Looking back over the shoulder: New insights on the unique scapular anatomy of the tapir (Perissodactyla: Tapiridae).

The musculoskeletal anatomy of the shoulder of many ungulates has been inferred from veterinary model taxa, with uniformity in muscle arrangements and attachment sites often assumed. In this study, I investigated the muscular and osteological anatomy of tapirs and their relatives (Perissodactyla: Tapiroidea), using a combination of gross dissection and digital imaging (photography and laser surface scanning). Dissections of three modern tapir species revealed that the m. infraspinatus originates from both supraspinous and infraspinous fossae for all species, lying on both sides of the distal scapular spine. The epimysial border between the m. supraspinatus and m. infraspinatus origin sites are marked in all species by an ossified ridge, sometimes extending the length of the scapular spine. This "supraspinous ridge" is clearly visible on the scapular surface of both modern and extinct Tapirus scapulae; however, the ridge does not appear present in any non-Tapirus tapiroids examined (e.g., Helaletes, Nexuotapirus), nor in other perissodactyls or artiodactyls. Moreover, the ridge exhibits a clearly distinct morphology in Tapirus indicus compared to all other Tapirus species examined. Combined, these findings indicate that the presence and position of the "supraspinous ridge" may represent a robust phylogenetic character for reconstructing relationships within tapiroids. Unfortunately, any functional locomotor outcomes or benefits of the m. infraspinatus straddling the scapular spine remains elusive. This study represents a firm reminder for anatomists, veterinarians, and paleontologists to (where possible) look beyond veterinary model systems when inferring musculoskeletal form or function in non-model organisms.

Sagittal crest morphology decoupled from relative bite performance in Pleistocene tapirs (Perissodactyla: Tapiridae).

Bite force is often associated with specific morphological features, such as sagittal crests. The presence of a pronounced sagittal crest in some tapirs (Perissodactyla: Tapiridae) was recently shown to be negatively correlated with hard-object feeding, in contrast with similar cranial structures in carnivorans. The aim of this study was to investigate bite forces and sagittal crest heights across a wide range of modern and extinct tapirs and apply a comparative investigation to establish whether these features are correlated across a broad phylogenetic scope. We examined a sample of 71 specimens representing 15 tapir species (5 extant, 10 extinct) using the dry-skull method, linear measurements of cranial features, phylogenetic reconstruction, and comparative analyses. Tapirs were found to exhibit variation in bite force and sagittal crest height across their phylogeny and between different biogeographical realms, with high-crested morphologies occurring mostly in Neotropical species. The highest bite forces within tapirs appear to be driven by estimates for the masseter-pterygoid muscle complex, rather than predicted forces for the temporalis muscle. Our results demonstrate that relative sagittal crest height is poorly correlated with relative cranial bite force, suggesting high force application is not a driver for pronounced sagittal crests in this sample. The divergent biomechanical capabilities of different contemporaneous tapirids may have allowed multiple species to occupy overlapping territories and partition resources to avoid excess competition. Bite forces in tapirs peak in Pleistocene species, independent of body size, suggesting possible dietary shifts as a potential result of climatic changes during this epoch.

Ecological signal in the size and shape of marine amniote teeth.

Amniotes have been a major component of marine trophic chains from the beginning of the Triassic to present day, with hundreds of species. However, inferences of their (palaeo)ecology have mostly been qualitative, making it difficult to track how dietary niches have changed through time and across clades. Here, we tackle this issue by applying a novel geometric morphometric protocol to three-dimensional models of tooth crowns across a wide range of raptorial marine amniotes. Our results highlight the phenomenon of dental simplification and widespread convergence in marine amniotes, limiting the range of tooth crown morphologies. Importantly, we quantitatively demonstrate that tooth crown shape and size are strongly associated with diet, whereas crown surface complexity is not. The maximal range of tooth shapes in both mammals and reptiles is seen in medium-sized taxa; large crowns are simple and restricted to a fraction of the morphospace. We recognize four principal raptorial guilds within toothed marine amniotes (durophages, generalists, flesh cutters and flesh piercers). Moreover, even though all these feeding guilds have been convergently colonized over the last 200 Myr, a series of dental morphologies are unique to the Mesozoic period, probably reflecting a distinct ecosystem structure.

