Evolution of the mammalian fauces region and the origin of suckling

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Citation Crompton, Alfred, Catherine Musinsky, Jose Bonaparte, Bhart- Anjan Bhullar, and Tomasz Owerkowicz. Evolution of the mammalian fauces region and the origin of suckling (2018).

Citable link https://nrs.harvard.edu/URN-3:HUL.INSTREPOS:37364482

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Evolution of the mammalian fauces region and the origin of suckling

Alfred Crompton1†, Catherine Musinsky1, Jose Bonaparte2, Bhart-Anjan Bhullar3, Tomasz

Owerkowicz4

1: Harvard University, Organismic and Evolutionary Biology Department, Museum of Comparative

Zoology, 26 Oxford St, Cambridge, MA 02138 USA

2: Museo Municipal de C. Naturales "C. Ameghino", 6600 MERCEDES – BS. AS. Argentina

3: Department of Geology & Geophysics, Yale University, PO Box 208109, New Haven, CT 06520-

8109 USA

4: Department of Biology, California State University in San Bernadino, 5500 University Pkwy, San

Bernardino, CA 92407 USA

†corresponding author: ORCID 0000-0001-6008-2587, [email protected], 617-495-3202

Acknowledgments

Thanks to Dr. Edgar Allin for his comments on an early draft of this paper. Thanks to the Museum of Comparative Zoology, its Director, Professor James Hanken, and to the

Center for Nanoscale Systems at Harvard University for providing the facilities and finances for this research.

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Abstract

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 3

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. (needs shortening)

Keywords

Fauces, Suckling, Monotremes, Therians, Soft palate

Introduction

Review of the suckling mechanism in therian mammals and published accounts of sucking in monotremes.

A characteristic feature of therian mammals is that newborns (neonates or perinates) nurture by suckling from the teats of mammary glands. Monotremes, on the 4

other hand, lack teats, and their young (hatchlings) ingest milk released from mammary glands onto the belly of the mother. Echidnas have two areolae situated on the dorsolateral walls of a pouch that houses hatchlings until they develop spines and leave the pouch. Milk exudes through sinuses on the surfaces of the mammary glands. Contrary to some published accounts that suggested hatchlings acquired milk by lapping from the hairs on the mother’s belly, Griffiths (1965a, 1965b) claimed that this was only true for newly hatched echidnas. Later in their development, hatchlings imbibe milk by vigorously sucking from the sinuses. Griffiths (1965b) obtained a tape recording of a complete sucking session.

A day’s ration amounting to 7-10% of the hatchling’s body weight was imbibed in about half an hour.

Burrell (1974) pointed out that platypuses lack pouches, and that their mammary glands are covered with hairs that hold milk through surface tension. These hairs apparently serve in place of therian teats, and hatchlings suck the milk from them. Burrell wrote, “the ‘lips’ of the young, owing to the shortness and underdeveloped form of the bill at this stage, are adapted for sucking in conjunction with the tongue.” He did not include details on the structure of the opening to the oral cavity or how intraoral pressure was sufficiently reduced to draw in milk. He did however confirm that platypus neonates can suck when he placed a drop of milk on his forearm, and reported “a sucking action sufficiently strong to bring a flush of blood to the spot.” (p. 187, Burrell 1974).

Monotremes lack an osteological feature that is associated with suckling in therian mammals, and can also be recognized in fossil genera closely related to mammalian 5

ancestors: the pair of bony plates called the pterygoid hamuli that descend like paired rudders from the ventral surface of the pterygoid on the skull base of therian mammals

(Fig. 2c). In order to identify features in extant monotremes that can also be preserved and recognized in ancestral monotremes, additional information on the skull and oral musculature of an adult platypus and echidna, as well as that of a hatchling and juvenile platypus, are included in the result section of this paper.

A brief review of results from our cineradiographic recordings of sucking

(Crompton et al 1997; Thexton et al 1998; Thexton et al 2004; Crompton et al 2008) and lapping (Hiiemae and Crompton 1985; Crompton and Musinsky 2011) in therian mammals follows. A similar study on sucking in monotremes has not been attempted. The fact that monotremes lack pterygoid hamuli suggests that the mechanism for reducing pressure in the oral cavity differs from that of therians; but, again, no osteological features linked to sucking have been identified in monotremes.

