Evolutionary and ontogenetic changes of the anatomical organization and modularity in the skull of archosaurs

Hiu Wai Lee,Borja Esteve-Altava,Arhat Abzhanov

doi:10.1038/s41598-020-73083-3

Hiu Wai Lee, Borja Esteve-Altava + Show 1 more

Open Access

https://doi.org/10.1038/s41598-020-73083-3

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Abstract

Comparative anatomy studies of the skull of archosaurs provide insights on the mechanisms of evolution for the morphologically and functionally diverse species of crocodiles and birds. One of the key attributes of skull evolution is the anatomical changes associated with the physical arrangement of cranial bones. Here, we compare the changes in anatomical organization and modularity of the skull of extinct and extant archosaurs using an Anatomical Network Analysis approach. We show that the number of bones, their topological arrangement, and modular organization can discriminate birds from non-avian dinosaurs, and crurotarsans. We could also discriminate extant taxa from extinct species when adult birds were included. By comparing within the same framework, juveniles and adults for crown birds and alligator (Alligator mississippiensis), we find that adult and juvenile alligator skulls are topologically similar, whereas juvenile bird skulls have a morphological complexity and anisomerism more similar to those of non-avian dinosaurs and crurotarsans than of their own adult forms. Clade-specific ontogenetic differences in skull organization, such as extensive postnatal fusion of cranial bones in crown birds, can explain this pattern. The fact that juvenile and adult skulls in birds do share a similar anatomical integration suggests the presence of a specific constraint to their ontogenetic growth.

Highlights

Comparative anatomy studies of the skull of archosaurs provide insights on the mechanisms of evolution for the morphologically and functionally diverse species of crocodiles and birds
Eight species represent the transition from crurotarsan archosaur ancestor to modern crocodilians and 13 species represent the transition from non-avian theropods to modern birds as described p reviously[34,35,36,37,38,39,40,41,42,43]
A Principal Component Analysis (PCA) of the eight topological variables measured in skull network models discriminates skulls with different anatomical organizations

Summary

Introduction

Comparative anatomy studies of the skull of archosaurs provide insights on the mechanisms of evolution for the morphologically and functionally diverse species of crocodiles and birds. Werneburg et al compared the skull network-anatomy of a highly derived Tyrannosaurus rex, Alligator mississippiensis and Gallus gallus with that of an opossum, a tuatara, and a turtle[29] They found that the tyrannosaur has the most modular skull organization among these amniotes, with a modular separation of the snout in upper and lower sub-modules and the presence of a lower. Plateau and Foth used anatomical network analysis to study postnatal ontogenetic changes in the skulls of crown bird and non-avian theropods[30]. They found that early juvenile crown birds have skulls that are less integrated and more modular than those of more derived birds, resembling their non-avian theropod ancestors. We compared skull architectures using topological variables (i.e. network parameters) that capture whole-skull anatomical feature (modelling and analysis of anatomical networks were detailed p reviously[20,25,31])

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