Global ecomorphological restructuring of dominant marine reptiles prior to the Cretaceous-Palaeogene mass extinction.

Mosasaurid squamates were the dominant amniote predators in marine ecosystems during most of the Late Cretaceous. Here, we use a suite of biomechanically rooted, functionally descriptive ratios in a framework adapted from population ecology to investigate how the morphofunctional disparity of mosasaurids evolved prior to the Cretaceous-Palaeogene (K/Pg) mass extinction. Our results suggest that taxonomic turnover in mosasaurid community composition from Campanian to Maastrichtian is reflected by a notable global increase in morphofunctional disparity, especially driving the North American record. Ecomorphospace occupation becomes polarized during the Late Maastrichtian, with morphofunctional disparity plateauing in the Southern Hemisphere and decreasing in the Northern Hemisphere. We show that these changes are not strongly associated with mosasaurid size, but rather with the functional capacities of their skulls. Our novel approach indicates that mosasaurid morphofunctional disparity was in decline in multiple provincial communities before the K/Pg mass extinction, highlighting region-specific patterns of disparity evolution and the importance of assessing vertebrate extinctions both globally and locally. Ecomorphological differentiation in mosasaurid communities, coupled with declines in other formerly abundant marine reptile groups, indicates widespread restructuring of higher trophic levels in marine food webs was well underway when the K/Pg mass extinction took place.

Biogeography a key influence on distal forelimb variation in horses through the Cenozoic.

Locomotion in terrestrial tetrapods is reliant on interactions between distal limb bones (e.g. metapodials and phalanges). The metapodial-phalangeal joint in horse (Equidae) limbs is highly specialized, facilitating vital functions (shock absorption; elastic recoil). While joint shape has changed throughout horse evolution, potential drivers of these modifications have not been quantitatively assessed. Here, I examine the morphology of the forelimb metacarpophalangeal (MCP) joint of horses and their extinct kin (palaeotheres) using geometric morphometrics and disparity analyses, within a phylogenetic context. I also develop a novel alignment protocol that explores the magnitude of shape change through time, correlated against body mass and diet. MCP shape was poorly correlated with mass or diet proxies, although significant temporal correlations were detected at 0-1 Myr intervals. A clear division was recovered between New and Old World hipparionin MCP morphologies. Significant changes in MCP disparity and high rates of shape divergence were observed during the Great American Biotic Interchange, with the MCP joint becoming broad and robust in two separate monodactyl lineages, possibly exhibiting novel locomotor behaviour. This large-scale study of MCP joint shape demonstrates the apparent capacity for horses to rapidly change their distal limb morphology to overcome discrete locomotor challenges in new habitats.

The macroevolutionary landscape of short-necked plesiosaurians.

Throughout their evolution, tetrapods have repeatedly colonised a series of ecological niches in marine ecosystems, producing textbook examples of convergent evolution. However, this evolutionary phenomenon has typically been assessed qualitatively and in broad-brush frameworks that imply simplistic macroevolutionary landscapes. We establish a protocol to visualize the density of trait space occupancy and thoroughly test for the existence of macroevolutionary landscapes. We apply this protocol to a new phenotypic dataset describing the morphology of short-necked plesiosaurians, a major component of the Mesozoic marine food webs (ca. 201 to 66 Mya). Plesiosaurians evolved this body plan multiple times during their 135-million-year history, making them an ideal test case for the existence of macroevolutionary landscapes. We find ample evidence for a bimodal craniodental macroevolutionary landscape separating latirostrines from longirostrine taxa, providing the first phylogenetically-explicit quantitative assessment of trophic diversity in extinct marine reptiles. This bimodal pattern was established as early as the Middle Jurassic and was maintained in evolutionary patterns of short-necked plesiosaurians until a Late Cretaceous (Turonian) collapse to a unimodal landscape comprising longirostrine forms with novel morphologies. This study highlights the potential of severe environmental perturbations to profoundly alter the macroevolutionary dynamics of animals occupying the top of food chains.

