Publications

Submitted
Alfred W. Crompton, Catherine Musinsky, José F. Bonaparte, Bhart-Anjan Bhullar, and Tomasz Owerkowicz. Submitted. “Evolution of the mammalian fauces region and the origin of suckling.” Journal of Mammalian Evolution.Abstract
Suckling in therian mammals requires synchronous activity in the tensor veli palatini, palatoglossus, mylohyoideus and intrinsic tongue muscles that close the fauces. These muscles draw the dorsal surface of the tongue against a tensed soft palate to form a seal between the oral cavity and oropharynx. Depressing the tongue in front of the seal induces negative pressure and draws milk into the oral cavity. To trace the origin of fauces region in mammals, we studied serial sections of a pouch young marsupial and CT scans of non-mammalian cynodonts, ictidosaurs, mammaliaforms, and extant mammals.In Late Triassic ictidosaurs (Brasilitherium) and mammaliaforms, the origin of a medial slip of the reptilian posterior pterygoideus migrated to the lateral surface of the pterygopalatine boss that supported the lateral edge of a non-muscular soft palate. Suckling arose in early mammals after fibers of this slip migrated into the soft palate to form the tensor veli palatini, and the palatoglossus separated from the pharyngeal constrictors. The added stress on the pterygopalatine boss led to the addition of a hamulus. Once the transverse process of the pterygoid was lost, the lateral posterior pterygoideus differentiated to form the medial pterygoid. Monotreme ancestors modified the fauces region to break down invertebrates between keratinized pads on the posterior tongue and under the ventral surface of a long palatine. They lost the tensor veli palatini and palatoglossus and lack the ability to suckle.
2020
B. A. S. Bhullar, A. R. Manafzadeh, J. A. Miyamae, E. A. Hoffman, E. L. Brainerd, C. Musinsky, and A. W. Crompton. 2020. “The origin of chewing in mammals required rolling of the jaw and involved broad continuity in molar form and function.” Integrative and Comparative Biology, 60, Pp. E17-E17.
B. A. S. Bhullar, A. R. Manafzadeh, J. A. Miyamae, E. A. Hoffman, E. L. Brainerd, C. Musinsky, and A. W. Crompton. 2020. “Reply to: Jaw roll and jaw yaw in early mammals.” Nature, 582, Pp. E9-E12.
2019
T. Owerkowicz, M. Poff, K. M. Middleton, and A. W. Crompton. 2019. “Metabolic and Environmental Factors Shaping the Morphology of Respiratory Turbinates in Mammals and Archosaurs.” Journal of Morphology, 280, Pp. S195-S195.
A. W. Crompton, C. A. Musinsky, B. A. Bhullar, and T. Owerkowicz. 2019. “Origin of Suckling in Therian Mammals.” Journal of Morphology, 280, Pp. S102-S102.
B. A. S. Bhullar, A. R. Manafzadeh, J. A. Miyamae, E. A. Hoffman, E. L. Brainerd, C. Musinsky, and A. W. Crompton. 2019. “Rolling of the jaw is essential for mammalian chewing and tribosphenic molar function.” Nature, 566, Pp. 528-+.Abstract
Over the past two centuries, mammalian chewing and related anatomical features have been among the most discussed of all vertebrate evolutionary innovations(1-3). Chief among these features are two characters: the dentary-only mandible, and the tribosphenic molar with its triangulated upper cusps and lower talonid basin(3-5). 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(6,7). Following the appearance of precise dental occlusion near the origin of the mammalian crown(8,9), 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(10-12). 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(13).
2017
José F. Bonaparte and Alfred W. Crompton. 6/2017. “Origin and relationships of the Ictidosauria to non-mammalian cynodonts and mammals.” Historical Biology. Publisher's VersionAbstract
Ictidosaurian genera are allocated to two families, Tritheledontidae and Therioherpetidae. This paper provides a diagnosis for Ictidosauria. The previously named family Brasilodontidae is shown to be a junior synonym of a family, Therioherpetidae. It is concluded that Ictidosauria originated from Late Permian procynosuchid non-mammalian cynodonts rather than from Middle Triassic probainognathid non-mammalian cynodonts. The structure of the skull and jaws of a derived traversodontid Ischignathus sudamericanus from the early Late Triassic of Argentina supports an earlier view that tritylodontids are more closely related to traversodontid than probainognathid non-mammalian cynodonts. Tritylodontids should not be included in Ictidosauria, nor should they considered to be a sister group to mammaliaforms.
bonapartecromptonictids.pdf
A. W. Crompton, Tomasz Owerkowicz, Bhart-Anjan Bhullar, and Catherine Musinsky. 1/2017. “Structure of the nasal region of non-mammalian cynodonts and mammaliaforms: speculations on the evolution of mammalian endothermy.” Journal of Vertebrate Paleontology, 37, 1.Abstract