During suckling in therian mammals, the tongue first forces the nipple against the roof of the mouth. Next, the lateral edges of the tongue curl around the edges of the nipple and reach the roof of the mouth to form a seal between the exterior and the oral cavity (Fig.

1A). A second seal closes the fauces, the narrow passage between the oral cavity and the oropharynx. To achieve this seal, the dorsal surface of the back of the tongue presses up against the ventral surface of the anterior region of the soft palate (Fig. 1a and 2b and c).

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The seal around the nipple prevents air from being sucked in from the exterior, and sealing the fauces prevents the transport of air or liquid from the oropharynx back to the oral cavity. When both seals are intact, depressing the tongue behind the nipple reduces intra-oral pressure (Thexton et al 2004) thereby drawing milk from the nipple into the oral cavity. Next, as the fauces’ seal relaxes, the mid-tongue elevates and forces milk through the fauces into the oropharynx (Fig. 1b). The fauces’ seal is then reestablished, and the tongue and pharyngeal constrictors force liquid into the esophagus, either over the larynx or around it, through the pyriform recesses (Fig. 1. See also Crompton et al 2008).

In lapping (Hiiemae and Crompton 1985; Crompton and Musinsky 2011), the tongue tip is extruded into a pool of liquid. A portion of liquid, or aliquot, adheres to the dorsal surface of the tongue tip and is drawn into the oral cavity as the tongue withdraws. As the tongue extrudes for the next lapping cycle, liquid previously drawn into the oral cavity is trapped between the dorsal surface of the tongue and the palatal rugae. When the tongue extrudes for a third time, milk ingested in the first cycle is carried back through the fauces to the oropharynx and is trapped there by closing of the fauces as the tongue continues to pick up more liquid in subsequent cycles. Repeated lapping cycles increase the volume of liquid in the oropharynx. Once a critical volume is reached, the milk is swallowed.

During mastication, the fauces are closed and solid food is broken down in the oral cavity through repeated chewing cycles to form a malleable bolus. The bolus is then transferred through the fauces to the oropharynx. The manipulation of solid food within 7

the oral cavity is referred to as Stage I transport, and transport of solid or liquids through the fauces as Stage II transport (Hiiemae and Crompton 1985).

Muscles that control the closing of the fauces

Several muscles including the intrinsic muscles of the tongue are involved in closing the fauces by pressing the dorsal surface of the tongue against the soft palate: (a) The long and slender tensor veli palatini muscle (Tachimura et al 2006) extends forward from the cochlear region of the petrosal bone, and hooks around the ventral edge of the pterygoid hamulus to insert into the soft palate (Fig. 2). When contracted it stiffens the soft palate. (b)

The palatoglossal muscle (Tachimura et al 2006) originates in the lateral surface of the tongue and inserts into the soft palate (Fig. 2c). It helps to pull the tongue toward the soft palate. (c) Left and right mylohyoideus muscles originate on the hemimandibles and weave together below the tongue (Fig. 2c) to form a hammock. When active, these muscles form a firm base below the tongue. and elevate it slightly. (d) The tongue itself is a constant volume structure (Kier and Smith 1985) capable of dramatic changes in shape through differential contraction of its intrinsic musculature. These muscles when acting together with the palatoglossal and mylohyoideus muscles increase the height of the posterior region of the tongue, and they help to press its dorsal surface against the soft palate to form a tight seal.

The oropharynx is the space between the back of the tongue and anterior surface of the epiglottis and palatopharyngeus (Fig. 1a). Also referred to as the valleculae, the 8

oropharynx in both monotremes and therians store and collect liquid and masticated food prior to swallowing.

The palatopharyngeus is perforated by a sphincter (Fig. 1 a & b marks this sphincter with a dotted line joining the posterior limit of the palatopharyngeus and esophagus).

During normal breathing, the sphincter surrounds the larynx preventing airflow between the lungs and nose from entering the oral cavity (Crompton et al 2008). This plays an important role in the conservation of water and heat in mammalian endothermy

(Crompton et al 2017b).

