The tongue, with fleshy, muscular, and bony components, is an innovation of the earliest land-dwelling vertebrates with key functions in both feeding and respiration. Here, we bring together evidence from preserved hyoid elements from dinosaurs and outgroup archosaurs, including pterosaurs, with enhanced contrast x-ray computed tomography data from extant taxa. Midline ossification is a key component of the origin of an avian hyoid. The elaboration of the avian tongue includes the evolution of multiple novel midline hyoid bones and a larynx suspended caudal to these midline elements. While variable in dentition and skull shape, most bird-line archosaurs show a simple hyoid structure. Bony, or well-mineralized, hyoid structures in dinosaurs show limited modification in response to dietary shifts and across significant changes in body-size. In Dinosauria, at least one such narrow, midline element is variably mineralized in some basal paravian theropods. Only in derived ornithischians, pterosaurs and birds is further significant hyoid elaboration recorded. Furthermore, only in the latter two taxa does the bony tongue structure include elongation of paired hyobranchial elements that have been associated in functional studies with hyolingual mobility. Pterosaurs and enantiornithine birds achieve similar elongation and inferred mobility via elongation of ceratobranchial elements while within ornithurine birds, including living Aves, ossified and separate paired epibranchial elements (caudal to the ceratobranchials) confer an increase in hyobranchial length. The mobile tongues seen in living birds may be present in other flighted archosaurs showing a similar elongation. Shifts from hypercarnivory to more diverse feeding ecologies and diets, with the evolution of novel locomotor strategies like flight, may explain the evolution of more complex tongue function.

Funding: The work was supported by the Strategic Priority Research Program of Chinese Academy of Sciences (Grant No. XDB26000000) and the Hundred Talents Program (KC 217113) from Chinese Academy of Sciences (ZL). This work was also supported by Craton destruction and terrestrial life evolution CNSF 41688103 (ZZ), the University of Texas at Austin (ZL and JAC), a Predoctoral Fellowship (ZL) from the Smithsonian Institution, and the Gordon and Betty Moore Foundation Grant No. 4498 (JAC).

Copyright: © 2018 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

The tongue of terrestrial vertebrates differs markedly related to divergence in feeding and respiratory strategies [1, 2]. Within extant Archosauria, birds display diverse tongue morphologies associated with radiation in feeding ecologies [1]. In Aves, extensive ossification of tongue elements occurs not only in the elongated paired ceratobranchials and epibranchials [3, 4], but in midline elements (i.e., paraglossal, basihyal, and urohyal) as well (Fig 1). Direct support of the muscular tongue by these bony components is linked to the origin of novel muscles allowing coordination of hyoid and jaw movements during feeding that may also be deployed during panting and vocalization [5, 6]. Rhythmic hyolingual movement coupled with cranial kinesis is critical in avian feeding, especially for a few neognath birds (e.g., Psittaciformes and Anatidae), which are characterized by extensive intra-oral processing of food [3, 7, 8–10]. Extreme morphologies are seen associated with tongue protrusion, involving hyper-elongate paired hyobranchial elements in woodpeckers, hummingbirds, and honeyeaters [2, 11–13].