Nasal regions of the non-mammalian cynodont, Massetognathus, Probainognathus, and Elliotherium were reconstructed from micro-CT 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.

Crompton_jvp_nose_evolution.pdf
A. W. Crompton, C Musinsky, G.W. Rougier, B.-A.S. Bhullar, and J. A. Miyamae. 2017. “Origin of the Lateral Wall of the Mammalian Skull: Fossils, Monotremes and Therians Revisited.” Journal of Mammalian Evolution, published online, 24 April 2017, Pp. 1–13.Abstract
To interpret the fundamental differences in the structure and origin of the braincase sidewalls of monotremes, multituberculates, and therians, we examined MicroCT scans of a mammaliaform, Morganucodon; two non-mammalian cynodonts, Massetognathus and Probainognathus; a stem therian, Vincelestes; a juvenile and adult monotreme, Ornithorhynchus; and two marsupials, Monodelphis and Didelphis. The skull of Morganucodon resembles the pattern predicted for an early mammal: the descending flanges of the frontal and parietal cover the lateral surface of the orbitosphenoid and the palatine forms most of the medial wall of the orbit. In monotremes, the lateral region of the chondrocranium ossifies to form a long presphenoid/orbitosphenoid complex. During the transition from early mammals to extant mammals the height of the alisphenoid decreased drastically, the anterior lamina extended anteriorly to form part of the sidewall while the lateral surface of the orbitosphenoid was exposed by the dorsal withdrawal of the frontal and parietal. By contrast, in multituberculates and therians the lateral edges of the frontals extended further ventrally and the orbitosphenoid was reduced to a smaller orbital exposure below the frontals. In multituberculates the alisphenoid decreased in height, replaced by an anterior extension of the anterior lamina. The palatine withdrew from the orbital wall, replaced by a dorsally directed expansion of the maxilla. Extant therians have lost the anterior lamina. The inferior edges of the frontal followed the further ventral migration of the orbitosphenoid. The alisphenoid and parietal form most of the braincase sidewall.
OriginOfTheLateralWall.pdf
2015
Tomasz Owerkowicz, Catherine Musinsky, Kevin M. Middleton, and A. W. Crompton. 2015. “Respiratory Turbinates and the Evolution of Endothermy in Extant Mammals and Birds.” In Great Transformations in Vertebrate Evolution, edited by Kenneth Dial, Elizabeth Brainerd, and Neil Shubin, Pp. 143–165. University of Chicago Press.
A. W. Crompton, Catherine Musinsky, and Tomasz Owerkowicz. 2015. “The Evolution of the Mammalian Nose.” In Great Transformations in Vertebrate Evolution, edited by Kenneth Dial, N. H. Shubin, and E. L. Brainerd. Chicago: University of Chicago Press. evolutionofmammalnose.pdf
Tomasz Owerkowicz, Catherine Musinsky, Kevin M. Middleton, and A. W. Crompton. 2015. “Respiratory Turbinates and the Evolution of Endothermy in Mammals and Birds.” In The Great Transformations in Vertebrate Evolution, edited by E. L. Brainerd, Kenneth Dial, and N. H. Shubin. Chicago: University of Chicago Press.
2011
A. W. Crompton and Catherine Musinsky. 2011. “How dogs lap: ingestion and intraoral transport in Canis familiaris.” Biological Letters, 7, Pp. 882-884.Abstract

 

