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Crompton, Alfred

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Crompton

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Crompton, Alfred
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    Rolling of the jaw is essential for mammalian chewing and tribosphenic molar function
    (Springer Science and Business Media LLC, 2019-02) Bhullar, Bhart-Anjan S.; Manafzadeh, Armita R.; Miyamae, Juri A.; Hoffman, Eva A.; Brainerd, Elizabeth L.; Musinsky, Catherine; Crompton, Alfred
    Over the past two centuries, mammalian chewing and related anatomical features have been among the most discussed of all vertebrate evolutionary innovations. Chief among these features are two characters: the dentary-only mandible, and the tribosphenic molar with its triangulated upper cusps and lower talonid basin. The flexible mandibular joint and the unfused symphysis of ancestral mammals-in combination with transformations of the adductor musculature and palate-are thought to have permitted greater mobility of each lower jaw, or hemimandible. Following the appearance of precise dental occlusion near the origin of the mammalian crown, therians evolved a tribosphenic molar with a craggy topography that is presumed to have been used to catch, cut and crush food. Here we describe the ancestral tribosphenic therian chewing stroke, as conserved in the short-tailed opossum Monodelphis domestica: it is a simple symmetrical sequence of lower tooth-row eversion and inversion during jaw opening and closing, respectively, enacted by hemimandibular long-axis rotation. This sequence is coupled with an eversion-inversion rotational grinding stroke. We infer that the ancestral therian chewing stroke relied heavily on long-axis rotation, including symmetrical eversion and inversion (inherited from the first mammaliaforms) as well as a mortar-and-pestle rotational grinding stroke that was inherited from stem therians along with the tribosphenic molar. The yaw-dominated masticatory cycle of primates, ungulates and other bunodont therians is derived; it is necessitated by a secondarily fused jaw symphysis, and permitted by the reduction of high, interlocking cusps. The development of an efficient masticatory system-culminating in the tribosphenic apparatus-allowed early mammals to begin the process of digestion by shearing and crushing food into small boli instead of swallowing larger pieces in the reptilian manner, which necessitates a long, slow and wholly chemical breakdown. The vast diversity of mammalian teeth has emerged from the basic tribosphenic groundplan.
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    Evolution of the mammalian fauces region and the origin of suckling
    (2018) Crompton, Alfred; Musinsky, Catherine; Bonaparte, Jose; Bhullar, Bhart-Anjan; Owerkowicz, Tomasz
    Therian suckling requires the presence of two oral seals: an anterior one formed by the tongue partially surrounding the teat and pressing it against the palate, thereby closing the gap between the exterior and oral cavity; and a posterior seal between the back of the tongue and the part of the soft palate that stretches between the ventral edges of the pterygoid hamuli. This posterior seal closes the fauces, viz. the passage between the oral cavity and oropharynx. While the anterior seal is formed by the tongue alone, the posterior seal requires synchronous activity in the tensor veli palatini, which stiffens the soft palate, along with the palatoglossus, mylohyoideus and intrinsic tongue muscles, all of which elevate the tongue against the soft palate. At the beginning of a suckling cycle both seals are intact. The surface of the tongue between the two seals lowers, causing negative pressure which draws milk into the oral cavity from the teat. Subsequently when the posterior seal relaxes, milk flows from the oral cavity through the fauces into the oropharynx. In therian mammals, the pterygoid bone’s hamuli and the tensors veli palatini they support play an important role in the transfer of liquids, whether acquired by sucking or lapping, from the oral cavity to the oropharynx. The first appearance of these structures in mammalian ancestors provides a clue as to when both suckling and the therian mechanism for food transport through the oral cavity first arose. To trace the origin of these features, we studied serial sections of a pouch young marsupial and CT scans of non-mammalian cynodonts, ictidosaurs, mammaliaforms. We conclude that the hamulus arose from the pterygopalatine bosses, and the tensor veli palatini from a medial slip of the reptilian posterior pterygoideus that shifted its origin from the posterior border of the pterygoid onto the lateral surface of the pterygopalatine bosses. We suggest that stress and strain on the on the precursor cells of pterygopalatine bosses by the tensor veli palatini led to the formation of secondary cartilage that ossified and fused with the bosses to form the pterygoid hamuli. The mammalian medial pterygoid arose from the lateral part of the posterior pterygoideus when its origin shifted from the transverse process of the pterygoid to the palatine and pterygoid hamulus. The mammalian lateral pterygoid arose from the reptilian pseudotemporalis. Monotreme ancestors either lost the tensor veli palatini, palatoglossus and pterygoid hamuli or never developed them. Extant monotreme hatchlings have tongues with a structure and function unique among mammals, and use a mechanism other than suckling to ingest maternal milk. Their fauces region was modified to break down invertebrates between keratinized pads on the posterior tongue and on the ventral surface of a long palatine.