Because the pterygoid hamuli and tensor veli palatini muscles play an important role during the transport of liquids, acquired by either suckling or lapping and solid food from the oral cavity to the valleculae, in the results section of this paper we document the progressive steps in mammalian ancestors leading to the origin of the pterygoid hamuli and the tensor veli palatini muscles. The presence of osteological precursors to the pterygoid hamuli provides a clue as to when Stage II transport and possibly also suckling first appeared in the ancestors of therian mammals.

Published views on the origin of the pterygoid/hamulus complex and tensor veli palatini muscles

In therian mammals the pterygoid/hamulus complex ossifies from two distinct aggregates of mesoderm that fuse before the formation of bone or cartilage (Presley and

Steel 1978). The dorsal aggregate gives rise to the pterygoid bone, a flat membrane bone with a thin ventrally directed keel. The ventral aggregate gives rise to the pterygoid 9

hamulus. Fig. 3 (a & b) illustrates the anatomy of the pterygoid hamulus complex in a pouch-young Didelphis. The dorsal surface of the pterygoid is closely applied to the ventral surface of the skull base. The hamulus, at this stage, consists of a keel extending ventrally from the pterygoid and a rod of secondary cartilage below the keel. This rod continues posteriorly as a stout process (Fig. 3b). The tensor veli palatini wraps around the ventral edge of the rod of secondary cartilage and extends into the soft palate. The hamulus overlaps the medial surface of the posterior border of the palatine and contributes to the lateral wall of the nasopharynx (Fig. 2c). In the adult, this secondary cartilage ossifies and fuses with the keel of the pterygoid (Fig. 2c). DeBeer (1937, p. 502) accounted for secondary cartilage in the hamulus as an “adaptation for resistance to precocious strains and stresses on part of the rudiments of membrane bones.” In fact, the secondary cartilage in the hamulus arises from the stress generated by a developing tensor veli palatini wrapping around the ventral aggregate of mesoderm. The same mechanism may also account for the presence of secondary cartilage on condylar process of the dentary in mammals, where adductor muscles subject the precursor cells of the condylar process to stress during ontogeny (Velasco et al 2009); or the cartilaginous growth structures in the palatal midline of therian mammals, resulting from strain patterns associated with suckling. After weaning these structures disappear and the palate ossifies (Li et al 2016).

Barghusen (1986) agreed with Allin (1976) that in Thrinaxodon (Fig. 4), the reptilian posterior pterygoid muscle originated on the posterior edge of the transverse process of the pterygoid, the lateral surface of the pterygoid, and the quadrate ramus of the 10

pterygoid; and inserted on the postdentary bones (see also Allin and Hopson 1992).

Barghusen (1986) suggested that the soft palate in an early non-mammalian cynodont such as Thrinaxodon consisted of a non-muscular velum (ve) that attached to the choanal ridge, continuing along a ridge on the ectopterygoids, and onto the lateral edges of the transverse process of the pterygoid (Fig. 4). He proposed (Barghusen 1986) that the posterior part of the velum attached to the pterygopalatine bosses to form a channel between them (see bold arrows in Fig. 4). This channel led to the opening of the larynx, and the two lateral channels to a space below the posterior pterygoideus muscle, the sulcus pharyngeus submandibularis (Shute 1956). Allin (1976) suggested that this space was the forerunner of the communication between the mammalian nasopharynx and middle ear.

Barghusen (1986) observed that in the transition from non-mammalian cynodonts to therian mammals, the massive pterygoid of the former was reduced to form the thin pterygoid bone on the skull base of the latter. He agreed however with Parrington and

Westholl (Parrington and Westoll 1940) and Presley and Steel (Presley and Steel 1978), that the hamulus of therian mammals derived from the ectopterygoid of non-mammalian cynodonts. Allin and Hopson (1992), on the other hand, suggested that the hamulus derived from the lateral edge of the transverse process of the pterygoid. According to

Barghusen (1986), the entire reptilian posterior pterygoideus muscle was lost in mammals except for a small lateral slip that formed the tensor veli palatini and tensor tympani muscles.