It has recently been suggested that the mechan- ism for lifting liquid from a bowl into the oral cavity during lapping is fundamentally different in cats and dogs: cats use adhesion of liquid to the tongue tip while dogs ‘scoop’ with their backwardly curled tongue. High-speed light videos and X-ray videos show that on the con- trary, both cats and dogs use the mechanism of adhesion. Liquid is transported through the oral cavity to the oesophagus, against gravity, on the surface of the tongue as it is drawn upwards, then a tight contact between the tongue surface and palatal rugae traps liquid and prevents its falling out as the tongue is protruded. At least three cycles are needed for intraoral transport of liquid in the dog.

cromptonMusinskyHowdogslap.pdf
A. W. Crompton. 2011. “Masticatory Motor Programs in Australian Herbivorous Mammals, Diprotodontia.” Integrative and Comparative Biology, 51, Pp. 271-281. mastmotorprog_icb-2011-crompton.pdf
Regina Campbell-Malone, Alfred W. Crompton, Allan J. Thexton, and Rebecca Z. German. 2011. “Ontogenetic Changes in Mammalian Feeding: Insights from Electromyographic Data.” Integrative and Comparative Biology, 51, 2, Pp. - 288282. Publisher's VersionAbstract

Synopsis All infant mammals make a transition from suckling milk to eating solid foods. Yet, the neuromuscular implications of the transition from a liquid-only diet to solid foods are unknown even though the transport and swallowing of liquids is different from that of solids. We used legacy electromyography (EMG) data to test hypotheses concerning the changes in motor pattern and neuromuscular control that occur during the transition from an all-liquid diet to consumption of solid food in a porcine model. EMG signals were recorded from five oropharyngeal muscles in pigs at three developmental stages (infants, juveniles, and adults) feeding on milk, on food of an intermediate consistency (porridge), and on dry chow (juveniles and adults only). We measured cycle frequency and its variation in "transport cycles" and "swallow cycles". In the swallow cycles, a measure of variation of the EMG signal was also calculated. Variation in cycle frequency for transport and swallow cycles was lowest in adults, as predicted, suggesting that maturation of feeding mechanisms occurs as animals reach adulthood. Infants had lower variation in transport cycle frequency than did juveniles drinking milk, which may be due to the greater efficiency of the infant's tight oral seal against the teat during suckling, compared to a juvenile drinking from a bowl where a tight seal is not possible. Within juveniles, variation in both transport and swallow cycle frequencies was directly related to food consistency, with the highest variation occurring when drinking milk and the lowest when feeding on solid food. There was no difference in the variation of the EMG activity between intact infants and juveniles swallowing milk, although when the latter swallow porridge the EMG signals were less variable than for milk. These results suggest that consistency of food is a highly significant determinant of the variation in motor pattern, particularly in newly weaned animals.

2011campmalonefeeding.pdf
2010
A. W. Crompton, T. Owerkowicz, and J. Skinner. 2010. “Masticatory motor pattern in the koala (Phascolarctos cinereus): a comparison of jaw movements in marsupial and placental herbivores.” Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 313A, Pp. 564-578.Abstract

Abstract 10.1002/jez.628.abs Do closely related marsupial herbivores (Diprotodontia) conserve a common masticatory motor pattern or are motor patterns linked to the structure and function of the masticatory apparatus? We recorded the sequence and duration of activity of the individual jaw closing muscles during rhythmic chewing in koalas and then compared their motor pattern with that of their closest extant relatives, wombats, and their more distant marsupial relatives, macropodoids. These three lineages prove to have fundamentally different motor patterns and jaw movements during mastication. Each motor pattern represents independent modifications of an earlier motor pattern that was probably present in an ancestral diprotodontian. We show that koalas evolved a motor program that is in many aspects similar to that of placental herbivores with a fused mandibular symphysis (artiodactyls, perissodactyls, and higher primates) and almost identical to one artiodactyl, viz. alpacas. Anatomically, koalas are convergent on placental herbivores because they lost the inflected mandibular angle and large external part of the medial pterygoid muscle characteristic of other marsupials. We support the view that many different motor programs evolved for the control of transverse jaw movements, but identical motor programs for the control of transverse jaw movements can evolve independently in distantly related taxa. J. Exp. Zool. 313A, 2010. © 2010 Wiley-Liss, Inc.

