Head posture impacts mammalian hyoid position and suprahyoid muscle length: implication for swallowing biomechanics.

Instantaneous head posture (IHP) can extensively alter resting hyoid position in humans, yet postural effects on resting hyoid position remain poorly documented among mammals in general. Clarifying this relationship is essential for evaluating interspecific variation in hyoid posture across evolution, and understanding its implications for hyolingual soft tissue function and swallowing motor control. Using Didelphis virginiana as a model, we conducted static manipulation experiments to show that head flexion shifts hyoid position rostrally relative to the cranium across different gapes. IHP-induced shifts in hyoid position along the anteroposterior axis are comparable to in vivo hyoid protraction distance during swallowing. IHP also has opposite effects on passive genio- and stylohyoid muscle lengths. High-speed biplanar videoradiography suggests Didelphis consistently swallows at neutral to flexed posture, with stereotyped hyoid kinematics across different head postures. IHP change can affect suprahyoid muscle force production by shifting their positions on the length-tension curve, and redirecting lines of action and the resultant force from supra- and infrahyoid muscles. We hypothesize that demands on muscle performance may constrain the range of swallowing head postures in mammals. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Three-dimensional mandibular kinematics of mastication in the marsupial Didelphis virginiana.

Didelphis virginiana (the Virginia opossum) is often used as an extant model for understanding feeding behaviour in Mesozoic mammaliaforms, primarily due to their morphological similarities, including an unfused mandibular symphysis and tribosphenic molars. However, the three-dimensional jaw kinematics of opossum chewing have not yet been fully quantified. We used biplanar videofluoroscopy and the X-Ray Reconstruction of Moving Morphology workflow to quantify mandibular kinematics in four wild-caught opossums feeding on hard (almonds) and soft (cheese cubes) foods. These data were used to test hypotheses regarding the importance of roll versus yaw in chewing by early mammals, and the impact of food material properties (FMPs) on jaw kinematics. The magnitude of roll exceeds that of yaw, but both are necessary for tooth-tooth or tooth-food-tooth contact between complex occlusal surfaces. We confirmed the utility of the four vertical kinematic gape cycle phases identified in tetrapods but we further defined two more in order to capture non-vertical kinematics. Statistical tests support the separation of chew cycle phases into two functional groups: occlusal and non-occlusal phases. The separation of slow close into two (occlusal) phases gives quantitative kinematic support for the long-hypothesized multifunctionality of the tribosphenic molar. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Functional reorganisation of the cranial skeleton during the cynodont-mammaliaform transition.

Skeletal simplification occurred in multiple vertebrate clades over the last 500 million years, including the evolution from premammalian cynodonts to mammals. This transition is characterised by the loss and reduction of cranial bones, the emergence of a novel jaw joint, and the rearrangement of the jaw musculature. These modifications have long been hypothesised to increase skull strength and efficiency during feeding. Here, we combine digital reconstruction and biomechanical modelling to show that there is no evidence for an increase in cranial strength and biomechanical performance. Our analyses demonstrate the selective functional reorganisation of the cranial skeleton, leading to reduced stresses in the braincase and the skull roof but increased stresses in the zygomatic region through this transition. This cranial functional reorganisation, reduction in mechanical advantage, and overall miniaturisation in body size are linked with a dietary specialisation to insectivory, permitting the subsequent morphological and ecological diversification of the mammalian lineage.

The earliest segmental sternum in a Permian synapsid and its implications for the evolution of mammalian locomotion and ventilation.

