Evolution of the Mammalian Neck from Developmental,Morpho-Functional,and Paleontological Perspectives

The mammalian neck adopts a variety of postures during daily life and generates numerous head trajectories. Despite its functional diversity, the neck is constrained to seven cervical vertebrae in (almost) all mammals. Given this low number, an unexpectedly high degree of modularity of the mammalian neck has more recently been uncovered. This work aims to review neck modularity in mammals from a developmental, morpho-functional, and paleontological perspective and how high functional diversity evolved in the mammalian neck after the occurrence of meristic limitations. The fixed number of cervical vertebrae and the developmental modularity of the mammalian neck are closely linked to anterior Hox genes expression and strong developmental integration between the neck and other body regions. In addition, basic neck biomechanics promote morpho-functional modularity due to preferred motion axes in the cranio-cervical and cervico-thoracic junction. These developmental and biomechanical determinants result in the characteristic and highly conserved shape variation among the vertebrae that delimits morphological modules. The step-wise acquisition of these unique cervical traits can be traced in the fossil record. The increasing functional specialization of neck modules, however, did not evolve all at once but started much earlier in the upper than in the lower neck. Overall, the strongly conserved modularity in the mammalian neck represents an evolutionary trade-off between the meristic constraints and functional diversity. Although a morpho-functional partition of the neck is common among amniotes, the degree of modularity and the way neck disparity is realized is unique in mammals.

     

Analysis of variability in vertebral morphology and growth ring counts in two Carcharhinid sharks

Inter- and intra-regional variations in vertebrae morphology and growth increment counts (band counts) were analyzed for two carcharhinid shark species, Carcharhinus plumbeus (n = 10) and C. limbatus (n = 11). Five sequential vertebrae were removed from the cervical region, above the branchial chamber and posterior to the chondrocrainium, and thoracic region, below the first dorsal fin. Dorsal–ventral height, medial–lateral breadth, and caudal–cranial length were measured for each sampled vertebra. Results indicate no significant difference in vertebral morphology within a sampled region of the vertebral column. However, a significant difference in vertebral morphology was noted between regions for both shark species, with thoracic vertebrae consistently larger than cervical vertebrae. A sub-set of three vertebrae was taken from each sampled region of each shark for sectioning and counting of growth increments. Analyses of growth increment counts by two readers indicated no significant difference in band counts within and between sampled regions.     

Morphology and Function of the Vertebral Column in Remingtonocetus domandaensis (Mammalia, Cetacea) from the Middle Eocene Domanda Formation of Pakistan

The archaeocete family Remingtonocetidae is a group of early cetaceans known from the Eocene of India and Pakistan. Previous studies of remingtonocetids focused primarily on cranial anatomy due to a paucity of well-preserved postcranial material. Here we describe the morphology of the known vertebral column in Remingtonocetus domandaensis based largely on a single well-preserved partial skeleton recovered from the upper Domanda Formation of Pakistan. The specimen preserves most of the precaudal vertebral column in articulation and includes seven complete cervical vertebrae, ten partial to complete thoracic vertebrae, six complete lumbar vertebrae, and the first three sacral vertebrae. Cervical centra are long and possess robust, imbricating transverse processes that stabilized the head and neck. Lumbar vertebrae allowed for limited flexibility and probably served primarily to stabilize the lumbar column during forceful retraction of the hind limbs. Vertebral evidence, taken together with pelvic and femoral morphology, is most consistent with interpretation of Remingtonocetus domandaensis as an animal that swam primarily by powerful movement of its hind limbs rather than dorsoventral undulation of its body axis.     

The giraffe (Giraffa camelopardalis) cervical vertebral column: a heuristic example in understanding evolutionary processes?

