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

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 nonavian 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.

A node-based informed modularity strategy to identify organizational modules in anatomical networks

“…These algorithms are faster and can be run unsupervised, which is important when analyzing many anatomical networks as part of a broader evolutionary study (e.g. Plateau and Foth, 2020 ) or when the actual modules are not the final end of the study (e.g. Esteve-Altava et al, 2019 ).…”

“…articulations), and then quantifies their topological organization as a proxy to understand the biological features of the organism. Anatomical studies using network analysis have focused on comparing the development, function, and evolution of morphological systems, from invertebrates to vertebrates, including extant and extinct organisms ( Dos Santos et al, 2017 ; Esteve-Altava et al, 2013a , b , 2018 , 2019 ; Fernández et al, 2020 ; Fontanarrosa et al, 2020 ; Kerkman et al, 2018 ; Murphy et al, 2018 ; Ostachuk, 2019 ; Plateau and Foth, 2020 ; Saucède et al, 2015 ; Sookias et al, 2020 ).…”

“…The vertebrate skull has attracted most of the research on morphological modularity ( Esteve-Altava, 2017b ). Here, anatomical network studies have tried to unveil the topological units of organization to understand how they vary in evolution ( Arnold et al, 2017 ; Esteve-Altava et al, 2015 ; Plateau and Foth, 2020 ; Werneburg et al, 2019 ), but also in normal and pathological development ( Diogo et al, 2019 ; Esteve-Altava and Rasskin-Gutman, 2015 ). Moreover, some other studies have applied network methods to identify modules of landmark-based morphometric correlations rather than topological relations ( Ivan Perez et al, 2009 ; Suzuki, 2013 ).…”

“…The second problem is that algorithms sometimes find asymmetric modules in otherwise symmetric networks, which challenges basic biological assumptions about symmetry of bilateral body parts (e.g. see discussion in the open peer-review report in Plateau and Foth, 2020 ). These problems can hinder anatomical network analyses and they fuel criticisms to this methodology from people unaware of these limitations.…”

The impact of allometry on vomer shape and its implications for the taxonomy and cranial kinesis of crown-group birds

“…Their kinesis is indicated by the loss of the jugal-postorbital bar and the ectopterygoid (resulting in a loss of contact in the jugal with the skull roof and the palate), the presence of a mobile bicondylar quadrate and a mobile joint between quadrate and quadratojugal. Recently, Plateau & Foth (2020)…”