Rolling of the jaw is essential for mammalian chewing and tribosphenic molar function.

Over the past two centuries, mammalian chewing and related anatomical features have been among the most discussed of all vertebrate evolutionary innovations1-3. Chief among these features are two characters: the dentary-only mandible, and the tribosphenic molar with its triangulated upper cusps and lower talonid basin3-5. 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 hemimandible6,7. Following the appearance of precise dental occlusion near the origin of the mammalian crown8,9, 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 cusps10-12. 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 groundplan13.

Muscle Logic: New Knowledge Resource for Anatomy Enables Comprehensive Searches of the Literature on the Feeding Muscles of Mammals.

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.

A preliminary analysis of correlations between chewing motor patterns and mandibular morphology across mammals.

The establishment of a publicly-accessible repository of physiological data on feeding in mammals, the Feeding Experiments End-user Database (FEED), along with improvements in reconstruction of mammalian phylogeny, significantly improves our ability to address long-standing questions about the evolution of mammalian feeding. In this study, we use comparative phylogenetic methods to examine correlations between jaw robusticity and both the relative recruitment and the relative time of peak activity for the superficial masseter, deep masseter, and temporalis muscles across 19 mammalian species from six orders. We find little evidence for a relationship between jaw robusticity and electromyographic (EMG) activity for either the superficial masseter or temporalis muscles across mammals. We hypothesize that future analyses may identify significant associations between these physiological and morphological variables within subgroups of mammals that share similar diets, feeding behaviors, and/or phylogenetic histories. Alternatively, the relative peak recruitment and timing of the balancing-side (i.e., non-chewing-side) deep masseter muscle (BDM) is significantly negatively correlated with the relative area of the mandibular symphysis across our mammalian sample. This relationship exists despite BDM activity being associated with different loading regimes in the symphyses of primates compared to ungulates, suggesting a basic association between magnitude of symphyseal loads and symphyseal area among these mammals. Because our sample primarily represents mammals that use significant transverse movements during chewing, future research should address whether the correlations between BDM activity and symphyseal morphology characterize all mammals or should be restricted to this "transverse chewing" group. Finally, the significant correlations observed in this study suggest that physiological parameters are an integrated and evolving component of feeding across mammals.

A preliminary analysis of correlated evolution in Mammalian chewing motor patterns.

Descriptive and quantitative analyses of electromyograms (EMG) from the jaw adductors during feeding in mammals have demonstrated both similarities and differences among species in chewing motor patterns. These observations have led to a number of hypotheses of the evolution of motor patterns, the most comprehensive of which was proposed by Weijs in 1994. Since then, new data have been collected and additional hypotheses for the evolution of motor patterns have been proposed. Here, we take advantage of these new data and a well-resolved species-level phylogeny for mammals to test for the correlated evolution of specific components of mammalian chewing motor patterns. We focus on the evolution of the coordination of working-side (WS) and balancing-side (BS) jaw adductors (i.e., Weijs' Triplets I and II), the evolution of WS and BS muscle recruitment levels, and the evolution of asynchrony between pairs of muscles. We converted existing chewing EMG data into binary traits to incorporate as much data as possible and facilitate robust phylogenetic analyses. We then tested hypotheses of correlated evolution of these traits across our phylogeny using a maximum likelihood method and the Bayesian Markov Chain Monte Carlo method. Both sets of analyses yielded similar results highlighting the evolutionary changes that have occurred across mammals in chewing motor patterns. We find support for the correlated evolution of (1) Triplets I and II, (2) BS deep masseter asynchrony and Triplets I and II, (3) a relative delay in the activity of the BS deep masseter and a decrease in the ratio of WS to BS muscle recruitment levels, and (4) a relative delay in the activity of the BS deep masseter and a delay in the activity of the BS posterior temporalis. In contrast, changes in relative WS and BS activity levels across mammals are not correlated with Triplets I and II. Results from this work can be integrated with dietary and morphological data to better understand how feeding and the masticatory apparatus have evolved across mammals in the context of new masticatory demands.

Masticatory motor programs in Australian herbivorous mammals: diprotodontia.

Movement of the jaw during molar occlusion is determined by the sequence of activity in the adductor muscles and this sequence is one way to define a masticatory motor program. Based on the similarity of molar structure, it is probable that the American opossum and the early Tertiary mammals that gave rise to all Australian marsupials probably shared a common "primitive" masticatory motor program. The distinct and various patterns of movement of the jaw in the major groups of Australian marsupial herbivores (diprotodontids) are achieved by both subtle and substantial shifts in the timing of the primitive sequence. All diprotodonts divide jaw movements during occlusion into a vertical Phase Im and horizontal Phase IIm, but the number of muscles involved and the level of activity associated with each phase varies considerably. In macropodids (potoroos and kangaroos) Phase Im dominates; in wombats Phase IIm dominates and in koalas the two phases are more evenly divided, with a more equal distribution of muscles between them. The motor program of koalas parallels that of some placental ungulates, while both macropodids and wombats have motor programs unique among mammals.

Ontogenetic changes in Mammalian feeding: insights from electromyographic data.

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.

Development of the movement of the epiglottis in infant and juvenile pigs.

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.

Volume and rate of milk delivery as determinants of swallowing in an infant model animal (Sus scrofia).

The volume transported into the valleculae by the rhythmic tongue movements of suckling is considered the prime factor for initiating pharyngeal swallowing (the movement of milk out of the valleculae and through the pharynx to the esophagus). This study addressed the impact of variation in two factors on sucking (oral phase) and on swallowing (pharyngeal phase) in infant pigs, as a model for mammalian function: (1) the delivery of different-volume aliquots of milk and (2) the delivery of equal-sized aliquots at different frequencies. The number of sucks per second remained constant with change in both aliquot volume and change in the frequency of milk delivery. However, while the number of swallows per second remained constant as delivery volume increased, it increased as delivery frequency increased. Conversely, swallow volume increased with both increase in aliquot volume and in the frequency of delivery. Piglets consequently initiated pharyngeal swallows with a highly variable amount of milk in the valleculae. We conclude that volume is only one factor initiating the pharyngeal swallow. The sensory stimulation of milk delivery to the anterior oral cavity is also a factor in determining the frequency of swallows and the volume of milk per swallow.