bullfrogs (Lithobates catesbeianus), turkeys (Meleagris gallopavo), alligators (Alligator mississippiensis), cane toads (Rhinella marina), laboratory mice (Mus musculus), and carp (Cyprinus carpio). All muscles studied contained a collagen-reinforced ECM with multiple morphologically distinct layers. An endomysium surrounding muscle fibers was apparent in all samples. A perimysium surrounding groups of muscle fibers was apparent in all but carp epaxial muscle; a muscle anatomically, functionally, and phylogenetically distinct from the others studied. An epimysium was apparent in all samples taken at the muscle periphery. These findings show that a multilayered ECM is a common feature of vertebrate muscle and suggest that a functionally relevant ECM should be considered in mechanical models of vertebrate muscle generally. It remains unclear whether cross-species variations in ECM architecture are the result of phylogenetic, anatomical, or functional differences, but understanding the influence of such variation on muscle mechanics may prove a fruitful area for future research.

The Multi-Scale, Three-Dimensional Nature of Skeletal Muscle Contraction.

Muscle contraction is a three-dimensional process, as anyone who has observed a bulging muscle knows. Recent studies suggest that the three-dimensional nature of muscle contraction influences its mechanical output. Shape changes and radial forces appear to be important across scales of organization. Muscle architectural gearing is an emerging example of this process.

Waddle and shuffle: gait alterations associated with domestication in turkeys.

Domestication has altered turkey morphology by artificially selecting for increased muscle mass and breast meat. Artificial selection has resulted in birds that weigh up to 3 times more than their wild counterparts, with relatively little change in the length of their bones and limbs. Considering these structural changes, it seems probable that domestic turkey locomotor kinematics and kinetics would also be altered. To examine the locomotor dynamics of wild and domestic turkeys, we had both strains walk down a runway with a force plate at the center to measure their ground reaction forces and gait parameters. The location of their center of mass was also quantified using a force plate and bi-planar x-ray and found to be further anterior in the domestic strain. The domestic turkeys locomoted across a lower range of speeds (0.25-1.64 ms-1) than the wild turkeys (0.26-3.26 ms-1) and increased their stride frequency at a higher rate. They also displayed large lateral oscillations, i.e. waddling, during walking that translated into relatively high medio-lateral ground reaction forces and lateral kinetic energy (3.5 times higher than that of wild turkeys). The results indicate that domestic turkey locomotion is not simply a slowed down version of wild turkey locomotion. The changes in gait observed are similar to the shuffling gait present in some human populations, such as Parkinson's patients, which serves to increase stability. The domestic turkey's increased body mass and more anterior center of mass position may require these kinematic and kinetic gait differences.

Patterns of musculoskeletal growth and dimensional changes associated with selection and developmental plasticity in domestic and wild strain turkeys.

Domestication is a type of experimental evolution in which humans have artificially selected for specific desired traits. Selected strain animals can be utilized to identify correlated responses by comparing them to the wild strain. In particular, domestic turkeys have been selected for increased body mass and high-growth rate, most significantly over the past 60 years. Yet it remains unclear how artificial selection has affected the morphology and evolution of the musculoskeletal system as a whole. Here, we compare growth rate over 21 weeks, hind limb bone scaling across ontogeny via in vivo CT scanning, and muscle proportions in wild and domestic turkeys to identify differences in structural scaling and the potential contributions of selection and developmental plasticity to whole-organism morphology. The domestic turkeys grew at a higher rate (0.14 kg/day vs. 0.05 kg/day) and reached over 3 times the body mass of wild birds. Comparing the proportional muscle masses in adult turkeys, only the trunk had a greater mass ratio in the domestic turkey, driven solely by M. pectoralis (2.8 times larger). The proportional increase in only breast meat and no other muscles highlights the surgical precision attainable with artificial selection. The domestic turkey femur and tibiotarsus displayed increases in polar moment of area, apparently maintaining torsional strength as body mass increased. The lack of dimensional change in the more vertically held tarsometatarsus is consistent with the pattern expected due to developmental plasticity. These results from the domestic turkey emphasize that there are morphological limits to preserving the balance between growth and function, and varying rates of trait evolution can further complicate this equilibrium.