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    Muscle Logic: New Knowledge Resource for Anatomy Enables Comprehensive Searches of the Literature on the Feeding Muscles of Mammals
    (Public Library of Science, 2016) Druzinsky, Robert E.; Balhoff, James P.; Crompton, Alfred; Done, James; German, Rebecca Z.; Haendel, Melissa A.; Herrel, Anthony; Herring, Susan W.; Lapp, Hilmar; Mabee, Paula M.; Muller, Hans-Michael; Mungall, Christopher J.; Sternberg, Paul W.; Van Auken, Kimberly; Vinyard, Christopher J.; Williams, Susan H.; Wall, Christine E.
    Background: In recent years large bibliographic databases have made much of the published literature of biology available for searches. However, the capabilities of the search engines integrated into these databases for text-based bibliographic searches are limited. To enable searches that deliver the results expected by comparative anatomists, an underlying logical structure known as an ontology is required. Development and Testing of the Ontology Here we present the Mammalian Feeding Muscle Ontology (MFMO), a multi-species ontology focused on anatomical structures that participate in feeding and other oral/pharyngeal behaviors. A unique feature of the MFMO is that a simple, computable, definition of each muscle, which includes its attachments and innervation, is true across mammals. This construction mirrors the logical foundation of comparative anatomy and permits searches using language familiar to biologists. Further, it provides a template for muscles that will be useful in extending any anatomy ontology. The MFMO is developed to support the Feeding Experiments End-User Database Project (FEED, https://feedexp.org/), a publicly-available, online repository for physiological data collected from in vivo studies of feeding (e.g., mastication, biting, swallowing) in mammals. Currently the MFMO is integrated into FEED and also into two literature-specific implementations of Textpresso, a text-mining system that facilitates powerful searches of a corpus of scientific publications. We evaluate the MFMO by asking questions that test the ability of the ontology to return appropriate answers (competency questions). We compare the results of queries of the MFMO to results from similar searches in PubMed and Google Scholar. Results and Significance Our tests demonstrate that the MFMO is competent to answer queries formed in the common language of comparative anatomy, but PubMed and Google Scholar are not. Overall, our results show that by incorporating anatomical ontologies into searches, an expanded and anatomically comprehensive set of results can be obtained. The broader scientific and publishing communities should consider taking up the challenge of semantically enabled search capabilities.
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    Control of Jaw Movements in Two Species of Macropodines (Macropus eugenii and Macropus rufus)
    (Elsevier, 2007) Crompton, Alfred; Barnet, J.; Lieberman, Daniel; Owerkowicz, T.; Skinner, J.; Baudinette, R. V.