In monotreme ontogeny, we suggest that the two aggregates of mesoderm do not fuse; and instead, give rise to two separate membrane bones, the pterygoid and the echidna 11

pterygoid (Presley and Steel 1978; De Beer 1985). We therefore consider the therian hamulus and monotreme echidna pterygoid homologous structures (Presley and Steel

1978). That the two aggregates, in therians and monotremes, stain in an identical manner lends further support to this conclusion. As Presley and Steel (1978, p. 105) stated, “each

[aggregate?] has undoubtedly appeared as a core membrane bone before any cartilage appeared in the ventral element.” Several other authors have also homologized the hamulus of therian mammals with the echidna pterygoid of monotremes (Broom 1914;

Watson 1916).

Presley and Steel (1978), Parrington and Westholl (1940), Barghusen, (1986) and

Zeller (1989) consider the therian pterygoid hamulus as homologous with the non- mammalian cynodont ectopterygoid. So confident of this homology was Zeller (1989) that he dropped the name echidna pterygoid and referred to it instead as the ectopterygoid.

Presley and Steele’s claim that the echidna pterygoid of the platypus “is more like those of true mammals, “even possibly to the extent of showing cartilage in relation to the tensor palatini muscles.” They further state,

We attribute the origin of the secondary cartilage in the

ectopterygoid to its special role in the mechanics of the secondary palate:

specifically to act as a ‘pulley’. Where the ectopterygoid serves mainly as an

element of the hard part of the palate, it remains a membrane bone. It

follows that the membrane bone is the primitive state of the ectopterygoid 12

and the cartilaginous hamulus represents an advanced character-state in

mammalian evolution. (Presley and Steel 1978, p. 109)

Few agree with DeBeer (De Beer 1985, p. 436) that the reptilian pterygoid is homologous with the echidna pterygoid. Parrington and Westholl (Parrington and Westoll

1940) pointed out that the transition from nonmammalian cynodonts to mammals is characterized by a massive reduction of the size of the pterygoid bone resulting in a loss of contact between the transverse process of the pterygoid and the coronoid bone on the inner surface of the lower jaw. Despite this reduction, they claimed that the ectopterygoid is retained in therians where it fuses with the pterygoid, and forms the hamulus and part of the lateral wall of the nasopharynx. Barghusen’s (1986) reason for homologizing the ectopterygoid with the hamulus in therians was, in part, based, on his conclusion that a ridge on the ventral surface of the non-mammalian cynodont ectopterygoid supported a non-muscular velum the same way as the hamulus does the soft palate in therian mammals

(see Fig. 2b).

Parrington and Westoll (1940) suggested that the reptilian adductor internus pterygoideus (referred to by Barghusen (1986) as the reptilian posterior pterygoideus (Fig.

4, ppm)) originated on the posterior edge of the transverse process of the pterygoid. This muscle progressively reduced in size along with the pterygoid’s diminishment in the transition to mammals. Parrington and Westholl (1940) concluded that a remnant of this muscle was retained in therians as the tensor veli palatini. Barghusen (1986) agreed with this conclusion, further claiming that this remnant also gave rise to the tensor tympani. In 13

an earlier draft of this paper we assumed Barghusen to be correct that the tensor arose together from the reptilian posterior pterygoideus. The fact that monotremes retain the tensor tympani but lack the tensor veli palatini would suggest that monotremes once possessed, then lost the tensor veli palatini. This so lacks parsimony that it brings into question the common origin of the tensors.

We disagree with Barghusen (1986) that the therian hamulus is homologous with the ectopterygoid, and suggest instead that it represents a new structure that arose on the ventral edges of the pterygopalatine ridges of non-mammalian cynodonts when the precursor cells of these ridges were subjected to stress by the tensor veli palatini.