Muscles are shown in color, while bone/cartilage elements are shown in grey, the airway in birds in white, and fleshy tongue body in pink. Increased mineralization or ossification of hyobranchial elements occurs in ceratobranchial I in Archosauria [1]. Ancestrally within land dwelling vertebrates, the pectoral girdle is the major anchor of the caudal hypobranchial muscles, which function in depressing the hyoid during respiration (insets on left) [49]. Homologous to the episternohyoid complex (ephc) in crocodilians, they are either lost or highly reduced in living birds [37], [50–51]; diminutive tracheal muscles such as M. sternotrachealis and M. tracheolateralis are proposed to be their homologs [51]. These two thin muscles arise from the caudal surface of the craniolateral process on the sternum and syrinx, and insert on the lateral surface of the tracheal wall just cranial to the syrinx and the lateral tracheal wall to the laryngeal cartilages, respectively (left inset, S2 Table; Fig 11). The hypobranchial muscles (mge, mhy, and ephc; dark turquoise) in most non-avian reptiles play an important role in hyoid protraction, retraction, stabilization, and suspension during respiration and feeding [22]. These functions are accomplished by distinct muscles in birds, including M. branchiomandibularis (green), M. stylohyoideus, and M. serpihyoideus (mbm and msh, red color) and associated connective tissues, i.e., hyoid sheath or fasciae [5]. The two antagonistic muscles (mbm and msh) link the hyoid with the lower jaw and facilitate protraction and retraction of the tongue [3]. This major reorganization of hyobranchial muscles is also referred to as hyolingual suspension, which is absent in non-avian reptiles (e.g., Sphenodon) [33]. Muscles involved in tongue protrusion are labeled with asterisk. They are also the muscle built in the buccal floor (labeled as pound) in reptiles but lost or reduced in birds. Coordination of the hyoid with the jaw movements during cyclic feeding motions is inferred to be a derived avian feature [3]. Abbreviations: bh, basihyal; ephc, episterno-hyoid complex; mge, M. genioglossus; mhys, M. hyoglossus cranialis and oblique; mbm, M. branchiomandibularis; mca, M. cricoarytenoid; mch, M. cricohyoideus; mhp, M. hypoglossus; msh, M. stylohyoideus and M. serpihyoideus. See Table 1 for specimen information and the tree was adopted from ref. [1]

In contrast to the diverse tongue morphologies of living birds, their extant sister taxon, Crocodylia, and all extinct basal archosaurs so far studied [14], consistently show a relatively simple hyoid structure [15–17]. Even though a tremendous radiation of Mesozoic Crocodylomorpha (including sphenosuchians) has been reported, their preserved hyoid bones are restricted to a single pair of rod-like ceratobranchials [14]. Megaphagy or hypercarnivory has been proposed as a major cause for the lack of tongue involvement in food acquisition in crocodilians and their extinct relatives [18]. Their broad and fleshy tongue is firmly attached to the buccal floor by muscles and connective tissues. Ossified and cartilaginous elements are small compared to the size of this fleshy tongue. The absence of direct and cranially-extensive support from bony elements make crocodilian tongue incapable of significant independent motion [18]. Relative to outgroup lepidosaurs and other tetrapods the bony structure in crocodilians and surveyed basal archosaurs is uniformly simple and small with a single pair of ceratobranchials and no well-mineralized midline element or fusion [19–22].

While some bony elements of the tongue, or hyoid bones, commonly enter the fossil record [14–18], their shape, and the relationship between muscular and bony components has not been systematically assessed in bird-line archosaurs. Here, we used dissection and diffusible iodine contrast-enhanced computed tomography (diceCT) [23–26] to assess the relationship between bony and muscular features of the tongue in living archosaurs ([18, 27]; Methods). More than 330 fossil specimens, ranging from Triassic stem archosaurs to Jurassic and Cretaceous non-avian dinosaurs and pterosaurs (S1 Table) were examined.

We detailed hyolingual muscles from exemplars of birds from Neognathae and Palaeognathae, and used these with comparison of outgroup taxa to inform estimation [28] of ancestral hyolingual features of Aves (Methods; supporting material). Identification of key soft-tissue correlates required comparison of avian hyoid features with those of outgroup reptiles. The anatomy and function of the tongue in extant crocodilians and inferred implications for basal archosaurs has already been recently treated [18]. Outgroup comparison was used to determine the ancestral hyoid condition for archosaurs and assess derived hyolingual features of birds [18, 28]. This work underpins and constrains the inference of shifts in tongue function in Archosauria and provide key insight into the possible co-evolution of tongue morphology and feeding ecology (Figs 1–7; Methods) [18, 23, 29, 30].