Building Cetacean Locomotor Muscles throughout Ontogeny to Support High-Performance Swimming into Adulthood

Abstract

Synopsis The demands on the locomotor muscles at birth are different for cetaceans than terrestrial mammals. Cetacean muscles do not need to support postural costs as the neonate transitions from the womb because water’s buoyant force supports body weight. Rather, neonatal cetacean muscles must sustain locomotion under hypoxic conditions as the neonate accompanies its mother swimming underwater. Despite disparate demands at birth, cetaceans like terrestrial mammals require postnatal development to attain mature musculature. Neonatal cetaceans have a low proportion of muscle mass, and their locomotor muscles have lower mitochondrial density, myoglobin content (Mb), and buffering capacity than those found in the adult locomotor muscle. For example, the locomotor muscle of the neonatal bottlenose dolphin has only 10 and 65% of the Mb and buffering capacity, respectively, found in the adult locomotor muscle. The maturation period required to achieve mature Mb and buffering capacity in the locomotor muscle varies across cetacean species from 0.75 to 4 and 1.17 to 3.4 years, respectively. The truncated nursing interval of harbor porpoises and sub-ice travel of beluga whales may be drivers for faster muscle maturation in these species. Despite these postnatal changes in the locomotor muscle, ontogenetic changes in locomotor muscle fiber type seem to be rare in cetaceans. Regardless, the underdeveloped aerobic and anaerobic capacities of the locomotor muscle of immature dolphins result in diminished thrusting capability and swim performance. Size-specific stroke amplitudes (23–26% of body length) of 0–3-month-old dolphins are significantly smaller than those of >10-month-olds (29–30% of body length), and 0–1-month-olds only achieve 37 and 52% of the mean and maximum swim speed of adults, respectively. Until swim performance improves with muscle maturation, young cetaceans are precluded from achieving their pod’s swim speeds, which could have demographic consequences when fleeing anthropogenic disturbances.

Comparative analysis of the myoglobin gene in whales and humans reveals evolutionary changes in regulatory elements and expression levels

“…We propose that the low transcription level is the result of multiple evolved regulatory differences between the human and minke genes. Low transcription levels may be acceptable because of the evolution of increased stability of the myoglobin protein [24,[62][63][64][65]106], allowing steady accumulation of the protein consistent with observations in vivo [12,60]. These findings also imply that the induction of transcription by physiological influences such as exercise [32,103] and diet [107] may be important in the ontogeny of the high muscle myoglobin protein levels seen in cetaceans.…”

“…In contrast to a transcriptional explanation for the high MB levels in Cetacea, recent studies of MB protein structure and evolution support the idea that the high levels may be due simply to the steady accumulation of a very stable protein. Observations show that neonates have low MB levels compared to adults, and the level of MB increases steadily during the early life of the animal [ 12 , 60 , 61 ]. Several evolutionary adaptations of the MB protein work together to increase MB stability [ 62 , 63 ] and solubility during synthesis and as mature folded myoglobin, despite the “macromolecular crowding” and acidic pH of the muscle cell cytoplasm [ 24 , 64 , 65 ].…”