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.

Figure 1

Hypothesized evolutionary transformations of the morphology and function of the axial system in craniates. Data were compiled from various sources (see text) and mapped onto a simplified phylogenetic hypothesis based on [71]. Character states plesiomorphic for craniates are indicated by arrows. -- Axial skeleton (rectangles): Notochordates (i.e., Cephalochordata + Craniata) ancestrally possess a notochord, eponymous for the group. In early vertebrates, cranio-caudally uniform vertebral elements evolved (VE). In gnathostomes, the axial skeleton is regionalized. A trunk (= dorsal, D) and tail region (caudal, CD) are distinguished in gnathostome fishes, while a cervical (C), truncal, sacral (S), and caudal region are present in early tetrapods. In mammals, the truncal region is further subdivided into a thoracic (T) and a lumbar (L) region. -- Axial musculature (circles): Gross anatomy and fiber orientation: Transformations in the arrangement of the perivertebral musculature are illustrated by schematic cross-sections showing the gross-anatomical changes (left) and cartoons of a few body segments in lateral perspective illustrating the changes in muscle and/or fiber arrangement (right). Dorsal and ventral parts of the myomeres are innervated by separate rami of the ventral root in agnathan fishes (light and dark brown). In each segment, muscle fibers span longitudinally between adjacent myosepta. In gnathostomes, the dorsal and ventral myomere parts are morphologically separated by the horizontal septum (pink) resulting in epaxial (ep) and hypaxial (hy) muscles. Likely associated with the evolutionarily new requirements to stabilize the body against long-axis torsion, deeper muscle fibers are obliquely oriented. In non-amniote tetrapods, the epaxial musculature retained its segmental organization in contrast to the hypaxial musculature, which comprises the polysegmental subvertebral (sv) and the abdominal wall muscles (the latter are not shown here). The majority of the epaxial fibers connects adjacent myosepta longitudinally, while deeper fibers run at different angles. In amniotes, the epaxial musculature is reorganized into three longitudinal and polysegmental muscle tracts (tr: transversospinal, lo: longissimus, ilc: iliocostalis). In mammals, the transversospinal muscle is subdivided into several entities forming the transversospinal system (trs). The mammalian ventrovertebral musculature is strengthened by the psoas major (ps). -- Axial muscle function (diamonds): The plesiomorphic function of the axial musculature is to mobilize the body in the horizontal plane. The horizontal and torsional moments that result from the evolution of fins and a heterocercal tail, which tend to laterally bend the trunk and cause long-axis torsion, respectively, have to be counteracted by the axial muscles in gnathostome fishes. In tetrapods, as a consequence of the evolution of supporting limbs and transition to land, the axial muscles additionally function to globally stabilize the trunk against inertial and extrinsic limb muscle forces as well as against gravitational forces. Note that the evolution of limbs preceded the transition to land. In tetrapods with a sprawled limb posture, extrinsic limb muscle forces in the horizontal plane are relatively large. The greater agility and maneuverability as well as an increased importance of limb action for body propulsion, likely requires the axial muscles to dynamically stabilize the trunk to a greater extent in amniotes than in non-amniote tetrapods. Associated with the evolution of sagittal mobility and a parasagittal limb posture in mammals, the axial muscles additionally function to globally stabilize the trunk against sagittal components of extrinsic limb muscle action as well as against inertia. Furthermore, the axial musculature mobilizes the trunk in the sagittal plane during asymmetrical gaits.

Figure 2

Histological cross-sections of the perivertebral musculature showing the distribution of the muscle fiber types (left) and schematic illustration of the segregations of fatigue-resistant fibers (right). Data were assembled from: hagfish, Myxine glutinosa: Sudan black B staining [from [30], reproduced with permission of author and Springer Verlag]; velvet belly lantern shark, Etmopterus spinax: cross-section from behind the anus, Sudan black B staining (Photos by P.R. Flood, Copyright by Bathybiologica AS); tiger salamander, Ambystoma tigrinum, 4th external trunk segment, enzyme-histochemical reaction for mATPase (acid preincubation) [7]; desert iguana, Dipsosaurus dorsalis, 14th trunk vertebra, combined enzyme-histochemical reaction for mATPase (alkaline preincubation) and NADH-TR (S. Moritz, unpubl. data); common vole, Microtus arvalis, intervertebral level between 6th and 7th lumbar vertebrae, enzyme-histochemical reaction for mATPase (alkaline preincubation) and NADH-TR [8]. Cross-sections were selected to illustrate of the muscular characters discussed in the text. Note that cranio-caudal changes in the proportion of the respective fiber types may occur (see text for details).

Figure 3

Activity patterns and hypothesized functions of the epaxial muscles in tetrapods during locomotion [modified from [118]]. Data for the epaxial muscle activity were assembled from: spotted salamander, Ambystoma maculatum, m. dorsalis trunci, 8th external trunk segment, mean and standard error [90]; desert iguana, Dipsosaurus dorsalis, m. longissimus dorsi, 14th trunk vertebra, mean and standard deviation (S. Moritz, unpubl. data); dog, Canis familiaris, m. longissimus thoracis et lumborum, 6th lumbar vertebra, median and upper and lower quartiles [118]. The x-axis represents the stride cycle beginning with the touch down of the ipsilateral hindlimb. The footfall patterns of the both hindlimbs are illustrated on the bottom of each graph (walk, trot: black: ipsilateral limb (iHL), gray: contralateral limb (cHL); gallop: black: trailing limb (tHL), gray: leading limb (lHL). Note that for the galloping dog, the EMG trace associated with the trailing hindlimb is black, the one associated with the leading hindlimb is gray. Bending traces above the electromyograms indicate the unimodal lateral flexion and extension on the body side ipsilateral to the recorded muscle activity (salamander, lizard) and the bimodal flexion and extension in the sagittal plane (mammal). Body planes in which moments and/or movements are suggested to occur are illustrated in the right top corner of each graph (for details see Figure 1). Note that the unilateral and monophasic epaxial activity in the walking salamander and lizard associated with the ipsilateral stance phase corresponds to the main activity observed in mammals. In mammals, the increased need for sagittal stability is met by bilateral activity resulting from a second burst during ipsilateral swing phase.