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Anatomical Abbreviations

a, b, c, or d: position of corresponding transverse section through the pharyngeal regions af air flow ep epiglottis

AL alisphenoid EP epipterygoid am auditory meatus eso esophagus ama anterior maxillary artery f fauces an annulus of the sternoglossus F frontal

AR articular fem free edge of mylohyoid b buxonators FO fenestra ovalis bd bony division of the palatopharyngeal ft forked tip

passage g glottis

BH basihyoid gh geniohyoideus

BO basioccipital gl glenoid fossa

BS basisphenoid ilppm insertion of lateral part of the posterior ca canine pterygoideus muscle ccb contact area with coronoid I/M incus/malleus ch internal choana imp insertion of medial pterygoid chc choanal crest imppm insertion of medial part of the posterior

D dentary pterygoideus muscle dt detrahens IN incus

EC ectopterygoid ippm insertion of posterior pterygoideus

ECH echidna pterygoid muscle

ECT ectotympanic ipst insertion of the pseudotemporalis emt ethmoturbinal itt insertion of tensor tympani 15

ipv interpterygoid vacuity OS orbitosphenoid ks keratinized surface P palatine

LAC lachrimal pa pila antotica lo laryngeal opening PAR prearticular lp lateral pterygoideus pf palatine foramen lppp lateral portion of the posterior pg palatoglossus

pterygoideus PH pterygoid hamulus ma mandibular angle pit pituitary

MAL malleus pn foramen for the lesser palatine nerve m masseter pp palatopharyngeus ma mandibular angle ppm posterior pterygoideus muscle

MC Meckel’s Cartilage ppr pterygopalatine ridge mg myoglossus PS parasphenoid mh mylohyoideus PSP presphenoid mhp mylohyoideus process PT pterygoid mp medial pterygoideus ptb pterygopalatine boss mppp medial portion of the posterior Q quadrate

pterygoideus qre quadrate ramus of epipterygoid ms medial slip of posterior pterygoideus qrp quadrate ramus of pterygoid

MX maxilla R reflected lamina np nasopharyngeal passage imppm insertion of medial part of the posterior

O1 origin of the pseudotemporalis pterygoideus

O2, O3 origin of reptilian pterygoideus rl reflected lamina oc oral cavity rp retroarticular process op oropharynx SA surangular oppm origin posterior pterygoideus sg sternoglossus 16

sh stylohyoideus te temporalis sp soft palate tp transverse process of pterygoid

SP splenial tvp tensor veli palatini

SQ squamosal V trigeminal nerve sr sharp ridge v valley

ST stapes ve non-muscular velum t tongue Z zygomatic arch td tissue division of the palatopharyngeal

passage

Institutional Abbreviations

AMNH—American Museum of Natural History, MCZ—Museum of Comparative Zoology, Harvard

New York; University, Cambridge, MA,

IVPP—Institute of Vertebrate Palaeontology and USA; UFRGS—Universidade Federal do Grande do

Paleoanthropology, Beijing; Sul. Porto Alegre

Materials and Methods

We used MicroCT technology to scan the skull of Thrinaxodon liorhinus (AMNH.

2226); Massetognathus pascuali (MCZ 3790); Probainognathus jenseni (MCZ 4280);

Kayentatherium weleai (MCZ 8811); Morganucodon watsoni (IVPP 8682); Ornithorhynchus anatinus (AMNH 2013); and uncatalogued specimens of Elliotherium sp. (on loan from Prof.

J. Hopson), Pachygenelus sp. (South African Museum), and uncatalogued specimens of

Monodelphis domestica and Didelphis virginiana. These specimens were scanned at Harvard 17

University’s Center for Nanoscale Systems using an Xtek HMXST Micro-CT X-ray imaging system that provided resolution of our specimens ranging from 0.01 mm per voxel to 0.07 mm per voxel. Scans for the skull of Brasilitherium riograndensis (UFRGS-PV-1043-T) were provided by Prof. Wolfgang Maier (scanning procedures followed are given in Rodrigues et al., 2013). To reconstruct the skulls of Thrinaxodon, Elliotherium, Pachygenelus,

Morganucodon, Ornithorhynchus and Brasilitherium, image stacks of voxel information were exported from CT-scanning software, Xtex CT Pro, processed in VG Studio Max and imported into Amira, where the bones were segmented and visualized in stereo. The skull of the juvenile Ornithorhynchus and adult Monodelphis were stained in lugols prior to scanning. The skull of an adult Ornithorhynchus, unfortunately lacking the posterior pharyngeal region, was embedded in plastic and serially sectioned. Uncatalogued, stained serial sections of a pouch-young Didelphis were also studied.