The current study considers the osteological morphology of the giraffe (Giraffa camelopardalis) vertebral column, with emphasis on evaluating both the adaptive and constraining features compared with other ungulates as a heuristic example in understanding evolutionary processes. Vertebral columns of giraffes varying in age from calf to adult were studied in order to understand the potential evolutionary scenarios that might have led to the modern phenotype. Data from the giraffe sample were then compared with the results from several other ungulate species, including the okapi and two species of camelids that also have visibly elongated necks. Our results show that the elongated neck of the modern giraffe appears to specifically result from evolutionary changes affecting the seven cervical vertebrae, independent of the remainder of the vertebral column. The cervical vertebrae comprise over half of the length of the total vertebral column in the giraffe. The increases in cervical vertebrae lengths also appear to be allometrically constrained, with alterations in the overall length of the neck resulting from the elongation of the entire cervical series, rather than from a single vertebra or subset of vertebrae. We place our results in the context of hypotheses concerning the origin and evolution of the giraffe neck, and the evolution of long necks in a broader sense. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155 , 736–757.     

Patterns of growth in the presacral vertebral column of the leopard gecko (Eublepharis macularius)

Postnatal growth patterns within the vertebral column may be informative about body proportions and regionalization. We measured femur length, lengths of all pre‐sacral vertebrae, and lengths of intervertebral spaces, from radiographs of a series of 21 Eublepharis macularius, raised under standard conditions and covering most of the ontogenetic body size range. Vertebrae were grouped into cervical, sternal, and dorsal compartments, and lengths of adjacent pairs of vertebrae were summed before analysis. Femur length was included as an index of body size. Principal component analysis of the variance‐covariance matrix of these data was used to investigate scaling among them. PC1 explained 94.19% of total variance, interpreted as the variance due to body size. PC1 differed significantly from the hypothetical isometric vector, indicating overall allometry. The atlas and axis vertebrae displayed strong negative allometry; the remainder of the vertebral pairs exhibited weak negative allometry, isometry or positive allometry. PC1 explained a markedly smaller amount of variance for the vertebral pairs of the cervical compartment than for the remainder of the vertebral pairs, with the exception of the final pair. The relative standard deviations of the eigenvalues from the PCAs of the three vertebral compartments indicated that the vertebrae of the cervical compartment were less strongly integrated by scaling than were the sternal or dorsal vertebrae, which did not differ greatly between themselves in their strong integration, suggesting that the growth of the cervical vertebrae is constrained by the mechanical requirements of the head. Regionalization of the remainder of the vertebral column is less clearly defined but may be associated with wave form propagation incident upon locomotion, and by locomotory changes occasioned by tail autotomy and regeneration. Femur length exhibits negative allometry relative to individual vertebral pairs and to vertebral column length, suggesting a change in locomotor requirements over the ontogenetic size range.     

Functional morphology of the primate head and neck

The vertebral column plays a key role in maintaining posture, locomotion, and transmitting loads between body components. Cervical vertebrae act as a bridge between the torso and head and play a crucial role in the maintenance of head position and the visual field. Despite its importance in positional behaviors, the functional morphology of the cervical region remains poorly understood, particularly in comparison to the thoracic and lumbar sections of the spinal column. This study tests whether morphological variation in the primate cervical vertebrae correlates with differences in postural behavior. Phylogenetic generalized least-squares analyses were performed on a taxonomically broad sample of 26 extant primate taxa to test the link between vertebral morphology and posture. Kinematic data on primate head and neck postures were used instead of behavioral categories in an effort to provide a more direct analysis of our functional hypothesis. Results provide evidence for a function-form link between cervical vertebral shape and postural behaviors. Specifically, taxa with more pronograde heads and necks and less kyphotic orbits exhibit cervical vertebrae with longer spinous processes, indicating increased mechanical advantage for deep nuchal musculature, and craniocaudally longer vertebral bodies and more coronally oriented zygapophyseal articular facets, suggesting an emphasis on curve formation and maintenance within the cervical lordosis, coupled with a greater resistance to translation and ventral displacement. These results not only document support for functional relationships in cervical vertebrae features across a wide range of primate taxa, but highlight the utility of quantitative behavioral data in functional investigations. Am J Phys Anthropol 156:531–542, 2015. © 2015 Wiley Periodicals, Inc.     