The sternum is a stabilizing element in the axial skeleton of most tetrapods, closely linked with the function of the pectoral girdle of the appendicular skeleton. Modern mammals have a distinctive sternum characterized by multiple ossified segments, the origins of which are poorly understood. Although the evolution of the pectoral girdle has been extensively studied in early members of the mammalian total group (Synapsida), only limited data exist for the sternum. Ancestrally, synapsids exhibit a single sternal element and previously the earliest report of a segmental sternum in non-mammalian synapsids was in the Middle Triassic cynodont Diademodon tetragonus. Here, we describe the well-preserved sternum of a gorgonopsian, a group of sabre-toothed synapsids from the Permian. It represents an ossified, multipartite element resembling the mammalian condition. This discovery pulls back the origin of the distinctive "mammalian" sternum to the base of Theriodontia, significantly extending the temporal range of this morphology. Through a review of sternal morphology across Synapsida, we reconstruct the evolutionary history of this structure. Furthermore, we explore its role in the evolution of mammalian posture, gait, and ventilation through progressive regionalization of the postcranium as well as the posteriorization of musculature associated with mammalian breathing.

Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy.

Endothermy underpins the ecological dominance of mammals and birds in diverse environmental settings1,2. However, it is unclear when this crucial feature emerged during mammalian evolutionary history, as most of the fossil evidence is ambiguous3-17. Here we show that this key evolutionary transition can be investigated using the morphology of the endolymph-filled semicircular ducts of the inner ear, which monitor head rotations and are essential for motor coordination, navigation and spatial awareness18-22. Increased body temperatures during the ectotherm-endotherm transition of mammal ancestors would decrease endolymph viscosity, negatively affecting semicircular duct biomechanics23,24, while simultaneously increasing behavioural activity25,26 probably required improved performance27. Morphological changes to the membranous ducts and enclosing bony canals would have been necessary to maintain optimal functionality during this transition. To track these morphofunctional changes in 56 extinct synapsid species, we developed the thermo-motility index, a proxy based on bony canal morphology. The results suggest that endothermy evolved abruptly during the Late Triassic period in Mammaliamorpha, correlated with a sharp increase in body temperature (5-9 °C) and an expansion of aerobic and anaerobic capacities. Contrary to previous suggestions3-14, all stem mammaliamorphs were most probably ectotherms. Endothermy, as a crucial physiological characteristic, joins other distinctive mammalian features that arose during this period of climatic instability28.

Evolution of inner ear neuroanatomy of bats and implications for echolocation.

Phylogenomics of bats suggests that their echolocation either evolved separately in the bat suborders Yinpterochiroptera and Yangochiroptera, or had a single origin in bat ancestors and was later lost in some yinpterochiropterans1-6. Hearing for echolocation behaviour depends on the inner ear, of which the spiral ganglion is an essential structure. Here we report the observation of highly derived structures of the spiral ganglion in yangochiropteran bats: a trans-otic ganglion with a wall-less Rosenthal's canal. This neuroanatomical arrangement permits a larger ganglion with more neurons, higher innervation density of neurons and denser clustering of cochlear nerve fascicles7-13. This differs from the plesiomorphic neuroanatomy of Yinpterochiroptera and non-chiropteran mammals. The osteological correlates of these derived ganglion features can now be traced into bat phylogeny, providing direct evidence of how Yangochiroptera differentiated from Yinpterochiroptera in spiral ganglion neuroanatomy. These features are highly variable across major clades and between species of Yangochiroptera, and in morphospace, exhibit much greater disparity in Yangochiroptera than Yinpterochiroptera. These highly variable ganglion features may be a neuroanatomical evolutionary driver for their diverse echolocating strategies4,14-17 and are associated with the explosive diversification of yangochiropterans, which include most bat families, genera and species.

Morphological disparity and evolutionary transformations in the primate hyoid apparatus.

