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Morphological consequences of artificial cranial deformation: Modularity and integration.

ABSTRACT: 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.

SUBMITTER: Puschel TA

PROVIDER: S-EPMC6980596 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Morphological consequences of artificial cranial deformation: Modularity and integration.

Püschel Thomas A TA Friess Martin M Manríquez Germán G

PloS one 20200124 1

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 t ...[more]

PMID: 31978063

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Project description:BackgroundAlthough variation provides the raw material for natural selection and evolution, few empirical data exist about the factors controlling morphological variation. Because developmental constraints on variation are expected to act by influencing trait correlations, studies of modularity offer promising approaches that quantify and summarize patterns of trait relationships. Modules, highly-correlated and semi-autonomous sets of traits, are observed at many levels of biological organization, from genes to colonies. The evolutionary significance of modularity is considerable, with potential effects including constraining the variation of individual traits, circumventing pleiotropy and canalization, and facilitating the transformation of functional structures. Despite these important consequences, there has been little empirical study of how modularity influences morphological evolution on a macroevolutionary scale. Here, we conduct the first morphometric analysis of modularity and disparity in two clades of placental mammals, Primates and Carnivora, and test if trait integration within modules constrains or facilitates morphological evolution.Principal findingsWe used both randomization methods and direct comparisons of landmark variance to compare disparity in the six cranial modules identified in previous studies. The cranial base, a highly-integrated module, showed significantly low disparity in Primates and low landmark variance in both Primates and Carnivora. The vault, zygomatic-pterygoid and orbit modules, characterized by low trait integration, displayed significantly high disparity within Carnivora. 14 of 24 results from analyses of disparity show no significant relationship between module integration and morphological disparity. Of the ten significant or marginally significant results, eight support the hypothesis that integration within modules constrains morphological evolution in the placental skull. Only the molar module, a highly-integrated and functionally important module, showed significantly high disparity in Carnivora, in support of the facilitation hypothesis.ConclusionsThis analysis of within-module disparity suggested that strong integration of traits had little influence on morphological evolution over large time scales. However, where significant results were found, the primary effect of strong integration of traits was to constrain morphological variation. Thus, within Primates and Carnivora, there was some support for the hypothesis that integration of traits within cranial modules limits morphological evolution, presumably by limiting the variation of individual traits.

Project description:A fundamental challenge of morphology is to identify the underlying evolutionary and developmental mechanisms leading to correlated phenotypic characters. Patterns and magnitudes of morphological integration and their association with environmental variables are essential for understanding the evolution of complex phenotypes, yet the nature of the relevant selective pressures remains poorly understood. In this study, the adaptive significance of morphological integration was evaluated through the association between feeding mechanics, ingestive behavior and craniofacial variation. Five capuchin species were examined, Cebus apella sensu stricto, Cebus libidinosus, Cebus nigritus, Cebus olivaceus and Cebus albifrons. Twenty three-dimensional landmarks were chosen to sample facial regions experiencing high strains during feeding, characteristics affecting muscular mechanical advantage and basicranial regions. Integration structure and magnitude between and within the oral and zygomatic subunits, between and within blocks maximizing modularity and within the face, the basicranium and the cranium were examined using partial-least squares, eigenvalue variance, integration indices compared inter-specifically at a common level of sampled population variance and cluster analyses. Results are consistent with previous findings reporting a relative constancy of facial and cranial correlation patterns across mammals, while covariance magnitudes vary. Results further suggest that food material properties structure integration among functionally-linked facial elements and possibly integration between the face and the basicranium. Hard-object-feeding capuchins, especially C. apella s.s., whose faces experience particularly high biomechanical loads are characterized by higher facial and cranial integration especially compared to C. albifrons, likely because morphotypes compromising feeding performance are selected against in species relying on obdurate fallback foods. This is the first study to report a link between food material properties and facial and cranial integration. Furthermore, results do not identify the consistent presence of cranial modules yielding support to suggestions that despite the distinct embryological imprints of its elements the cranium of placental mammals is not characterized by a modular architecture.

Project description:BackgroundCaecilians (Gymnophiona) are the least speciose extant lissamphibian order, yet living forms capture approximately 250 million years of evolution since their earliest divergences. This long history is reflected in the broad range of skull morphologies exhibited by this largely fossorial, but developmentally diverse, clade. However, this diversity of form makes quantification of caecilian cranial morphology challenging, with highly variable presence or absence of many structures. Consequently, few studies have examined morphological evolution across caecilians. This extensive variation also raises the question of degree of conservation of cranial modules (semi-autonomous subsets of highly-integrated traits) within this clade, allowing us to assess the importance of modular organisation in shaping morphological evolution. We used an intensive surface geometric morphometric approach to quantify cranial morphological variation across all 32 extant caecilian genera. We defined 16 cranial regions using 53 landmarks and 687 curve and 729 surface sliding semilandmarks. With these unprecedented high-dimensional data, we analysed cranial shape and modularity across caecilians assessing phylogenetic, allometric and ecological influences on cranial evolution, as well as investigating the relationships among integration, evolutionary rate, and morphological disparity.ResultsWe found highest support for a ten-module model, with greater integration of the posterior skull. Phylogenetic signal was significant (Kmult?=?0.87, p < 0.01), but stronger in anterior modules, while allometric influences were also significant (R2?=?0.16, p?< 0.01), but stronger posteriorly. Reproductive strategy and degree of fossoriality were small but significant influences on cranial morphology (R2?=?0.03-0.05), after phylogenetic (p?<?0.03) and multiple-test (p?<?0.05) corrections. The quadrate-squamosal 'cheek' module was the fastest evolving module, perhaps due to its pivotal role in the unique dual jaw-closing mechanism of caecilians. Highly integrated modules exhibited both high and low disparities, and no relationship was evident between integration and evolutionary rate.ConclusionsOur high-dimensional approach robustly characterises caecilian cranial evolution and demonstrates that caecilian crania are highly modular and that cranial modules are shaped by differential phylogenetic, allometric, and ecological effects. More broadly, and in contrast to recent studies, this work suggests that there is no simple relationship between integration and evolutionary rate or disparity.

Dataset Information

Morphological consequences of artificial cranial deformation: Modularity and integration.

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Morphological consequences of artificial cranial deformation: Modularity and integration.

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