An ontogenetic perspective on symphyseal fusion, occlusion and mandibular loading in alpacas (Vicugna pacos).

A primary hypothesis for the evolution of mandibular symphyseal fusion in some mammals is that it functions to resist loads incurred during routine mastication. Anecdotal support for this hypothesis is based on the fact that when the symphysis fuses, it typically does so early during postnatal ontogeny prior to or around the time of weaning. However, little is known about the process of fusion, particularly relative to feeding behaviors and the dynamics of mastication, including occlusion and masticatory loading. In the present study, we investigate the timing and process of symphyseal fusion in alpacas (Vicugna pacos) in the context of maturation of the oral apparatus and oral behavior. We also report on in vivo strains from the symphysis and corpus in young alpacas prior to and following full fusion and M1 occlusion. Results show that fusion begins rostrally by 1 month and is complete by 6-7 months whereas all deciduous premolars and M1 come into occlusion by 6 months. Although symphyseal loading patterns are maintained throughout ontogeny, in young alpacas symphyseal strain magnitudes are low compared with adults but corpus strain magnitudes are comparable to those found in adults. Reduced symphyseal loading in young individuals is contrary to what might be predicted given that the symphysis is still fusing. When considered in light of the development of occlusion and rumination, strain magnitudes may be necessarily low and reflect an overall delay in the maturation of masticatory dynamics.

Locomotory fatigue during moderate and severe hypoxia and hypercapnia in the Atlantic blue crab, Callinectes sapidus.

The Atlantic blue crab, Callinectes sapidus (Rathbun), is a highly mobile crustacean that must locomote to find food, evade predators, find mates, and avoid adverse conditions such as hypoxia. In this study we tested the effects of two levels of hypoxia (10.4 kPa, 50% air saturation = moderate hypoxia; 4 kPa, 20% air saturation = severe hypoxia) and hypercapnic hypoxia (50% air saturation O(2) with Pco(2) = 2 kPa) on fatigue during sustained continuous exercise. Fatigue was induced by an exercise trial that entailed continuous sideways hexapedal walking on an underwater treadmill. Fatigue was quantified using two methods: (1) a pull force test that measures the holding strength of the legs, and (2) the number of fatigue-resisting behaviors (180° turns and stopping). Fatigue was defined as a pull force of 67% or less of the initial pre-exercise pull force and was reached after 6.12 h of walking for crabs in well-aerated normoxic seawater, 4 h in 50% air saturation, 2.07 h in 20% air saturation, and 4.58 h in 50% air saturation and hypercapnia. The number of fatigue-resisting behaviors increased with walking time in all treatments. Performance decreased in hypoxia, with fatigue being reached more quickly as the level of hypoxia intensified. Hypercapnia in moderate hypoxia did not have a deleterious influence on behavior and lengthened slightly the time it took crabs to fatigue. In addition, severe hypoxia exacerbated changes in gait kinematics as crabs became fatigued, by significantly increasing stride length and decreasing stride frequency.

Mandibular corpus bone strains during mastication in goats (Capra hircus): a comparison of ingestive and rumination chewing.