The hyoid apparatus plays an integral role in swallowing, respiration, and vocalization in mammals. Most placental mammals have a rod-shaped basihyal connected to the basicranium via both soft tissues and a mobile bony chain-the anterior cornu-whereas anthropoid primates have broad, shield-like or even cup-shaped basihyals suspended from the basicranium by soft tissues only. How the unique anthropoid hyoid morphology evolved is unknown, and hyoid morphology of nonanthropoid primates is poorly documented. Here we use phylogenetic comparative methods and linear morphometrics to address knowledge gaps in hyoid evolution among primates and their euarchontan outgroups. We find that dermopterans have variable reduction of cornu elements. Cynocephalus volans are sexually dimorphic in hyoid morphology. Tupaia and all lemuroids except Daubentonia have a fully ossified anterior cornu connecting a rod-shaped basihyal to the basicranium; this is the ancestral mammalian pattern that is also characteristic of the last common ancestor of Primates. Haplorhines exhibit a reduced anterior cornu, and anthropoids underwent further increase in basihyal aspect ratio values and in relative basihyal volume. Convergent with haplorhines, lorisoid strepsirrhines independently evolved a broad basihyal and reduced anterior cornua. While a reduced anterior cornu is hypothesized to facilitate vocal tract lengthening and lower formant frequencies in some mammals, our results suggest vocalization adaptations alone are unlikely to drive the iterative reduction of anterior cornua within Primates. Our new data on euarchontan hyoid evolution provide an anatomical basis for further exploring the form-function relationships of the hyoid across different behaviors, including vocalization, chewing, and swallowing.

Incomplete convergence of gliding mammal skeletons.

Ecology and biomechanics play central roles in the generation of phenotypic diversity. When unrelated taxa invade a similar ecological niche, biomechanical demands can drive convergent morphological transformations. Thus, examining convergence helps to elucidate the key catalysts of phenotypic change. Gliding mammals are often presented as a classic case of convergent evolution because they independently evolved in numerous clades, each possessing patagia ("wing" membranes) that generate lift during gliding. We use phylogenetic comparative methods to test whether the skeletal morphologies of the six clades of extant gliding mammals demonstrate convergence. Our results indicate that glider skeletons are convergent, with glider groups consistently evolving proportionally longer, more gracile limbs than arborealists, likely to increase patagial surface area. Nonetheless, we interpret gliders to represent incomplete convergence because (1) evolutionary model-fitting analyses do not indicate strong selective pressures for glider trait optima, (2) the three marsupial glider groups diverge rather than converge, and (3) the gliding groups remain separated in morphospace (rather than converging on a single morphotype), which is reflected by an unexpectedly high level of morphological disparity. That glider skeletons are morphologically diverse is further demonstrated by fossil gliders from the Mesozoic Era, which possess unique skeletal characteristics that are absent in extant gliders. Glider morphologies may be strongly influenced by factors such as body size and attachment location of patagia on the forelimb, which can vary among clades. Thus, convergence in gliders appears to be driven by a simple lengthening of the limbs, whereas additional skeletal traits reflect nuances of the gliding apparatus that are distinct among different evolutionary lineages. Our unexpected results add to growing evidence that incomplete convergence is prevalent in vertebrate clades, even among classic cases of convergence, and they highlight the importance of examining form-function relationships in light of phylogeny, biomechanics, and the fossil record.

New Jurassic mammaliaform sheds light on early evolution of mammal-like hyoid bones.

We report a new Jurassic docodontan mammaliaform found in China that is preserved with the hyoid bones. Its basihyal, ceratohyal, epihyal, and thyrohyal bones have mobile joints and are arranged in a saddle-shaped configuration, as in the mobile linkage of the hyoid apparatus of extant mammals. These are fundamentally different from the simple hyoid rods of nonmammaliaform cynodonts, which were likely associated with a wide, nonmuscularized throat, as seen in extant reptiles. The hyoid apparatus provides a framework for the larynx and for the constricted, muscularized esophagus, crucial for transport and powered swallowing of the masticated food and liquid in extant mammals. These derived structural components of hyoids evolved among early diverging mammaliaforms, before the disconnection of the middle ear from the mandible in crown mammals.

The role of miniaturization in the evolution of the mammalian jaw and middle ear.

