Birds have peramorphic skulls, too: anatomical network analyses reveal oppositional heterochronies in avian skull evolution

Olivia Plateau,Christian Foth

doi:10.1038/s42003-020-0914-4

Abstract

In contrast to the vast majority of reptiles, the skulls of adult crown birds are characterized by a high degree of integration due to bone fusion, e.g., an ontogenetic event generating a net reduction in the number of bones. To understand this process in an evolutionary context, we investigate postnatal ontogenetic changes in the skulls of crown bird and non-avian theropods using anatomical network analysis (AnNA). Due to the greater number of bones and bone contacts, early juvenile crown birds have less integrated skulls, resembling their non-avian theropod ancestors, including Archaeopteryx lithographica and Ichthyornis dispars. Phylogenetic comparisons indicate that skull bone fusion and the resulting modular integration represent a peramorphosis (developmental exaggeration of the ancestral adult trait) that evolved late during avialan evolution, at the origin of crown-birds. Succeeding the general paedomorphic shape trend, the occurrence of an additional peramorphosis reflects the mosaic complexity of the avian skull evolution.

Highlights

In contrast to the vast majority of reptiles, the skulls of adult crown birds are characterized by a high degree of integration due to bone fusion, e.g., an ontogenetic event generating a net reduction in the number of bones
A similar relationship was found for the connectivity modularity in the skull of the non-avian theropod Tyrannosaurus rex and crown bird Gallus gallus, which based on anatomical network analysis (AnNA)[11] (Fig. 1a, b)
The skulls of adult non-avian archosaurs, including Archaeopteryx and Ichthyornis, differ significantly from adult crown birds in the number of bones (N) and bone contacts (K), density of connections (D), mean shortest path length (L), quality of identified modular partition (Qmax), parcellation (P), and number of S-modules and Q-modules, (Fig. 2; Table 1; all parameters are defined in the method section)

Summary

Introduction

In contrast to the vast majority of reptiles, the skulls of adult crown birds are characterized by a high degree of integration due to bone fusion, e.g., an ontogenetic event generating a net reduction in the number of bones. The skull bone configuration of extant bird hatchlings resembles, to a certain degree, that of nonavian theropods, implying a less integrated skull network with high connectivity modularity (Fig. 1c) To test this hypothesis, we investigated the contact and fusion patterns of skull bones and their impact on modularity during ontogeny in 41 extant birds and compared them with those of non-avian archosaurs (including 15 adult and two juvenile non-avian dinosaurs and an ontogenetic pair of Alligator mississippiensis; see Supplementary Data 1 and 2 file), using AnNA and phylogenetic comparative analyses (see the “Methods” section). The skulls of early juvenile crown birds, resemble those of non-avian theropods, including Archaeopteryx lithographica and Ichthyornis dispars In this context, phylogenetic comparisons indicate that the highly integrated adult bird skull evolved late during avian evolution, at the origin of crown-birds, and are a result of a peramorphosis (developmental exaggeration of the ancestral adult trait), which might be related to the origin of cranial kinesis. The sequential occurrence of oppositional heterochronies (i.e., a trended skull shape paedomorphosis within Coelurosauria followed by peramorphic skull bone fusion in the last common ancestor of crown birds) reflects the mosaic complexity of avian skull evolution, facilitating shape and ecological diversity

Methods

Results

Conclusion