We have reconstructed and compared CT scans of the palatal regions of

Thrinaxodon, Massetognathus, Probainognathus, Kayentatherium, Elliotherium,

Pachygenelus, Brasilitherium and Morganucodon; as well the extant monotremes

Ornithorhynchus anatinus and Tachyglossus aculeatus; and the primitive marsupials

Monodelphis domestica and Didelphis virginiana. What follows is a hypothesis about how the structure of the bony palate in mammalian ancestors led to the divergent palatal structures in therians and monotremes. 18

Results

Oropharyngeal region in Monotremes (Figs. 4 and 5)

The structure of the oropharyngeal region of monotremes reflects their unique mechanism for processing food. The diet of adult platypuses consists of small aquatic invertebrates which they break down in two ways: by crushing them between horny plates that replace Therian-like molars during develoment, and between keratinous pads on the dorsal surface of the tongue and ventral surface of the palate (Fig. 5a, ks). The latter lies directly below the palatine bone, which extends backwards nearly as far as the basisphenoid/basioccipital contact, and forms a floor to a divided nasopharyngeal passage

(Fig. 4c). Echidnas feed on terrestrial invertebrates (Grant 1984) and have tooth-like keratinous “denticles” covering the dorsal surface of the posterior tongue and ventral surface of the palate between which they grind their food (figure in progress). The echidna tongue rapidly protracts and retracts both for food good gathering and processing of food.

In both, after food is sifted to remove exoskeletons, the digestible remains pass into a deep pocket that Göppert (1901) referred to as a “pharyngeal vestibulum.” This appears to be homologous with the oropharynx of therians (Fig. 5a), and the narrow opening into the oropharynx the equivalent of the fauces in therian mammals. In both therians and monotremes this oropharyngeal space is bordered by the palatopharyngeus, epiglottis, and the posterior surface of the tongue.

The soft palate of Ornithorhynchus consists of a small anterior region (Fig. 4a) and a longer posterior region formed by the palatopharyngeus (Fig. 5a). The anterior part of the 19

echidna pterygoid is a flat horizontal blade lying parallel to but not in contact with the lateral edge of the palatine (Fig. 4a). The posterior dorsal edge of the echidna pterygoid abuts the ventral surface of the descending processes of the basisphenoid (Fig. 4b) and extends ventrolaterally as a hook-shaped process that comes close to the ectotympanic.

The posterior edge of the palatine, the posterior medial edge of the anterior portion of the echidna pterygoid, and the descending flanges of the basisphenoid together support the anterior portion of the soft palate (Fig. 4b); but the soft palate does not attach to the hook- shaped posterior process of the echidna pterygoid. Of the juvenile and adult platypuses that we studied, neither larynx was completely preserved; however, in a smaller hatchling the pharyngeal region is complete (Fig. 5a). In the adult, the oropharynx is deep, extending backwards on both sides of the wide and thick soft palate containing the palatopharyngeus

(Fig. 5b), and lies medial to the stylohyoid cornu (best illustrated in two transverse sections through the oropharynx, Fig. 5c, d). The epithelium of the oropharynx is thick and convoluted, and seemingly glandular, unlike that in therians where the walls are thin and smooth.

In contrast to therians, the anterior, forward curving portion of the stylohyoid in monotremes is embedded in the posterior region of the tongue (Fig. 5). A well-developed stylohyoideus muscle inserts on the stylohyoid (Schulman 1906) and can draw the posterior region of the tongue in a posterodorsal direction. A prominent mylohyoideus process (referred to as the lingula mandibulae by Zeller 1989) protrudes from the inner surface of each dentary hemimandible and serves as the origin for the posteromedial edge 20

of a powerful mylohyoideus muscle. Anterior to this point the muscle has a long slender insertion on the inner surface of the hemimandibles. Below the mylohyoideus process, each mylohyoideus directs vertically downward, parallel to the lateral surface of the tongue,

(Fig. 5c) and as in therians meets the opposite side mylohyoideus below the tongue. The mandibular branch of the trigeminal nerve lies below the mylohyoid process and between the mylohyoid and dentary (Fig. 5b). It enters the mandible through a foramen below the mylohyoid process. Acting together with the tongue muscles the mylohyoideus and stylohyoideus can elevate the tongue to press its rough, keratinized dorsal surface against the similarly rough and keratinized ventral surface below the palatine. Fibers of the medial pterygoid align transversely from its origin on the basisphenoid to its attachment on the dentary. Acting unilaterally these muscles can draw the hemimandibles to one side or the other.

