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Ecomorphological diversification in squamates from conserved pattern of cranial integration.

ABSTRACT: Factors intrinsic and extrinsic to organisms dictate the course of morphological evolution but are seldom considered together in comparative analyses. Among vertebrates, squamates (lizards and snakes) exhibit remarkable morphological and developmental variations that parallel their incredible ecological spectrum. However, this exceptional diversity also makes systematic quantification and analysis of their morphological evolution challenging. We present a squamate-wide, high-density morphometric analysis of the skull across 181 modern and extinct species to identify the primary drivers of their cranial evolution within a unified, quantitative framework. Diet and habitat preferences, but not reproductive mode, are major influences on skull-shape evolution across squamates, with fossorial and aquatic taxa exhibiting convergent and rapid changes in skull shape. In lizards, diet is associated with the shape of the rostrum, reflecting its use in grasping prey, whereas snakes show a correlation between diet and the shape of posterior skull bones important for gape widening. Similarly, we observe the highest rates of evolution and greatest disparity in regions associated with jaw musculature in lizards, whereas those forming the jaw articulation evolve faster in snakes. In addition, high-resolution ancestral cranial reconstructions from these data support a terrestrial, nonfossorial origin for snakes. Despite their disparate evolutionary trends, lizards and snakes unexpectedly share a common pattern of trait integration, with the highest correlations in the occiput, jaw articulation, and palate. We thus demonstrate that highly diverse phenotypes, exemplified by lizards and snakes, can and do arise from differential selection acting on conserved patterns of phenotypic integration.

SUBMITTER: Watanabe A

PROVIDER: S-EPMC6642379 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Ecomorphological diversification in squamates from conserved pattern of cranial integration.

Watanabe Akinobu A Fabre Anne-Claire AC Felice Ryan N RN Maisano Jessica A JA Müller Johannes J Herrel Anthony A Goswami Anjali A

Proceedings of the National Academy of Sciences of the United States of America 20190701 29

Factors intrinsic and extrinsic to organisms dictate the course of morphological evolution but are seldom considered together in comparative analyses. Among vertebrates, squamates (lizards and snakes) exhibit remarkable morphological and developmental variations that parallel their incredible ecological spectrum. However, this exceptional diversity also makes systematic quantification and analysis of their morphological evolution challenging. We present a squamate-wide, high-density morphometric ...[more]

PMID: 31262818

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Project description:BackgroundMorphological integration refers to the tendency of anatomical structures to show correlated variations because they develop in response to shared developmental processes or function in concert with other structures. The objective of this study was to determine the relationships between the dimensions of different cranial-cervical-facial structures in patients with Down syndrome (DS).MethodologyThe study group consisted of 41 individuals with DS who had undergone cone-beam computed tomography (CBCT) at the Dental Radiology Unit of the University of Santiago de Compostela (Spain). In the historical archive of this same unit, 41 CBCTs belonging to individuals with no known systemic disorders or severe malformations of the maxillofacial region were selected, forming an age and sex-matched control group. Twenty-nine measurements were performed on each participant's CBCT images, which were grouped into three blocks: atlantoaxial dimensions, craniovertebral dimensions and cephalometric dimensions. To determine whether there were significant differences between the dimensions obtained in the DS and control groups, we applied multiple analysis of variance and linear discriminant analysis tests. The analysis of the association between blocks (in pairs) was performed with the canonical correlation analysis test.ResultsThe dimensions evaluated in the three blocks of variables of individuals with DS differ significantly from those of nonsyndromic controls (p < 0.001). The highest discriminative capacity to identify controls and patients with DS was obtained with the cephalometric dimensions (87.5%). With regard to the association between blocks (two-by-two measurements), we found no significant relationship in the DS group. However, we confirmed a statistically significant correlation between all pairs of blocks of variables in the controls, especially between the atlantoaxial and cephalometric dimensions (p < 0.001) and between the craniovertebral and cephalometric dimensions (p < 0.001).ConclusionsOur results confirm a very poor morphological integration of the cranial-cervical-maxillary complex in individuals with DS. This finding reinforces the proposal that gene overload enhances the channeling process.