Morphological integration and serial homology: A case study of the cranium and anterior vertebrae in salamanders

Serial homology or the repetition of equivalent developmental units and their derivatives is a phenomenon encountered in a variety of organisms, with the vertebrate axial skeleton as one of the most notable examples. Serially homologous structures can be viewed as an appropriate model system for studying morphological integration and modularity, due to the strong impact of development on their covariation. Here, we explored the pattern of morphological integration of the cranium and the first three serially homologous structures (atlas, first, and second trunk vertebrae) in salamandrid salamanders, using micro-CT scanning and three-dimensional geometric morphometrics. We explored the integration between structures at static and evolutionary levels. Effects of allometry on patterns of modularity were also taken into account. At the static level (within species), we analyzed inter-individual variation in shape to detect functional modules and intra-individual variation to detect developmental modules. Significant integration (based on inter-individual variation) among all structures was detected and allometry is shown to be an important integrating factor. The pattern of intra-individual, asymmetric variation indicates statistically significant developmental integration between the cranium and the atlas and between the first two trunk vertebrae. At the evolutionary level (among species), the cranium, atlas, and trunk vertebrae separate as different modules. Our results show that morphological integration at the evolutionary level coincides with morphological and functional differentiation of the axial skeleton, allowing the more or less independent evolutionary changes of the cranial skeleton and the vertebral column, regardless of the relatively strong integration at the static level. The observed patterns of morphological integration differ across levels, indicating different impacts of developmental and phylogenetic constraints and functional demands.     

Modular evolution of the Cetacean vertebral column

Modular theory predicts that hierarchical developmental processes generate hierarchical phenotypic units that are capable of independent modification. The vertebral column is an overtly modular structure, and its rapid phenotypic transformation in cetacean evolution provides a case study for modularity. Terrestrial mammals have five morphologically discrete vertebral series that are now known to be coincident with Hox gene expression patterns. Here, I present the hypothesis that in living Carnivora and Artiodactyla, and by inference in the terrestrial ancestors of whales, the series are themselves components of larger precaudal and caudal modular units. Column morphology in a series of fossil and living whales is used to predict the type and sequence of developmental changes responsible for modification of that ancestral pattern. Developmental innovations inferred include independent meristic additions to the precaudal column in basal archaeocetes and basilosaurids, stepwise homeotic reduction of the sacral series in protocetids, and dissociation of the caudal series into anterior tail and fluke subunits in basilosaurids. The most dramatic change was the novel association of lumbar and anterior caudal vertebrae in a module that crosses the precaudal/caudal boundary. This large unit is defined by shared patterns of vertebral morphology, count, and size in all living whales (Neoceti).     

A method for estimation of lateral and vertical mobility of platycoelous vertebrae of tetrapods

A new method for the estimation of dorsoventral and lateral mobility of platycoelous vertebrae with V-shaped (radial) articular facets on the zygapophyses is developed. This vertebral pattern is observed in dinosaurs, some other fossil reptiles, and in the cervical and lumbar regions of mammals. Based on theoretical biomechanical analysis of the intervertebral discs and articulations between zygapophyses, the estimation formulas are developed and calibrated, using precise measurements of mobility between cervical vertebrae of domestic sheep. The method is applied to the presacral vertebrae of the horned dinosaur Protoceratops andrewsi. In its cervical, lumbar, and anterior thoracic regions, the differences between the calculated amplitudes of movements and the sought true values are expected to range within ±5°. As compared to the sheep, Protoceratops shows a greater lateral mobility in the presacral region and reduced vertical mobility in the cervical region.     