Although monotremes lack pterygoid hamuli and the therian fauces-closing muscles, the tensor veli palatini and palatoglossus, they do possess tensor tympani muscles. These insert on the incus and originate on the ventral surfaces of the petrosal (Fig. 4a).

A distinctive feature of monotremes, and in sharp contrast with therian mammals, nonmammalian cynodonts and mammaliaformes, is a long palatine that extends backwards

(compare Figs 2b and 4a) below the pterygoids to form a floor to the nasopharyngeal passage (Fig. 4c). In non-mammalian cynodonts the ectopterygoid lies directly posterior to the palatine. It is possible that as the palatine grew backwards, the ectopterygoids shifted underneath it. In the adult (Fig. 5b, c and d), a flap of tissue (td) attached to the dorsal wall 21

of the nasopharynx extends the bony division (bd) . This progressively decreases in height and only partially divides the nasopharynx.

The general consensus seems to accept a homology between the ectopterygoid, hamulus and echidna pterygoid, but it is far from clear as to whether the echidna pterygoid arose directly from the ectopterygoid or from the hamulus. If true, the former would suggest that the ancestors of monotremes lacked a pterygoid hamulus at all (?), while the latter story would suggest that a hamulus was present in monotreme ancestors and then lost together with the tensor veli palatini in extant monotremes. A third option, that we favor, abandons any homologies with the ectopterygoid, and suggests that a pterygopalatine ridge gave rise to the pterygoid hamulus in therians; and that in monotremes the palatine grows far enough posteriorly to separate the anlage of the hamulus, which became the echidna pterygoid, from that of the dorsal part of the pterygoid.

Ancestral monotremes (Archer et al 1993; Rich et al 2001; Rowe et al 2008) had large molars with shearing surfaces. The molars are replaced with horny plates during ontogeny in extant monotremes, and these, together with the keratinized surfaces on the tongue and palate, are associated with their unique feeding mechanism. The echidna

Tachyglossus aculeatus (Doran and Baggett 1972; Murray 1981) has especially well- developed horny plates. 22

Monotreme mothers do not have nipples; instead, they extrude milk from areolae onto the belly (Koyama et al 2013). Platypus hatchlings do not suckle, rather they lick up their mothers’ milk (Grant and Temple-Smith 1998), exposing them to microbes.

Green et al. (1985) claimed that pouch young echidnas actually suckle. We doubt this because echidnas lack nipples and other adaptations associated with suckling. It is more likely that they lap up milk in the same way as platypus nestlings do.

Epicynodontia

Palate of Thrinaxodon (Fig. 7)

The reptilian pterygoideus and pseudotemporalis muscles appear to have originated on three surfaces that blend into one another on the pterygoid and epipterygoid of Thrinaxodon. The pseudotemporalis must have originated on the vertical surface of the pterygoid (O1) above its lateral edge. The posterior pterygoideus would have originated on the surface of the pterygoid behind its transverse process (O2) and on the posterior surface of the transverse process and its descending flange (O3). The posteroventral edge of the transverse process forms a sharp ridge, separated from the tall pterygopalatine boss (ptb) by a shallow valley (v). The bosses extend forward, not in the form of pterygopalatine ridges but rather by rounded edges that lie medial to the flat horizontal lateral surfaces of the palatines. Prominent pterygoid bosses are also present in the Permian non-mammalian cynodonts such as Leavachia (Brink 1963a). We agree with Barghusen (1986) that the airway probably passed backwards between the pterygopalatine bosses to reach the glottis. 23

We doubt, however, that a large non-muscular velum stretched between the lateral edges of the transverse processes and ridge on the ectopterygoid (Barghusen 1986), since the flat ventral surface of the ectopterygoid lacks a ridge, and the choanal crest on the palatine terminates anterior to the ectopterygoid. We suggest instead that the choanal crest alone supported a non-muscular soft palate, the posterior border of which did not extend beyond the palatine.