OBJECTIVE: To compare the mechanical loading environment of the jaw in goats during ingestive and rumination chewing. DESIGN: Rosette strain gauges were attached to the external surface of the mandibular corpus in five goats to record bone strains during the mastication of hay and rumination. RESULTS: Strain magnitudes and maximum physiological strain rates during the mastication of hay are significantly higher than during rumination chewing on the working and balancing sides. Principal strain ratios and orientations are similar between the two chewing behaviours. Loading and chewing cycle duration are all longer during rumination chewing, whereas chew duty factor and variances in load and chewing cycle durations are higher during ingestive chewing. For most of the variables, differences in strain magnitudes or durations are similar at all three gauge sites, suggesting that rumination and ingestive chewing do not differentially influence bone at the three gauge sites. CONCLUSIONS: Despite lower strain magnitudes, the repetitive nature of rumination chewing makes it an important component of the mechanical loading environment of the selenodont artiodactyl jaw. However, similarities in principal strain orientations and ratios indicate that rumination chewing need not be considered as a unique loading behaviour influencing the biomechanics of the selenodont artiodactyl jaw. Differences in loading and chewing cycle durations during rumination and ingestion demonstrate flexibility in adult chewing frequencies. Finally, although the low within-sequence variability in chewing cycle durations supports the hypothesis that mammalian mastication is energetically efficient, chewing during rumination may not be more efficient than during ingestion.

Intraspecific scaling of chewing cycle duration in three species of domestic ungulates.

In mammals, chewing cycle duration (CCD) increases with various measures of size, scaling with body mass(0.13-0.28) and jaw length(0.55). Proposed explanations for these scaling relationships include the allometry of body size, basal metabolic rate and tooth size, on the one hand, and pendular mechanics treating the jaw as a gravity-driven pendulum, on the other. Little is known, however, about the relationship between CCD and size within species. Recent research in dogs demonstrates altogether different scaling exponents and weaker correlations. This research suggests that breed-specific growth rates influence the maturation of the neural networks generating chewing rhythm, which may be altered because of changes in jaw mass during early postnatal growth. Here, we explored the intraspecific scaling of CCD within a sample of adult horses ranging from miniatures to draft breeds and an ontogenetic sample of goats and alpacas from infants to adults. In horses, CCD scales with body mass(0.19) and jaw length(0.57), although in neither case is the correlation significant. In the ontogenetic samples of goats and alpacas, CCD is significantly correlated with body mass, scaling as CCD∝body mass(0.37) in both species. In goats, but not alpacas, CCD is also significantly correlated with jaw length, scaling as jaw length(1.032). As in dogs, the scaling of CCD in horses may reflect the influence of selective breeding on growth trajectories of different breeds, resulting in reduced body and jaw size differences among infants, when CCD is established, compared with adults. However, the allometric scaling of tooth size in horses of different breeds may be a potential influence on the scaling of CCD. The scaling of CCD with body and jaw size in goats, and to a lesser extent in alpacas, also suggests that the development of peripheral masticatory structures such as the teeth and occlusal relations may play a role in changes in CCD during the earliest stages of postnatal ontogeny.

Occlusal development and masseter activity in Alpacas (Lama pacos).

Tooth eruption and the development of occlusion are significant ontogenetic changes in the masticatory apparatus of mammals. Here, we test the hypothesis that changes in masseter activity are correlated with increased occlusal contacts at major stages of dental development in the alpaca, Lama pacos. We compare electromyographic data from the superficial and deep masseter in infant and juvenile alpacas prior to and following m1 occlusion and from adults with full permanent dentitions. The pre-m1 and post-m1 occlusion groups exhibit similar masseter activity durations, chewing cycle durations, and with the exception of the balancing-side deep masseter, similar timing differences between the jaw muscles. On average, the balancing-side deep masseter fires significantly later in the post-m1 occlusion group. The m2-m3 group exhibits significantly longer chewing cycle length and an even later firing balancing-side deep masseter. Increased occlusion is also associated with an increase in the relative amount of working-side superficial and deep masseter muscle activity when compared with the balancing side muscles. Although the development of occlusal relations in infant and juvenile alpacas are associated with minor changes in masseter activation patterns, additional molar occlusal contacts increase chewing cycle duration resulting in concomitant changes in masseter recruitment patterns. Currently, we cannot rule out that musculoskeletal development influences masseter activity as demonstrated in other mammals. However, the data presented here indicate that alpacas have a relatively delayed onset of the adult motor pattern that may be correlated with changes in occlusal relations due to tooth eruption.