Abstract
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.
Highlights
Caecilians (Gymnophiona) are the least speciose extant lissamphibian order, yet living forms capture approximately 250 million years of evolution since their earliest divergences
As there is a tendency for analyses of densely sampled semilandmarks to favour highly parameterised models and because not all possible groupings of modules can be assessed in Evaluating Modularity with Maximum Likelihood (EMMLi) analysis at present, we followed Felice and Goswami [19] and assessed the within- and between-region trait correlations for this model to determine whether any regions could be reasonably combined into larger modules
For the non-corrected data, five of the defined cranial regions were combined with other regions to form multi-region modules, resulting in a ten-module model of modularity
Summary
Caecilians (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. 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. Multiple levels of functional and developmental interactions have been demonstrated within Felidae, from the level of the individual vertebrae [9], to different vertebral regions [10], to the level of the presacral vertebral column [11] This hierarchy of interactions across the presacral vertebral column of felids demonstrates how multiple levels of organisation shape the morphological evolution of a complex structure
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