jexpzool313acrompton.pdf
2009
A. J. Thexton, A. W. Crompton, T. Owerkowicz, and R. Z. German. 2009. “Impact of rhythmic oral activity on the timing of muscle activation in the swallow of the decerebrate pig.” J Neurophysiol, 101, Pp. 1386-93.Abstract

The pharyngeal swallow can be elicited as an isolated event but, in normal animals, it occurs within the context of rhythmic tongue and jaw movement (RTJM). The response includes activation of the multifunctional geniohyoid muscle, which can either protract the hyoid or assist jaw opening; in conscious nonprimate mammals, two bursts of geniohyoid EMG activity (GHemg) occur in swallow cycles at times consistent with these two actions. However, during experimentally elicited pharyngeal swallows, GHemg classically occurs at the same time as hyoglossus and mylohyoid activity (short latency response) but, when the swallow is elicited in the decerebrate in the absence of RTJM, GHemg occurs later in the swallow (long latency response). We tested the hypothesis that it was not influences from higher centers but a brain stem mechanism, associated with RTJM, which caused GHemg to occur earlier in the swallow. In 38 decerebrate piglets, RTJM occurred sporadically in seven animals. Before RTJM, GHemg had a long latency, but, during RTJM, swallow related GHemg occurred synchronously with activity in hyoglossus and mylohyoid, early in the swallow. Both early and late responses were present during the changeover period. During this changeover period, duplicate electrodes in the geniohyoid could individually detect either the early or the late burst in the same swallow. This suggested that two sets of geniohyoid task units existed that were potentially active in the swallow and that they were differentially facilitated or inhibited depending on the presence or absence of rhythmic activity originating in the brain stem.

2008
A. W. Crompton, J. Barnet, D. E. Lieberman, T. Owerkowicz, J. Skinner, and R. V. Baudinette. 2008. “Control of jaw movements in two species of macropodines (Macropus eugenii and Macropus rufus).” Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 150, Pp. 109-123.Abstract

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.

cromptonbarnetetal2008.pdf
Alfred W. Crompton, Rebecca Z. German, and Allan J. Thexton. 2008. “Development of the movement of the epiglottis in infant and juvenile pigs.” Zoology, 111, Pp. 339-349.Abstract

Although backward folding of the epiglottis is one of the signal events of the mammalian adult swallow, the epiglottis does not fold during the infant swallow. How this functional change occurs is unknown, but we hypothesize that a change in swallow mechanism occurs with maturation, prior to weaning. Using videofluoroscopy, we found three characteristic patterns of swallowing movement at different ages in the pig: an infant swallow, a transitional swallow and a post-weaning (juvenile or adult) swallow. In animals of all ages, the dorsal region of the epiglottis and larynx was held in an intranarial position by a muscular sphincter formed by the palatopharyngeal arch. In the infant swallow, increasing pressure in the oropharynx forced a liquid bolus through the piriform recesses on either side of a relatively stationary epiglottis into the esophagus. As the infant matured, the palatopharyngeal arch and the soft palate elevated at the beginning of the swallow, so exposing a larger area of the epiglottis to bolus pressure. In transitional swallows, the epiglottis was tilted backward relatively slowly by a combination of bolus pressure and squeezing of the epiglottis by closure of the palatopharyngeal sphincter. The bolus, however, traveled alongside but never over the tip of the epiglottis. In the juvenile swallow, the bolus always passed over the tip of the epiglottis. The tilting of the epiglottis resulted from several factors, including the action of the palatopharyngeal sphincter, higher bolus pressure exerted on the epiglottis and the allometry of increased size. In both transitional and juvenile swallows, the subsequent relaxation of the palatopharyngeal sphincter released the epiglottis, which sprang back to its original intranarial position.

zool25109.pdf
Alfred W. Crompton, Daniel E Lieberman, Tomasz Owerkowicz, Russell V. Baudinette, and Jayne Skinner. 2008. “Motor control of masticatory movements in the Southern hairy-nosed wombat (Lasiorihinus latifrons).” In Primate Craniofacial Function and Biology, edited by J. Vinyard, Christopher, J. Ravosa, Matthew, and E. Wall, Christine. New York: Springer. wombat2008.pdf

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