    The masticatory motor patterns of three tammar wallabies and two red kangaroos were determined by analyzing the pattern of electromyographic (EMG) activity of the jaw adductors and correlating it with lower jaw movements, as recorded by digital video and videoradiography. Transverse jaw movements were limited by the width of the upper incisal arcade. Molars engaged in food breakdown during two distinct occlusal phases characterized by abrupt changes in the direction of working-side hemimandible movement. Separate orthal (Phase I) and transverse (Phase II) trajectories were observed. The working-side lower jaw initially was drawn laterally by the balancing-side medial pterygoid and then orthally by overlapping activity in the balancing- and working-side temporalis and the balancing-side superficial masseter and medial pterygoid. Transverse movement occurred principally via the working-side medial pterygoid and superficial masseter. This pattern contrasted to that of placental herbivores, which are known to break down food when they move the working-side lower jaw transversely along a relatively longer linear path without changing direction during the power stroke. The placental trajectory results from overlapping activity in the working- and balancing-side adductor muscles, suggesting that macropods and placental herbivores have modified the primitive masticatory motor pattern in different ways.
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    Masticatory Motor Patterns in Six Herbivorous Australian Marsupials
    (John Wiley & Sons, 2007) Crompton, Alfred; Lieberman, Daniel; Owerkovicz, Tomasz; Skinner, John
    Electomyograms of the adductor muscles of the hairy-nosed wombat (Lasiorhinus latifrons), red kangaroo (Macropus rufus), Tammar wallaby (M. eugenii), koala (Phascolarctos cinereus), potoroo (Potorous tridactylus) and the brush-tailed possum (Trichosurus vulpecula) were analyzed and compared with those of placental herbivores. Marsupials have developed several different and distinct masticatory motor patterns that are all fundamentally different from those of placental herbivores where jaw movements are controlled by a relatively conservative pattern of working and balancing side muscle pairs (Triplet I and II or Diagonals I and II). For example, in the three species of macropods, all regions of the balancing and working side temporalis are active synchronously and the power stroke is divided into two distinct shearing and grinding phases. In addition, force generated by the balancing side muscles exceeds that of the working and is transferred to the working side via a slender mobile unfused mandibular symphysis. In wombats only the working side adductors are active during the power stroke. Koalas have lost the ubiquitous inflected mandibular angle of marsupials and their motor pattern is convergent on that of placental herbivores. In ring-tailed possums the pattern is transitional between the ‘‘primitive pattern’’ of placentals and that of macropods. This greater variety of motor patterns reflects the independent acquisition of mammalian herbivory in Australasia when the continent was isolated during much of the Tertiary.
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    Structure of the nasal region of non-mammalian cynodonts and mammaliaforms: Speculations on the evolution of mammalian endothermy
    (Informa UK Limited, 2017-01-02) Crompton, Alfred; Owerkowicz, T.; Bhullar, B.-A. S.; Musinsky, Catherine
    Nasal regions of the non-mammalian cynodonts Massetognathus, Probainognathus, and Elliotherium were reconstructed from micro-computed tomography scans and compared with scans and published accounts of more derived forms, including Brasilitherium, Morganucodon, Haldanodon, and extant mammals. The basic structure of the modern mammalian nose, already present in non-mammalian cynodonts of the Early Triassic, underwent little modification during the Triassic. A respiratory chamber opened into a nasopharyngeal passage through an enlarged primary choana bordered posteriorly by a transverse lamina that formed the floor to a more posterior olfactory chamber. Cartilaginous respiratory turbinals initially provided a surface for evaporative cooling during periods of increased activity in the exceptionally high ambient temperatures of the Triassic. A similar mechanism for heat loss is present in extant crocodilians, squamates, and mammals. In the Late Triassic and Early Jurassic non-mammaliaform cynodonts (Elliotherium) and mammaliaforms (Morganucodon), the pterygopalatine ridges behind the hard secondary palate extended ventrally and formed the lateral walls to a narrow nasopharynx, as pterygoid hamuli do in extant mammals. Ridges in this position suggest the presence of a palatopharyngeus muscle in late non-mammaliaform cynodonts that could hold the larynx in an intranarial position during rest or low activity levels to prevent inhaled air from entering the oral cavity, thus allowing cartilaginous respiratory turbinals to assume an additional role as temporal countercurrent exchange sites for heat and water conservation. Ossification of respiratory turbinals in mammals enhanced their efficiency for conserving heat and water at rest, as well as their ability to dissipate heat during thermal stress.