Evolutionary insights from an anatomical network analysis of the hyolaryngeal apparatus in extant archosaurs (birds and crocodilians)

Abstract

Adaptive radiation of archosaurs, represented by crocodilians, non-avian dinosaurs, and birds, since the Mesozoic has been studied mainly based on their major skeletal elements (skull, vertebrae, and limbs). However, little is known about the evolution of their hyolaryngeal apparatus, which is involved with feeding, respiration, and vocalization, because of poor fossil preservation and the difficulty in determining the musculoskeletal homology of the apparatus. Network analysis is a framework to quantitatively characterize the topological organization of anatomical structures for comparing structural integration and modularity regardless of ambiguous homology. Herein, we modeled the musculoskeletal system of hyolarynx in six species of extant archosaurs and its sister-taxon turtle, and conducted a network analysis using network parameters, modular partition, and bone centrality in a phylogenetic framework. The network parameters reveal that ancestral archosaurs have reduced the numbers of elements and links and acquired complex networks as a whole domain with strong modularity in the hyolarynx. Furthermore, the modular partition and centrality reveal that the hyoids are highly evolvable, while the larynx is constrained and less evolvable.The archosaur hyolarynx exhibits different evolutionary trends: crocodilians with the system integration, basihyal simplification, and ceratobranchial centralization; and birds with the simplicity, weak integration, and modularity of the hyolarynx, laryngeal integration with cricoid centrality, and tongue-module expansion with the acquisition of paraglossal. Four hyolaryngeal bones (ceratobranchial, basihyal, paraglossal, and cricoid) have played important roles in archosaur evolution, and their fossil records are keys to understanding the two major archosaur lineages toward crocodilians and birds.

Morphological Diversity of Turtle Hyoid Apparatus is Linked to Feeding Behavior

“…In addition, they tend to develop broad attachment sites for musculature in the cornu brachiale I (e.g., Cyclanorbis, Pelochelys, Chitra, Chelus, and Chelodina ). Similar trends can be observed in association to the diversity of the musculature in the head of turtles, and in its integration with the hyoid apparatus ( Werneburg 2011 ; Yoshida et al. 2023 , respectively).…”

Dinosaurs of all ilks bow and pay tribute to Peter Dodson, their intrepid chronicler, in an Anatomical Record Special Issue in his honor

“…Rather, to name just some, they span a glorious gamut: from detailed descriptions of unusual Therapods from New Jersey (really? hadrosaurs, Jimmy Hoffa…who knew Jersey was actually interesting; sorry, JL is a native New Yorker and has little control when commenting on New Jersey; Gallagher, 2023); reports on a new iguanodontian dinosaur from South Africa (Forster et al, 2023); new insights on evolutionary relationships from analyses of the hyolaryngeal apparatus in extant archosaurs (i.e., birds and crocodilians; Yoshida et al, 2023); new reconstructions of the pectoral girdle and forelimb musculature of Megaraptora (Rolando et al, 2023); insights from osteohistology of Dromornis stironi with implications for understanding the histology of Australian mihirung birds (Chinsamy et al, 2023); insightful observations on fracture and disease in a large‐bodied ornithomimosaur with insights into identifying unusual endosteal bone in the fossil record (Chinzorig et al, 2023); a comprehensive assessment of the history and future of the study of morphometrics in the study on non‐avian dinosaurs (Hedrick, 2023); detailed modeling to assess and predict the abundance of large carnivorous dinosaurs of the Upper Jurassic Morrison Formation and the Upper Cretaceous Dinosaur Park formation (by Peter and JL's Yale classmate, the ever‐creative James Farlow; JL is still in awe at all the super‐bright dino dudes that surrounded him at Yale “back in the day”; Farlow et al, 2023); to a number of papers—naturally—on Peter's great love, the ceratopsians, including those by lead Guest Editor Fiorillo (Fiorillo & Tykoski, 2023) and Peter's successor teaching anatomy at Penn, Ali Nabavizadeh (Nabavizadeh, 2023). Even the cover of this Special Issue has been a creative homage to Peter, lovingly created by Anatomical Record Associate Editor (and artist extraordinaire) Adam Hartstone‐Rose (Hartstone‐Rose et al, 2023).…”

Introduction to Dinosaurs: New Ideas from Old Bones papers honoring Peter Dodson

“…They applied, for the first time, a network analysis to quantify evolutionary trends in the apparatus. Their study showed that the ceratobranchial, basihyal, cricoid, and paraglossal are likely keys in archosaur hyolaryngeal evolution (Yoshida et al, 2023). Mallon et al (2023) examined the smallest known examples of Gryposaurus notabilis that either reinforce or shed new light on developmental growth and biomechanics within the hadrosaurs.…”

“…Our understanding of the radiation of archosaurs has largely been based on major skeletal elements commonly found in the fossil record. Yoshida et al (2023) turned their attention instead to the hyolaryngeal apparatus, an important system for feeding, respiration, and vocalization. They applied, for the first time, a network analysis to quantify evolutionary trends in the apparatus.…”

“…They applied, for the first time, a network analysis to quantify evolutionary trends in the apparatus. Their study showed that the ceratobranchial, basihyal, cricoid, and paraglossal are likely keys in archosaur hyolaryngeal evolution (Yoshida et al, 2023).…”