In all vertebrates, the vertebral column is derived entirely from paraxial mesoderm (Christ et al., 2000). Segmentation of the paraxial mesoderm leads to somitic formation and establishes an anterior–posterior polarity within the somites and their derivatives. The somitic mesoderm differentiates into a dorsal and ventral domain (dermomyotome and sclerotome, respectively) with undifferentiated somitocoele mesenchyme occupying the center of the somite (Fig. 4A). The dermomyotome (skeletal muscle, dermis, scapulae) migrates to the dorsolateral margin as the sclerotome differentiates into four distinct regions forming the dorsal, central, ventral, and lateral sclerotome (Fig. 4B,C). The dorsal sclerotome gives rise to the spinous process and the dorsal portion of the neural arch, while the pedicle and lamina of the neural arch and the proximal ribs are formed from central sclerotome with some contribution from somitocoele mesechyme. The ventral sclerotome gives rise to the vertebral body, whereas the distal ribs derive from the lateral sclerotome (Fig. 4D,E) (Huang et al., 1994; Christ et al., 2000; Stockdale et al., 2000; Mittapalli et al., 2005; for review see Christ and Scaal, 2008).
Figure 4. The following series depicts the development of the four sclerotomal subdomains and their derivatives. (A) Somite differentiation into dermomyotome and sclerotome, which surrounds the somitocoele mesenchyme. (B) Sclerotome differentiates into four subdomains: dorsal, ventral, central, and lateral. (C) Scleretome migrates around the notochord and neural tube. (D) Vertebral derivatives of each sclerotomal subdomain. (E) Fully developed caudal vertebra with two mesenchyme derivatives, intervertebral joints (IJ), and intervertebral disc (ID).
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The somites undergo a further division called resegmentation, a process by which anteroposterior polarized somites divide into a cranial and caudal-half somite (Fig. 5A,B). The caudal-half somite then fuses with the following cranial-half somite to form a resegmented somite from which the metameric vertebrae and ribs arise (Fig. 5C) (Bagnall et al., 1988). It is during resegmentation that the somitocoele mesenchyme migrates to the caudal-half somite. The mesenchyme itself is segregated into dorsal and ventral compartments; these compartmentalized cells give rise to the intervertebral joints and intervertebral discs (Huang et al., 1994; Mittapalli et al., 2005; Christ and Scaal, 2008). This general model of vertebral development is dominantly derived from studies using the quail-chick chimeric system, although recent research has demonstrated similar results in an amphibian model (Piekarski and Olsson, 2013). The similarities seen in the amphibian and quail-chick chimeric system provide an extant phylogenetic bracket appropriate for the study of dinosaurian vertebral development (sensu Witmer, 1995).
Figure 5. Resegmentation of the sclerotome provides a half-somite posterior shift for axial musculature to overlap preceding vertebra. (A) Discrete somites derive from paraxial mesoderm. (B) Sclerotome segregates into a cranial- and caudal-half somite. (C) Caudal-half somite fuses with proceeding cranial-half somite. Note: Somitocoele mesenchyme expressed on anterior surface of caudal-half somite contributes to intervertebral disc. (D) Sclerotomal derivatives shown as fully formed normal and block vertebrae.
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Fusion of caudal vertebrae due to trauma or disease is not uncommon in sauropod dinosaurs. Rothschild and Berman (1991) reported osseous overgrowths spanning vertebral bodies in two of four specimens of Apatosaurus and three of six Diplodocus specimens studied with appropriate mid-anterior portions of the tail preserved. Diffuse idiopathic skeletal hyperostosis (DISH) has been suggested as the likely cause of these pathologies (Rothschild, 1987; Rothschild and Berman, 1991). The ligamentous, tendonous, or capsular ossification in specimens exhibiting DISH often display a “pasted-on” or “dripped candle-wax” appearance (Rothschild et al., 1994). Although WDC LA-188 does fall within the range of pathologically affected mid-anterior caudal vertebrae commonly observed in diplodocoid sauropods, its expressed morphology is not consistent with DISH. Specifically, there are no indications of ligamentous or tendonous fusions, no outgrowths that typify the physical manifestation of this disease, and no vacuity formerly occupied by the intervertebral disc (e.g., Rothschild and Berman, 1991).