The evolution of the mammalian jaw is one of the most important innovations in vertebrate history, and underpins the exceptional radiation and diversification of mammals over the last 220 million years1,2. In particular, the transformation of the mandible into a single tooth-bearing bone and the emergence of a novel jaw joint-while incorporating some of the ancestral jaw bones into the mammalian middle ear-is often cited as a classic example of the repurposing of morphological structures3,4. Although it is remarkably well-documented in the fossil record, the evolution of the mammalian jaw still poses the paradox of how the bones of the ancestral jaw joint could function both as a joint hinge for powerful load-bearing mastication and as a mandibular middle ear that was delicate enough for hearing. Here we use digital reconstructions, computational modelling and biomechanical analyses to demonstrate that the miniaturization of the early mammalian jaw was the primary driver for the transformation of the jaw joint. We show that there is no evidence for a concurrent reduction in jaw-joint stress and increase in bite force in key non-mammaliaform taxa in the cynodont-mammaliaform transition, as previously thought5-8. Although a shift in the recruitment of the jaw musculature occurred during the evolution of modern mammals, the optimization of mandibular function to increase bite force while reducing joint loads did not occur until after the emergence of the neomorphic mammalian jaw joint. This suggests that miniaturization provided a selective regime for the evolution of the mammalian jaw joint, followed by the integration of the postdentary bones into the mammalian middle ear.

Publisher Correction: Late-surviving stem mammal links the lowermost Cretaceous of North America and Gondwana.

The asterisked footnote to Extended Data Table 1 should state '*Including Thomasia and Haramiyavia'. This has been corrected online.

Late-surviving stem mammal links the lowermost Cretaceous of North America and Gondwana.

Haramiyida was a successful clade of mammaliaforms, spanning the Late Triassic period to at least the Late Jurassic period, but their fossils are scant outside Eurasia and Cretaceous records are controversial1-4. Here we report, to our knowledge, the first cranium of a large haramiyidan from the basal Cretaceous of North America. This cranium possesses an amalgam of stem mammaliaform plesiomorphies and crown mammalian apomorphies. Moreover, it shows dental traits that are diagnostic of isolated teeth of supposed multituberculate affinities from the Cretaceous of Morocco, which have been assigned to the enigmatic 'Hahnodontidae'. Exceptional preservation of this specimen also provides insights into the evolution of the ancestral mammalian brain. We demonstrate the haramiyidan affinities of Gondwanan hahnodontid teeth, removing them from multituberculates, and suggest that hahnodontid mammaliaforms had a much wider, possibly Pangaean distribution during the Jurassic-Cretaceous transition.

New gliding mammaliaforms from the Jurassic.

Stem mammaliaforms are Mesozoic forerunners to mammals, and they offer critical evidence for the anatomical evolution and ecological diversification during the earliest mammalian history. Two new eleutherodonts from the Late Jurassic period have skin membranes and skeletal features that are adapted for gliding. Characteristics of their digits provide evidence of roosting behaviour, as in dermopterans and bats, and their feet have a calcaneal calcar to support the uropagatium as in bats. The new volant taxa are phylogenetically nested with arboreal eleutherodonts. Together, they show an evolutionary experimentation similar to the iterative evolutions of gliders within arboreal groups of marsupial and placental mammals. However, gliding eleutherodonts possess rigid interclavicle-clavicle structures, convergent to the avian furculum, and they retain shoulder girdle plesiomorphies of mammaliaforms and monotremes. Forelimb mobility required by gliding occurs at the acromion-clavicle and glenohumeral joints, is different from and convergent to the shoulder mobility at the pivotal clavicle-sternal joint in marsupial and placental gliders.

New evidence for mammaliaform ear evolution and feeding adaptation in a Jurassic ecosystem.

Stem mammaliaforms are forerunners to modern mammals, and they achieved considerable ecomorphological diversity in their own right. Recent discoveries suggest that eleutherodontids, a subclade of Haramiyida, were more species-rich during the Jurassic period in Asia than previously recognized. Here we report a new Jurassic eleutherodontid mammaliaform with an unusual mosaic of highly specialized characteristics, and the results of phylogenetic analyses that support the hypothesis that haramiyidans are stem mammaliaforms. The new fossil shows fossilized skin membranes that are interpreted to be for gliding and a mandibular middle ear with a unique character combination previously unknown in mammaliaforms. Incisor replacement is prolonged until well after molars are fully erupted, a timing pattern unique to most other mammaliaforms. In situ molar occlusion and a functional analysis reveal a new mode of dental occlusion: dual mortar-pestle occlusion of opposing upper and lower molars, probably for dual crushing and grinding. This suggests that eleutherodontids are herbivorous, and probably specialized for granivory or feeding on soft plant tissues. The inferred dietary adaptation of eleutherodontid gliders represents a remarkable evolutionary convergence with herbivorous gliders in Theria. These Jurassic fossils represent volant, herbivorous stem mammaliaforms associated with pre-angiosperm plants that appear long before the later, iterative associations between angiosperm plants and volant herbivores in various therian clades.