Project description:The cranium is an anatomically complex structure. One source of its complexity is due to its modular organization. Cranial modules are distinct and partially independent units that interact substantially during ontogeny thus generating morphological integration. Artificial Cranial Deformation (ACD) occurs when the human skull is intentionally deformed, through the use of different deforming devices applied to the head while it is developing. Hence, ACD provides an interesting example to assess the degree to which biomechanical perturbations of the developing neurocranium impact on the degree of morphological integration in the skull as a whole. The main objective of this study was to assess how ACD affects the morphological integration of the skull. This was accomplished by comparing a sample of non-deformed crania and two sets of deformed crania (i.e. antero-posterior and oblique). Both developmental and static modularity and integration were assessed through Generalized Procrustes Analysis by considering the symmetric and asymmetric components of variation in adults, using 3D landmark coordinates as raw data. The presence of two developmental modules (i.e. viscero and neurocranium) in the skull was tested. Then, in order to understand how ACD affects morphological integration, the covariation pattern between the neuro and viscerocranium was examined in antero-posterior, oblique and non-deformed cranial categories using Partial Least-Squares. The main objective of this study was to assess how ACD affects the morphological integration of the skull. This was accomplished by comparing a sample of deformed (i.e. antero-posterior and oblique) and non-deformed crania. Hence, differences in integration patterns were compared between groups. The obtained results support the modular organization of the human skull in the two analyzed modules. The integration analyses show that the oblique ACD style differentially affects the static morphological integration of the skull by increasing the covariance between neuro and viscerocranium in a more constrained way than in antero-posterior and non-deformed skulls. In addition, the antero-posterior ACD style seems to affect the developmental integration of the skull by directing the covariation pattern in a more defined manner as compared to the other cranial categories.

Project description:Replacement of lost cranial bone (partly mesodermal and partly neural crest-derived) is challenging and includes the use of nonviable allografts. To revitalize allografts, bone marrow-derived mesenchymal stromal cells (mesoderm-derived BM-MSCs) have been used with limited success. We hypothesize that coating of allografts with induced neural crest cell-mesenchymal progenitor cells (iNCC-MPCs) improves implant-to-bone integration in mouse cranial defects. Human induced pluripotent stem cells were reprogramed from dermal fibroblasts, differentiated to iNCCs and then to iNCC-MPCs. BM-MSCs were used as reference. Cells were labeled with luciferase (Luc2) and characterized for MSC consensus markers expression, differentiation, and risk of cellular transformation. A calvarial defect was created in non-obese diabetic/severe combined immunodeficiency (NOD/SCID) mice and allografts were implanted, with or without cell coating. Bioluminescence imaging (BLI), microcomputed tomography (μCT), histology, immunofluorescence, and biomechanical tests were performed. Characterization of iNCC-MPC-Luc2 vs BM-MSC-Luc2 showed no difference in MSC markers expression and differentiation in vitro. In vivo, BLI indicated survival of both cell types for at least 8 weeks. At week 8, μCT analysis showed enhanced structural parameters in the iNCC-MPC-Luc2 group and increased bone volume in the BM-MSC-Luc2 group compared to controls. Histology demonstrated improved integration of iNCC-MPC-Luc2 allografts compared to BM-MSC-Luc2 group and controls. Human osteocalcin and collagen type 1 were detected at the allograft-host interphase in cell-seeded groups. The iNCC-MPC-Luc2 group also demonstrated improved biomechanical properties compared to BM-MSC-Luc2 implants and cell-free controls. Our results show an improved integration of iNCC-MPC-Luc2-coated allografts compared to BM-MSC-Luc2 and controls, suggesting the use of iNCC-MPCs as potential cell source for cranial bone repair.

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Ecomorphological diversification in squamates from conserved pattern of cranial integration.

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Ecomorphological diversification in squamates from conserved pattern of cranial integration.

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