Evolution of the axial system in craniates: morphology and function of the perivertebral musculature

Abstract

The axial musculoskeletal system represents the plesiomorphic locomotor engine of the vertebrate body, playing a central role in locomotion. In craniates, the evolution of the postcranial skeleton is characterized by two major transformations. First, the axial skeleton became increasingly functionally and morphologically regionalized. Second, the axial-based locomotion plesiomorphic for craniates became progressively appendage-based with the evolution of extremities in tetrapods. These changes, together with the transition to land, caused increased complexity in the planes in which axial movements occur and moments act on the body and were accompanied by profound changes in axial muscle function. To increase our understanding of the evolutionary transformations of the structure and function of the perivertebral musculature, this review integrates recent anatomical and physiological data (e.g., muscle fiber types, activation patterns) with gross-anatomical and kinematic findings for pivotal craniate taxa. This information is mapped onto a phylogenetic hypothesis to infer the putative character set of the last common ancestor of the respective taxa and to conjecture patterns of locomotor and muscular evolution. The increasing anatomical and functional complexity in the muscular arrangement during craniate evolution is associated with changes in fiber angulation and fiber-type distribution, i.e., increasing obliqueness in fiber orientation and segregation of fatigue-resistant fibers in deeper muscle regions. The loss of superficial fatigue-resistant fibers may be related to the profound gross anatomical reorganization of the axial musculature during the tetrapod evolution. The plesiomorphic function of the axial musculature -mobilization- is retained in all craniates. Along with the evolution of limbs and the subsequent transition to land, axial muscles additionally function to globally stabilize the trunk against inertial and extrinsic limb muscle forces as well as gravitational forces. Associated with the evolution of sagittal mobility and a parasagittal limb posture, axial muscles in mammals also stabilize the trunk against sagittal components of extrinsic limb muscle action as well as the inertia of the body's center of mass. Thus, the axial system is central to the static and dynamic control of the body posture in all craniates and, in gnathostomes, additionally provides the foundation for the mechanical work of the appendicular system.

New insights on equid locomotor evolution from the lumbar region of fossil horses

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“…In particular, bending of the lumbar region is involved in the fastest mammalian gaits (asymmetric gaits, e.g. gallop or bound) [3,4]. While lumbar flexion and extension in the sagittal plane is characteristic of mammals, increasing both stride length and acceleration, several groups of large-bodied mammals have secondarily lost this feature, instead stabilizing the lumbar region [5,6].…”

Muscular anatomy of the tail of the western grey kangaroo, Macropus fuliginosus

“…The connection forms a functional chain of muscles from the presacral spine to the tail, and may act to maintain posture and stability of the body-axis during the floating phase of hopping. This function is analogous to that seen in quadrupedal mammals during running (Schilling 2011). The extensive thoracolumbar fasciae of the lumbar and caudal regions are also likely to contribute to support the body-axis during the hopping cycle.…”

Empirical validation of a spined sagittal-plane quadrupedal model

“…The belt drive is actuated through a sprocket by two parallel TMotor U8-16 brushless motors 5 housed in the rear body segment. These motors pull on the belt against a fixed sprocket in the front of the robot, allowing the motors to pitch the spine upwards or downwards.…”

“…The biological literature on core actuation offers several careful studies regarding its low-level mechanics [3], [4], [5] and its proposed role as a mechanical energy storage in gaits [6]. To the best of the authors' knowledge, however, there is a lack of work concerning biological templates [7] of core actuation.…”