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Correlation between Hox code and vertebral morphology in archosaurs.

Böhmer C, Rauhut OW, Wörheide G - Proc. Biol. Sci. (2015)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department für Geo- und Umweltwissenschaften und GeoBio-Center, Ludwig-Maximilians-Universität München, Richard-Wagner-Strasse 10, München 80333, Deutschland SNSB - Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Strasse 10, München 80333, Deutschland boehmer@vertevo.de.

ABSTRACT
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.

No MeSH data available.


Landmark set used in the geometric morphometric analysis. The numbered three-dimensional landmarks (red points) are shown on the fourth cervical vertebra of A. mississippiensis (three-dimensional scan). Detailed definitions of the 17 homologous landmarks are provided in the electronic supplementary material.
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RSPB20150077F1: Landmark set used in the geometric morphometric analysis. The numbered three-dimensional landmarks (red points) are shown on the fourth cervical vertebra of A. mississippiensis (three-dimensional scan). Detailed definitions of the 17 homologous landmarks are provided in the electronic supplementary material.

Mentions: Morphological variability within the cervical vertebral column of alligator, crocodile, chicken and the dinosaur Plateosaurus was evaluated by a combined morphological analysis. First, qualitative characters were collected and coded as binary or multistate characters. These characters include the presence and absence of osteological features, such as a ventral keel, a bifurcated neural spine and muscle insertion points that vary within each cervical series and could not be captured by homologous landmarks. Second, the morphological differences between the vertebrae within a cervical vertebral column were quantitatively analysed via three-dimensional landmark-based geometric morphometrics. Applying the software Landmark v. 3.0 [42], a series of 17 homologous landmarks were digitized on the three-dimensional scans of the cervical vertebrae (figure 1). The homologous points abstract the vertebral shape and characterize important osteological features, such as the articulation facets of the cervical ribs (diapophysis and parapophysis), which correlate with the corresponding articulating structures of the ribs (tuberculum and capitulum). The first cervical vertebra (atlas) is not included in the geometric morphometric analysis as it is highly modified and lacks specific serial homologies with postatlantal cervicals, and thus, several landmarks cannot be applied to it. The same three-dimensional landmark sets were applied to all analysed taxa in order to provide a comparable basis for the morphological study. Although there are transverse processes connecting the cervical ribs with the vertebral centrum, landmarks (LM) 13 and 14 are not applied in the analysis of chicken because their placement is not exactly repeatable owing to fusion of the ribs to the centra. Geometric morphometric data were processed using the software Morphologika [43] with the following procedures. The coordinates of all landmark sets were superimposed using general procrustes analysis. The Relative Warps (RW) analysis summarized the multi-dimensional information. With the applied settings, this method is equivalent to a principal components analysis. The shape differences were visualized with three-dimensional thin-plate splines. Using the software PAST [44], both datasets were assembled to one data matrix that served as basis for Principal Coordinates (PCO) Analysis. In order to find the similarity relationships among the vertebrae for each taxon, the superimposed three-dimensional landmark coordinates assembled with the qualitative character matrix were analysed with a PCO Analysis applying the Gower index [45,46]. Via the cluster analysis using the single linkage algorithm in combination with the Gower similarity index, the vertebrae were joined based on the smallest distance between them. This resulted in the establishment of morphological subregion patterns of the cervical series for the analysed taxa. Further details are provided in the electronic supplementary material.Figure 1.


Correlation between Hox code and vertebral morphology in archosaurs.

Böhmer C, Rauhut OW, Wörheide G - Proc. Biol. Sci. (2015)

Landmark set used in the geometric morphometric analysis. The numbered three-dimensional landmarks (red points) are shown on the fourth cervical vertebra of A. mississippiensis (three-dimensional scan). Detailed definitions of the 17 homologous landmarks are provided in the electronic supplementary material.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4590465&req=5

RSPB20150077F1: Landmark set used in the geometric morphometric analysis. The numbered three-dimensional landmarks (red points) are shown on the fourth cervical vertebra of A. mississippiensis (three-dimensional scan). Detailed definitions of the 17 homologous landmarks are provided in the electronic supplementary material.
Mentions: Morphological variability within the cervical vertebral column of alligator, crocodile, chicken and the dinosaur Plateosaurus was evaluated by a combined morphological analysis. First, qualitative characters were collected and coded as binary or multistate characters. These characters include the presence and absence of osteological features, such as a ventral keel, a bifurcated neural spine and muscle insertion points that vary within each cervical series and could not be captured by homologous landmarks. Second, the morphological differences between the vertebrae within a cervical vertebral column were quantitatively analysed via three-dimensional landmark-based geometric morphometrics. Applying the software Landmark v. 3.0 [42], a series of 17 homologous landmarks were digitized on the three-dimensional scans of the cervical vertebrae (figure 1). The homologous points abstract the vertebral shape and characterize important osteological features, such as the articulation facets of the cervical ribs (diapophysis and parapophysis), which correlate with the corresponding articulating structures of the ribs (tuberculum and capitulum). The first cervical vertebra (atlas) is not included in the geometric morphometric analysis as it is highly modified and lacks specific serial homologies with postatlantal cervicals, and thus, several landmarks cannot be applied to it. The same three-dimensional landmark sets were applied to all analysed taxa in order to provide a comparable basis for the morphological study. Although there are transverse processes connecting the cervical ribs with the vertebral centrum, landmarks (LM) 13 and 14 are not applied in the analysis of chicken because their placement is not exactly repeatable owing to fusion of the ribs to the centra. Geometric morphometric data were processed using the software Morphologika [43] with the following procedures. The coordinates of all landmark sets were superimposed using general procrustes analysis. The Relative Warps (RW) analysis summarized the multi-dimensional information. With the applied settings, this method is equivalent to a principal components analysis. The shape differences were visualized with three-dimensional thin-plate splines. Using the software PAST [44], both datasets were assembled to one data matrix that served as basis for Principal Coordinates (PCO) Analysis. In order to find the similarity relationships among the vertebrae for each taxon, the superimposed three-dimensional landmark coordinates assembled with the qualitative character matrix were analysed with a PCO Analysis applying the Gower index [45,46]. Via the cluster analysis using the single linkage algorithm in combination with the Gower similarity index, the vertebrae were joined based on the smallest distance between them. This resulted in the establishment of morphological subregion patterns of the cervical series for the analysed taxa. Further details are provided in the electronic supplementary material.Figure 1.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department für Geo- und Umweltwissenschaften und GeoBio-Center, Ludwig-Maximilians-Universität München, Richard-Wagner-Strasse 10, München 80333, Deutschland SNSB - Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Strasse 10, München 80333, Deutschland boehmer@vertevo.de.

ABSTRACT
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.

No MeSH data available.