Regional variation in morphology of vertebral centra and intervertebral joints in striped bass,Morone saxatilis

The vertebral column of fishes has traditionally been divided into just two distinct regions, abdominal and caudal. Recently, however, developmental, morphological, and mechanical investigations have brought this traditional regionalization scheme into question. Alternative regionalization schema advocate the division of the abdominal vertebrae into cervical, abdominal, and in some cases, transitional regions. Here, we investigate regional variation at the level of the vertebrae and intervertebral joint (IVJ) tissues in the striped bass, Morone saxatilis. We use gross dissection, histology, and polarized light imaging to quantify vertebral height, width, length, IVJ length, IVJ tissue volume and cross‐sectional area, and vertical septum fiber populations, and angles of insertion. Our results reveal regional differences between the first four (most rostral) abdominal vertebrae and IVJs and the next six abdominal vertebrae and IVJs, supporting the recognition of a distinct cervical region. We found significant variation in vertebral length, width, and height from cranial to caudal. In addition, we see a significant decline in the volume of notochordal cells and the cross‐sectional area of the fibrous sheath from cranial to caudal. Further, polarized light imaging revealed four distinct fiber populations within the vertical septum in the cervical and abdominal regions in contrast with just one fiber population found in the caudal region. Measurement of the insertion angles of these fiber populations revealed significant differences between the cervical and abdominal regions. Differences in vertebral, IVJ, and vertical septum morphology all predict greater range of motion and decreased stiffness in the caudal region of the fish compared with the cervical and abdominal regions. J. Morphol., 2012. © 2011 Wiley Periodicals, Inc.     

Correlation between Hox code and vertebral morphology in archosaurs

The relationship between developmental genes and phenotypic variation is of central interest in evolutionary biology. An excellent example is the role of Hox genes in the anteroposterior regionalization of the vertebral column in vertebrates. Archosaurs (crocodiles, dinosaurs including birds) are highly variable both in vertebral morphology and number. Nevertheless, functionally equivalent Hox genes are active in the axial skeleton during embryonic development, indicating that the morphological variation across taxa is likely owing to modifications in the pattern of Hox gene expression. By using geometric morphometrics, we demonstrate a correlation between vertebral Hox code and quantifiable vertebral morphology in modern archosaurs, in which the boundaries between morphological subgroups of vertebrae can be linked to anterior Hox gene expression boundaries. Our findings reveal homologous units of cervical vertebrae in modern archosaurs, each with their specific Hox gene pattern, enabling us to trace these homologies in the extinct sauropodomorph dinosaurs, a group with highly variable vertebral counts. Based on the quantifiable vertebral morphology, this allows us to infer the underlying genetic mechanisms in vertebral evolution in fossils, which represents not only an important case study, but will lead to a better understanding of the origin of morphological disparity in recent archosaur vertebral columns.     

Can habitat characteristics shape vertebral morphology in dolphins? An example of two phylogenetically related species from southern South America

Fast swimming pelagic cetacean species have osteological characteristics that promote a more stable spine in comparison to that of coastal species. The Peale's dolphin (Lagenorhynchus australis) and the hourglass dolphin (Lagenorhynchus cruciger) have a close phylogenetic relationship and are found in coastal and pelagic waters in the Southern Hemisphere, respectively. The aim of this work was to study the relationship between the vertebral column's morphology and its flexibility, across these species of contrasting habitats. Vertebral counts and multiple measurements of each vertebra were used to infer intervertebral flexibility. Bivariate plots and discriminant multivariate analyses were employed to compare each functional region along the vertebral column. Both species displayed a regionalization of the column into three stable regions and two flexible areas, which statistically differ in the proportion of the skeleton occupied in each species. While the Peale's dolphin has rounder vertebrae, associated with higher flexibility, the hourglass dolphin has disk‐shaped vertebrae and strongly inclined processes related to high stability. Although the species are closely related phylogenetically, vertebral morphology is influenced by a diverse set of ecological and behavioral factors, reflecting a high degree of vertebral plasticity within the genus.     