Comparative forelimb myology and muscular architecture of a juvenile Malayan tapir (Tapirus indicus).

The absence of preserved soft tissues in the fossil record is frequently a hindrance for palaeontologists wishing to investigate morphological shifts in key skeletal systems, such as the limbs. Understanding the soft tissue composition of modern species can aid in understanding changes in musculoskeletal features through evolution, including those pertaining to locomotion. Establishing anatomical differences in soft tissues utilising an extant phylogenetic bracket can, in turn, assist in interpreting morphological changes in hard tissues and modelling musculoskeletal movements during evolutionary transitions (e.g. digit reduction in perissodactyls). Perissodactyls (horses, rhinoceroses, tapirs and their relatives) are known to have originated with a four-toed (tetradactyl) forelimb condition. Equids proceeded to reduce all but their central digit, resulting in monodactyly, whereas tapirs retained the ancestral tetradactyl state. The modern Malayan tapir (Tapirus indicus) has been shown to exhibit fully functional tetradactyly in its forelimb, more so than any other tapir, and represents an ideal case-study for muscular arrangement and architectural comparison with the highly derived monodactyl Equus. Here, we present the first quantification of muscular architecture of a tetradactyl perissodactyl (T. indicus), and compare it to measurements from modern monodactyl caballine horse (Equus ferus caballus). Each muscle of the tapir forelimb was dissected out from a cadaver and measured for architectural properties: muscle-tendon unit (MTU) length, MTU mass, muscle mass, pennation angle, and resting fibre length. Comparative parameters [physiological cross-sectional area (PCSA), muscle volume, and % muscle mass] were then calculated from the raw measurements. In the shoulder region, the infraspinatus of T. indicus exhibits dual origination sites on either side of the deflected scapular spine. Within ungulates, this condition has only been previously reported in suids. Differences in relative contribution to limb muscle mass between T. indicus and Equus highlight forelimb muscles that affect mobility in the lateral and medial digits (e.g. extensor digitorum lateralis). These muscles were likely reduced in equids during their evolutionary transition from tetradactyl forest-dwellers to monodactyl, open-habitat specialists. Patterns of PCSA across the forelimb were similar between T. indicus and Equus, with the notable exceptions of the biceps brachii and flexor carpi ulnaris, which were much larger in Equus. The differences observed in PCSA between the tapir and horse forelimb muscles highlight muscles that are essential for maintaining stability in the monodactyl limb while moving at high speeds. This quantitative dataset of muscle architecture in a functionally tetradactyl perissodactyl is a pivotal first step towards reconstructing the locomotor capabilities of extinct, four-toed ancestors of modern perissodactyls, and providing further insights into the equid locomotor transition.

Interspecific variation in the tetradactyl manus of modern tapirs (Perissodactyla: Tapirus) exposed using geometric morphometrics.

The distal forelimb (autopodium) of quadrupedal mammals is a key morphological unit involved in locomotion, body support, and interaction with the substrate. The manus of the tapir (Perissodactyla: Tapirus) is unique within modern perissodactyls, as it retains the plesiomorphic tetradactyl (four-toed) condition also exhibited by basal equids and rhinoceroses. Tapirs are known to exhibit anatomical mesaxonic symmetry in the manus, although interspecific differences and biomechanical mesaxony have yet to be rigorously tested. Here, we investigate variation in the manus morphology of four modern tapir species (Tapirus indicus, Tapirus bairdii, Tapirus pinchaque, and Tapirus terrestris) using a geometric morphometric approach. Autopodial bones were laser scanned to capture surface shape and morphology was quantified using 3D-landmark analysis. Landmarks were aligned using Generalised Procrustes Analysis, with discriminant function and partial least square analyses performed on aligned coordinate data to identify features that significantly separate tapir species. Overall, our results support the previously held hypothesis that T. indicus is morphologically separate from neotropical tapirs; however, previous conclusions regarding function from morphological differences are shown to require reassessment. We find evidence indicating that T. bairdii exhibits reduced reliance on the lateral fifth digit compared to other tapirs. Morphometric assessment of the metacarpophalangeal joint and the morphology of the distal facets of the lunate lend evidence toward high loading on the lateral digits of both the large T. indicus (large body mass) and the small, long limbed T. pinchaque (ground impact). Our results support other recent studies on T. pinchaque, suggesting subtle but important adaptations to a compliant but inclined habitat. In conclusion, we demonstrate further evidence that the modern tapir forelimb is a variable locomotor unit with a range of interspecific features tailored to habitual and biomechanical needs of each species.