Meckel's cartilage breakdown offers clues to mammalian middle ear evolution.

A key transformation in mammalian ear evolution was incorporation of the primary jaw joint of premammalian synapsids into the definitive mammalian middle ear of living mammals. This evolutionary transition occurred in two-steps, starting with a partial or "transitional" mammalian middle ear in which the ectotympanic and malleus were still connected to the mandible by an ossified Meckel's Cartilage (MC), as observed in many Mesozoic mammals. This was followed by MC breakdown, freeing the ectotympanic and the malleus from the mandible and creating the definitive mammalian middle ear. Here we report novel findings on the role of chondroclasts in MC breakdown, shedding light on how therian mammals lost MC connecting the ear to the jaw. Genetic or pharmacological loss of clast cells in mice and opossums leads to persistence of embryonic MC beyond juvenile stages, with MC ossification in mutant mice. The persistent MC causes a distinctive postnatal groove on the mouse dentary. This morphology phenocopies the ossified MC and Meckelian groove observed in Mesozoic mammals. Clast cell recruitment to MC is not observed in reptiles, where MC persists as a cartilaginous structure. We hypothesize that ossification of MC is an ancestral feature of mammaliaforms, and that a shift in the timing of clast cell recruitment to MC prior to its ossification is a key developmental mechanism for the evolution of the definitive mammalian middle ear in extant therians.

A new developmental mechanism for the separation of the mammalian middle ear ossicles from the jaw.

Multiple mammalian lineages independently evolved a definitive mammalian middle ear (DMME) through breakdown of Meckel's cartilage (MC). However, the cellular and molecular drivers of this evolutionary transition remain unknown for most mammal groups. Here, we identify such drivers in the living marsupial opossum Monodelphis domestica, whose MC transformation during development anatomically mirrors the evolutionary transformation observed in fossils. Specifically, we link increases in cellular apoptosis and TGF-BR2 signalling to MC breakdown in opossums. We demonstrate that a simple change in TGF-ß signalling is sufficient to inhibit MC breakdown during opossum development, indicating that changes in TGF-ß signalling might be key during mammalian evolution. Furthermore, the apoptosis that we observe during opossum MC breakdown does not seemingly occur in mouse, consistent with homoplastic DMME evolution in the marsupial and placental lineages.

Morphological evolution of the mammalian jaw adductor complex.

The evolution of the mammalian jaw during the transition from non-mammalian synapsids to crown mammals is a key event in vertebrate history and characterised by the gradual reduction of its individual bones into a single element and the concomitant transformation of the jaw joint and its incorporation into the middle ear complex. This osteological transformation is accompanied by a rearrangement and modification of the jaw adductor musculature, which is thought to have allowed the evolution of a more-efficient masticatory system in comparison to the plesiomorphic synapsid condition. While osteological characters relating to this transition are well documented in the fossil record, the exact arrangement and modifications of the individual adductor muscles during the cynodont-mammaliaform transition have been debated for nearly a century. We review the existing knowledge about the musculoskeletal evolution of the mammalian jaw adductor complex and evaluate previous hypotheses in the light of recently documented fossils that represent new specimens of existing species, which are of central importance to the mammalian origins debate. By employing computed tomography (CT) and digital reconstruction techniques to create three-dimensional models of the jaw adductor musculature in a number of representative non-mammalian cynodonts and mammaliaforms, we provide an updated perspective on mammalian jaw muscle evolution. As an emerging consensus, current evidence suggests that the mammal-like division of the jaw adductor musculature (into deep and superficial components of the m. masseter, the m. temporalis and the m. pterygoideus) was completed in Eucynodontia. The arrangement of the jaw adductor musculature in a mammalian fashion, with the m. pterygoideus group inserting on the dentary was completed in basal Mammaliaformes as suggested by the muscle reconstruction of Morganucodon oehleri. Consequently, transformation of the jaw adductor musculature from the ancestral ('reptilian') to the mammalian condition must have preceded the emergence of Mammalia and the full formation of the mammalian jaw joint. This suggests that the modification of the jaw adductor system played a pivotal role in the functional morphology and biomechanical stability of the jaw joint.