Turning maneuvers in sharks: Predicting body curvature from axial morphology

Given the diversity of vertebral morphologies among fishes, it is tempting to propose causal links between axial morphology and body curvature. We propose that shape and size of the vertebrae, intervertebral joints, and the body will more accurately predict differences in body curvature during swimming rather than a single meristic such as total vertebral number alone. We examined the correlation between morphological features and maximum body curvature seen during routine turns in five species of shark: Triakis semifasciata, Heterodontus francisci, Chiloscyllium plagiosum, Chiloscyllium punctatum, and Hemiscyllium ocellatum. We quantified overall body curvature using three different metrics. From a separate group of size‐matched individuals, we measured 16 morphological features from precaudal vertebrae and the body. As predicted, a larger pool of morphological features yielded a more robust prediction of maximal body curvature than vertebral number alone. Stepwise linear regression showed that up to 11 features were significant predictors of the three measures of body curvature, yielding highly significant multiple regressions with r² values of 0.523, 0.537, and 0.584. The second moment of area of the centrum was always the best predictor, followed by either centrum length or transverse height. Ranking as the fifth most important variable in three different models, the body's total length, fineness ratio, and width were the most important non‐vertebral morphologies. Without considering the effects of muscle activity, these correlations suggest a dominant role for the vertebral column in providing the passive mechanical properties of the body that control, in part, body curvature during swimming. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Evolution of the hominoid vertebral column: The long and the short of it

The postcranial axial skeleton exhibits considerable morphological and functional diversity among living primates. Particularly striking are the derived features in hominoids that distinguish them from most other primates and mammals. In contrast to the primitive catarrhine morphotype, which presumably possessed an external (protruding) tail and emphasized more pronograde trunk posture, all living hominoids are characterized by the absence of an external tail and adaptations to orthograde trunk posture. Moreover, modern humans evolved unique vertebral features that satisfy the demands of balancing an upright torso over the hind limbs during habitual terrestrial bipedalism. Our ability to identify the evolutionary timing and understand the functional and phylogenetic significance of these fundamental changes in postcranial axial skeletal anatomy in the hominoid fossil record is key to reconstructing ancestral hominoid patterns and retracing the evolutionary pathways that led to living apes and modern humans. Here, we provide an overview of what is known about evolution of the hominoid vertebral column, focusing on the currently available anatomical evidence of three major transitions: tail loss and adaptations to orthograde posture and bipedal locomotion.     

The ontogenic development of the vertebrae in some gekkonoid lizards

The ontogeny of amphicoelous vertebrae was studied in Ptyodactylus hasselquistii and Hemidactylus turcicus, and that of procoelous vertebrae, in Sphaerodactylus argus. The embryos were assigned arbitrary stages, drawn to scale, and mostly studied in serial sections. Resegmentation occurs as in all amniotes. A sclerocoel divides each sclerotome into an anterior “presclerotomite” and a denser posterior “postsclerotomite.” Tissue surrounding the intersegmental boundary forms the centrum, which is intersegmental. Tissue around the sclerocoel builds the intervertebral structures, which are midsegmental. In the trunk and neck, postsclerotomites form neural arches, and presclerotomites build zygapophyses. The adult centrum consists of the perichordal primary centrum, plus neural arch bases (= secondary centrum). Between the latter and the arch proper, a neurocentral suture persists until obliterated in maturity. A dorso-ventral central canal persists on either side of the primary centrum, between the latter and the secondary centrum. The notochord becomes true cartilage midvertebrally in all vertebrae, and elastic cartilage intervertebrally in the posterior caudal region. Elsewhere its characteristic tissue persists. Intervertebrally, cervical hypapophyses, caudal chevrons and chevron-bases in the trunk are preformed early in cartilage. Directly ossifying median intercentra are added later in all regions. The first cervical presclerotomite is absent: the hypapophysis (= corpus) of the atlas consists exclusively of postsclerotomitic tissue, there is no proatlas, and the odontoid lacks the apical half-centrum present in other lepidosaurians. In the autotomous caudal region presclerotomites are as prominent as postsclerotomites. Both build neural arches, the two arches of each vertebra remaining distinct and ossifying separately, so that the intersegmental autotomy split persists between them. The last sclerotome is complete, its postsclerotomite forming a half centrum which ossifies. In Sphaerodactylus, while the vertebrae ossify, each intervertebral ring becomes concave anteriorly, convex posteriorly; it remains as a cushion between the condyle and a facet formed by differential growth of the centra. Thus these procoelous centra resemble the amphicoelous centra of Ptyodactylus and Hemidactylus, rather than the procoelus centra of other squamates. The vertebral column of Gekkonoidea closely resembles in its development and microscopical structure that of Sphenodon.     