Birkemeier and Swor (2007) suggested spondyloarthropathy (infectious arthritis) as a potential cause for the malformation seen in WDC LA-188. Spondyloarthropathy in vertebrae can lead to erosion or fusion of the zygapophyseal joints and vertebral body; zygapophyseal erosion has been reported in four consecutive caudal vertebrae of Camarasaurus (Rothschild et al., 2002). However, an aberrant vertebral body and reduced neural spines and lack of a space for an intervertebral disc (e.g., complete fusion) are not consistent with spondyloarthropathy (Rothschild et al., 1994).
It is suggested that a developmental error, rather than trauma or disease, led to the unique morphology exhibited by WDC LA-188, a morphology that resembles previously reported incidences of congenital block vertebrae (Kaplan et al., 2005; Rothschild and Tanke, 2005). Failures of segmentation in the spinal column lead to defects such as hemivertebae, scoliosis, wedge vertebrae, and block vertebrae (Kaplan et al., 2005; Witzmann, 2007; Witzmann et al., 2008). Block vertebrae involve the entire vertebra and there is no growth plate or somitocoele mesenchyme to form the intervertebral disc or intervertebral joints (Huang et al., 1994; Mittapalli, et al., 2005; Christ and Scaal, 2008). The lack of a discrete separation, both internally and externally, between the anterior and posterior halves of the vertebral body suggests an absence of an intervertebral disc. This is consistent with the hypothesis that WDC LA-188 is a congenital block vertebra (Fig. 5D) and not the result of spondyloarthropathy or DISH.
Externally, it is possible to distinguish between the anterior and posterior halves of WDC LA-188 by the weakly developed vertical ridge externally. Internally, there is an evident increase in density in the anterior half, in part due to differential permineralization; this disparity is thought to highlight differences in internal morphology rather than a strict result of taphonomic circumstance (Fig. 3). Furthermore, there is a thin (1–2 cm) vertical zone of markedly increased density along the anterior and posterior margins of the specimen, as well as medially along the same plane as the weakly developed ridge seen externally (Fig. 3C). The location and density contrast are consisted with known regions of cortical bone development indicating that WDC LA-188 is composed of two vertebral bodies.
Although it is difficult to diagnose the exact nature of this malformation, it is suggested that the most likely cause is the loss of the somitocoele mesenchyme during somitogenesis. A failure of the mesenchyme to migrate or proliferate in the caudal-half somite during resegmentation (sensu Bagnall et al., 1988) would result in the absence of intervertebral joints and an intervertebral disc (Huang et al., 1994; Mittapalli et al., 2005). The differences in density between the anterior and posterior halves of WDC LA-188 could also be explained by the lack of somitocoele mesenchyme. In addition to contributing to the proximal portion of dorsal ribs, intervertebral joints, and intervertebral discs, somitocoele mesenchyme is also know to have angiogenic potency (Huang et al., 1994). Loss of mesenchyme would have affected vascularization of the posterior vertebra, which might account for the differential permineralization of pore spaces seen in CT images.
What differentiates WDC LA-188 from other reported block vertebrae is the expected length for two fused vertebrae from this anatomical position. The morphology is consistent with a diplodocoid caudal and its association with the skeletal remains of an isolated Apatosaurus is compelling. However, if this vertebra does belong to the excavated Apatosaurus skeleton, the fused vertebral bodies are shorter than expected for two “normal” vertebrae. Although the shortened vertebrae may be the result of a misdiagnosed taxonomic assignment, it is suggested the shortening is a result of aberrant vertebral development due to the lack of a growth plate in addition to the absence of an intervertebral disc.
In conclusion, the developmental abnormality expressed in WDC LA-188 is consistent with a somitic resegmentation error. This error occurred during early embryonic development and led to the formation of a block vertebra. The absence of somitocoele mesenchyme would have inhibited the formation of intervertebral joints, including the intervertebral disc leading to the fusion of two vertebral elements. It is suggested that the loss of the growth plate at this margin prevented the anterior and posterior vertebral bodies that comprise the block vertebra to reach the lengths typical for its hypothesized anatomical position. WDC LA-188 displays morphological features that are strongly associated with failures of segmentation and represents the first congenital malformation observed in a sauropod dinosaur.