Inner ear labyrinth anatomy of monotremes and implications for mammalian inner ear evolution.

The monophyletic clade Monotremata branches early from the rest of the mammalian crown group in the Jurassic and members of this clade retain many ancestral mammalian traits. Thus, accurate and detailed anatomical descriptions of this group can offer unique insight into the early evolutionary history of Mammalia. In this study, we examine the inner ear anatomy of two extant monotremes, Ornithorhynchus anatinus and Tachyglossus aculeatus, with the primary goals of elucidating the ancestral mammalian ear morphology and resolving inconsistencies found within previous descriptive literature. We use histological serial sections and high-resolution microcomputed tomography (µCT) for correlating soft tissue features of the vestibule and cochlea to the osseous labyrinth endocast. We found that in both monotremes the scala tympani coils to a lesser degree than scala vestibuli and scala media, although all three scalae show an apical coil inside the osseous cochlear tube. The helicotrema (conduit between scala tympani and scala vestibuli) is in subapical position, and the cochlear and lagenar ganglia and their associated nerve fibers are not enclosed by bone. In comparison, in extant therian mammals (i.e., marsupials and placentals) the helicotrema is located at the apex of the osseous cochlear canal, the three scalae coil to the same degree and the cochlear ganglion is enclosed by the primary bony lamina. Whether the lagenar ganglion is lost in therian mammals or integrated into the cochlear ganglion is still debated. The presence of a sensory lagenar macula at the apex of the membranous cochlear duct, innervated by a separate lagenar nerve and ganglion is a plesiomorphic condition of amniotes that monotremes share. A separate osseous lagenar canaliculus for the lagenar nerve, and the coiling of the distended lagenar sac at the end of the cochlear duct are autapomorphies of monotremes. Based on our findings we hypothesize that the ancestral inner ear of stem mammaliaforms is characterized by a straight or slightly curved osseous cochlear canal, a lagenar macula, lagenar nerve fibers separated from a larger bundle of cochlear nerve fibers, the presence of an organ of Corti and an intra-otic cochlear ganglion suspended by membranous connective tissue. Among the major Mesozoic clades of crown mammals, cladotherians and gondwanatherians most likely acquired a fully functioning organ of Corti but lost the sensory lagenar macula, like extant therians. However, Mesozoic spalacotherioids, multituberculates and eutriconodonts likely retained the mammaliaform condition. J. Morphol. 278:236-263, 2017. © 2016 Wiley Periodicals,Inc.

X-ray computed tomography datasets for forensic analysis of vertebrate fossils.

We describe X-ray computed tomography (CT) datasets from three specimens recovered from Early Cretaceous lakebeds of China that illustrate the forensic interpretation of CT imagery for paleontology. Fossil vertebrates from thinly bedded sediments often shatter upon discovery and are commonly repaired as amalgamated mosaics grouted to a solid backing slab of rock or plaster. Such methods are prone to inadvertent error and willful forgery, and once required potentially destructive methods to identify mistakes in reconstruction. CT is an efficient, nondestructive alternative that can disclose many clues about how a specimen was handled and repaired. These annotated datasets illustrate the power of CT in documenting specimen integrity and are intended as a reference in applying CT more broadly to evaluating the authenticity of comparable fossils.