Morphometrics of the skeleton of Dermophis mexicanus (Amphibia: Gymnophiona). Part I. The vertebrae,with comparisons to other species

Morphometric analysis of vertebral structure in caecilians (Amphibia: Gymnophiona) is presented. Ontogenetic variation in Dermophis mexicanus is analyzed through the 100+ vertebrae composing the column. Vertebral structure in adult D. mexicanus is compared with that in Ichthyophis glutinosus and Typhlonectes compressicauda. Centra of the atlas, second, tenth, 20th, and 50th vertebrae grow at allometrically different rates in D. mexicanus, though the 20th and 50th are not significantly different, Growth appears significantly slower in several dimensions of anterior and posterior vertebrae relative to midtrunk vertebrae in all three species. Mensural patterns throughout the entire column are similar in the terrestrial burrowers D. mexicanus and I. glutinosus; patterns in the aquatic T. compressicauda differ substantially from those of the burrowing species and are strongly influenced by allometry. Of the 112 D. mexicanus examined, 13.4% had vertebral anomalies, usually fusions.     

Crossing the frontier: a hypothesis for the origins of meristic constraint in mammalian axial patterning

Serially homologous systems with high internal differentiation frequently exhibit meristic constraints, although the developmental basis for constraint is unknown. Constraints in the counts of the cervical and lumbosacral vertebral series are unique to mammals, and appeared in the Triassic, early in their history. Concurrent adaptive modifications of the mammalian respiratory and locomotor systems involved a novel source of cells for muscularization of the diaphragm from cervical somites, and the loss of ribs from lumbar vertebrae. Each of these innovations increased the modularity of the somitic mesoderm, and altered somitic and lateral plate mesodermal interactions across the lateral somitic frontier. These developmental innovations are hypothesized here to constrain the anteroposterior transposition of the limbs along the column, and thus also cervical and thoracolumbar count. Meristic constraints are therefore regarded here as the nonadaptive, secondary consequences of adaptive respiratory and locomotor traits.     

A new hero emerges: another exceptional mammalian spine and its potential adaptive significance

The hero shrew''s (Scutisorex somereni) massive interlocking lumbar vertebrae represent the most extreme modification of the vertebral column known in mammals. No intermediate form of this remarkable morphology is known, nor is there any convincing theory to explain its functional significance. We document a new species in the heretofore monotypic genus Scutisorex; the new species possesses cranial and vertebral features representing intermediate character states between S. somereni and other shrews. Phylogenetic analyses of DNA sequences support a sister relationship between the new species and S. somereni. While the function of the unusual spine in Scutisorex is unknown, it gives these small animals incredible vertebral strength. Based on field observations, we hypothesize that the unique vertebral column is an adaptation allowing these shrews to lever heavy or compressive objects to access concentrated food resources inaccessible to other animals.     

Shape variation in presacral vertebrae of saltasaurine titanosaurs (Dinosauria,Sauropoda)

Titanosaurs were small- to giant-sized sauropods, highly derived and highly pneumatic. Using morphometric analyses, we studied differences in shape of the presacral vertebral centra in some of these sauropods, especially in saltasaurines, and compared asymmetry patterns in lateral pneumatic foramina (LPF) between these titanosaurs and avian and non-avian theropods. Geometric morphometric analyses showed that the cervical centra tend to be elongated and dorsoventrally short, with an elliptical LPF located in the middle of the centrum; dorsal centra tend to be short and higher than the cervical centra, with the LPF slightly displaced to the anterior region. Shape variation can be described as a result of the ordering of the vertebrae within both the cervical and dorsal sequences, and therefore these methods can be applied to predict the position of isolated vertebrae. A persistent pattern of asymmetry among LPF was observed when length–height indexes were plotted. The right LPF are usually larger than those on the left side in the cervical vertebrae (except in Saltasaurus loricatus) but variable in the dorsal vertebrae. We propose an explanation of this asymmetry based on the asymmetric arrangement of viscera and late development of the respiratory (and air sacs) system.