Scaling of left ventricle cardiomyocyte ultrastructure across development in the kangaroo Macropus fuliginosus

Abstract

The heart and left ventricle of the marsupial western grey kangaroo Macropus fuliginosus exhibit biphasic allometric growth, whereby a negative shift in the trajectory of cardiac growth occurs at pouch exit. In this study, we used transmission electron microscopy to examine the scaling of left ventricle cardiomyocyte ultrastructure across development in the western grey kangaroo over a 190-fold body mass range (0.355−67.5 kg). The volume-density (%) of myofibrils, mitochondria, sarcoplasmic reticuli and T-tubules increase significantly during in-pouch growth, such that the absolute volume (ml) of these organelles scales with body mass (M b ; kg) with steep hyperallometry: , respectively. The steep hyperallometry of organelle volumes and volume-densities across in-pouch growth is consistent with the improved contractile performance of isolated cardiac muscle during fetal development in placental mammals, and is probably critical in augmenting cardiac output to levels necessary for endothermy and independent locomotion in the young kangaroo as it prepares for pouch exit. The shallow hypoallometry of organelle volumes during post-pouch growth suggests a decrease in relative cardiac requirements as body mass increases in free-roaming kangaroos, which is possibly because the energy required for hopping is independent of speed, and the capacity for energy storage during hopping could increase as the kangaroo grows.

Scaling of the ankle extensor muscle‐tendon units and the biomechanical implications for bipedal hopping locomotion in the post‐pouch kangarooMacropus fuliginosus

“…Smaller western grey kangaroos also have hearts that are relatively larger for their body mass than do larger kangaroos (Snelling et al. ,b). Relatively larger hearts (for aerobic capacity) and relatively greater ankle torques (for acceleration and hopping speed) of smaller kangaroos may reflect their greater predation risk (Dawson, ).…”

Novel large-particle FACS purification of adult ventricular myocytes reveals accumulation of myosin and actin disproportionate to cell size and proteome in normal post-weaning development

“…Protein content per-MC and MC median volumes were scaled to animal growth using the regression line between log-log covariates with the equation y = bx α for ontogenic allometry 15 where y is the trait being scaled, x is the growth determinant, and b (intercept) & α (slope) are constants. The animal age is replaced as the growth determinant by body mass and time is cancelled out in the derivative 14,19,20 . Cell growth and protein accumulation are the traits of interest.…”

Development of endothermy and concomitant increases in cardiac and skeletal muscle mitochondrial respiration in the precocial Pekin duck (Anas platyrhynchos domestica)

“…Snelling et al (2015b) found that heart mass of grey kangaroo joeys grows hyperallometrically while the joeys are in the pouch, as they approach attaining endothermy and leaving the pouch. Associated changes at the cellular level in the heart also occur within the joey, with increases in mitochondria volume and muscle contractile machinery associated with leaving the pouch and obtaining endothermy (Snelling et al, 2015a). Through day 42 post-hatching in the chicken, ventricle size increases through both hyperplasia and hypertrophy after hatching (Li et al, 1997).…”