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

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.

Modeling Skull Network Integrity at the Dawn of Amniote Diversification With Considerations on Functional Morphology and Fossil Jaw Muscle Reconstructions

“…Early diapsids are thought to have been adapted to feeding on agile prey (Evans, 2008), for which an increased intracranial mobility was necessary (see discussion further below). More crownward diapsids (Lee et al, 2020;Plateau and Foth, 2020) differ from the modeled early diapsids. Differences are likely associated with a change to a more carnivorous feeding behavior as exemplified in archosauriform evolution with †Euparkeria capensis representing a transitional form (Sookias et al, 2020) or †Tyrannosaurus rex showing specific snout adaptations .…”

“…Functional considerations of skull anatomy cannot be performed without proper knowledge on muscle anatomy, which is usually barely described in the literature for extant taxa and usually misses relevant information of muscle fiber-compositions and orientations and tendinous components. For extinct taxa, only gross morphology of musculature can be reconstructed on a rough anatomical level, mainly based on phylogenetic bracketing and by considering indications of possible attachment sites on bones (Witzmann and Werneburg, 2017) Rasskin-Gutman and Esteve-Altava, 2014; Diogo et al, 2015;Molnar et al, 2017;Lee et al, 2020;Plateau and Foth, 2020;Sookias et al, 2020). Rasskin-Gutman (2003) provided a first attempt to study skull modularity in relation to temporal openings and found, by comparing nine different tetrapod skulls, that the orbit is surrounded by a rather simple modular arrangement with one element attaching to at least three other adjacent elements.…”

“…Whereas "active" ones between three adjacent bones (i.e., foramina) cannot close because they surround other ("active") tissue like nerves or vessels, the "passive" ones in between four or more bones remain stable ("passive") along a phylogenetic lineage as long as no heterochronic event (relative growth in ontogeny) closes that opening. As such, to better understand transformations in temporal architecture, a greater focus on ontogenetic studies (Rieppel, 1984;Haridy et al, 2016;Werneburg, 2019;Lee et al, 2020) are urgently needed in the future.…”

Modularity patterns in mammalian domestication: Assessing developmental hypotheses for diversification

“…Within‐module integration levels have also been linked to the generation of disparity: lower integration within modules is linked to higher magnitudes of cranial disparity in mammals (Goswami and Polly 2010a) and archosaurs (Felice et al 2018; Lee et al. 2020). Thus, the architecture of trait interactions may affect an organism's response to selection, directing lineage diversification along favored pathways (Shirai and Marroig 2010; Melo et al.…”

Time to synchronize our clocks: Connecting developmental mechanisms and evolutionary consequences of heterochrony

“…Within the same organism, different traits can experience different types of heterochronies-a phenomenon known as mosaic or modular heterochrony (Bastir & Rosas, 2009;Koyabu et al, 2014). In birds, enlargement of the eyes and brain and shortening of the face are considered paedomorphic, while enlargement of the premaxilla to form a beak and the fusion of cranial bones within the same skull are peramorphic (Bhullar et al, 2012;Lee et al, 2020). In humans, the base of the skull that enables upright walking and the larger brain, cranium, and body sizes, result from an extended growth period and are peramorphic compared to ancestral apes (hypermorphosis).…”