Herbivorous dinosaur jaw disparity and its relationship to extrinsic evolutionary drivers.

Morphological responses of nonmammalian herbivores to external ecological drivers have not been quantified over extended timescales. Herbivorous nonavian dinosaurs are an ideal group to test for such responses, because they dominated terrestrial ecosystems for more than 155 Myr and included the largest herbivores that ever existed. The radiation of dinosaurs was punctuated by several ecologically important events, including extinctions at the Triassic/Jurassic (Tr/J) and Jurassic/Cretaceous (J/K) boundaries, the decline of cycadophytes, and the origin of angiosperms, all of which may have had profound consequences for herbivore communities. Here we present the first analysis of morphological and biomechanical disparity for sauropodomorph and ornithischian dinosaurs in order to investigate patterns of jaw shape and function through time. We find that morphological and biomechanical mandibular disparity are decoupled: mandibular shape disparity follows taxonomic diversity, with a steady increase through the Mesozoic. By contrast, biomechanical disparity builds to a peak in the Late Jurassic that corresponds to increased functional variation among sauropods. The reduction in biomechanical disparity following this peak coincides with the J/K extinction, the associated loss of sauropod and stegosaur diversity, and the decline of cycadophytes. We find no specific correspondence between biomechanical disparity and the proliferation of angiosperms. Continual ecological and functional replacement of pre-existing taxa accounts for disparity patterns through much of the Cretaceous, with the exception of several unique groups, such as psittacosaurids that are never replaced in their biomechanical or morphological profiles.

A three-dimensional morphometric analysis of upper forelimb morphology in the enigmatic tapir (Perissodactyla: Tapirus) hints at subtle variations in locomotor ecology.

Forelimb morphology is an indicator for terrestrial locomotor ecology. The limb morphology of the enigmatic tapir (Perissodactyla: Tapirus) has often been compared to that of basal perissodactyls, despite the lack of quantitative studies comparing forelimb variation in modern tapirs. Here, we present a quantitative assessment of tapir upper forelimb osteology using three-dimensional geometric morphometrics to test whether the four modern tapir species are monomorphic in their forelimb skeleton. The shape of the upper forelimb bones across four species (T. indicus; T. bairdii; T. terrestris; T. pinchaque) was investigated. Bones were laser scanned to capture surface morphology and 3D landmark analysis was used to quantify shape. Discriminant function analyses were performed to reveal features which could be used for interspecific discrimination. Overall our results show that the appendicular skeleton contains notable interspecific differences. We demonstrate that upper forelimb bones can be used to discriminate between species (>91% accuracy), with the scapula proving the most diagnostic bone (100% accuracy). Features that most successfully discriminate between the four species include the placement of the cranial angle of the scapula, depth of the humeral condyle, and the caudal deflection of the olecranon. Previous studies comparing the limbs of T. indicus and T. terrestris are corroborated by our quantitative findings. Moreover, the mountain tapir T. pinchaque consistently exhibited the greatest divergence in morphology from the other three species. Despite previous studies describing tapirs as functionally mediportal in their locomotor style, we find osteological evidence suggesting a spectrum of locomotor adaptations in the tapirs. We conclude that modern tapir forelimbs are neither monomorphic nor are tapirs as conserved in their locomotor habits as previously described. J. Morphol. 277:1469-1485, 2016. © 2016 Wiley Periodicals, Inc.