The pterygoid bosses in Thrinaxodon, those in therocephalians such as

Theriognathus (Huttenlocker and Abdala 2015), in Regisaurus (Mendrez 1972) and gorgonopsians (Sigogneau 1970) lie in the same relative position as the fauces in therian mammals. Some manipulation and breakdown of food probably occurred in the oral cavity of all these therapsids because they possessed heterodont dentitions (incisors, canines and postcanines). We suggest that the intermandibularis (homologue of the mylohyoid) elevated the tongue to press its dorsal surface against the dentigerous tuberosities or bosses, thus forming a variable division between the pharynx and oral cavity that prevented premature passage of food into the pharynx. This may represent an early step in the formation of tongue/soft palate contact in therian mammals that separated the oral cavity from the oropharynx.

In lepidosaurian reptiles, the pterygoideus muscle inserts medially, ventrally, and laterally on the angular. The pseudotemporalis originates on the rod-like epipterygoid and inserts on the dorsal and medial surfaces of the surangular (Iordansky 2010). In

Thrinaxodon (Fig. 8), as suggested by Barghusen (1986), the pterygoideus muscle inserted 24

on the medial surface of the postdentary bones, including the prearticular (PAR) and ventrally directed retroarticular process (rp). The pseudotemporalis originated on the ventral exterior surface of the epipterygoid (O1) and inserted on the broad medial surface of the surangular (SA).

Eucynodontia

Massetognathus and Probainognathus (Fig. 9)

The palates of these two genera share basically the same structure as that of

Thrinaxodon. The specimens of Massetognathus and Probainognathus we studied lack pronounced pterygoid bosses, but these are present in others, e.g., Diademodon (Brink

1963b). This difference may be due to the fact that these structures are easily damaged or destroyed during mechanical preparation.

As in Thrinaxodon, a shallow valley separates the sharp posterior edge of the transverse process and the pterygopalatine ridge. The surface for the origin of the pterygoideus extends from the lateral surface of the pterygoid onto the tall vertical descending flange of the pterygoid’s transverse process (O3, Fig. 9c), avoiding the ventral surface of the transverse process. In an anterior direction the pterygopalatine ridges terminate just past the pterygoid/palatine suture and continue forward as rounded edges, as in Thrinaxodon. The posterior end of the choanal crest terminates where it turns abruptly medially to form the border of a small foramen in the palatine bone. 25

We propose that a non-musculature velum inserted on the choanal crests and did not extend back beyond their termination on the palatine. An ectopterygoid has not been identified in eucynodonts.

The postdentary bones behind and below the coronoid in eucynodonts, for example

Cynognathus (Fig. 8), are, in comparison with epicynodonts, greatly reduced in size and depth, and partially supported by a shallow depression of the medial surface of the dentary.

In Thrinaxodon, the medial surface of the angle of the dentary is completely covered by the splenial. In eucynodonts, reduction of the postdentary bones exposes the medial surface of the angle of the dentary below them. Eucynodonts show no substantial decrease in the area for the origin of the pterygoideus muscle, and hence its size. In epicynodonts, the pterygoideus inserted only on the postdentary bones and it is unlikely that in eucynodonts the reduced postdentary bones provided the sole area for the insertion of the pterygoideus.

We suggest that part of the insertion moved onto the exposed medial surface of the angle of the dentary. In addition, we speculate that the insertion of the pseudotemporalis expanded onto the medial surface of the dentary above the surangular.

Tritylodontidae

Kayentatherium (Fig. 10)

A juvenile specimen of the tritylodontid, Kayentatherium (Sues 1986) has a tall descending flange of the transverse process, and a large area for the origin of a pterygoideus muscle on its posterior surface (Fig. 10c, O3). The valley between the posterior edge of the transverse process of the pterygoid and the pterygopalatine ridge is 26

absent (compare Figs. 9c and 10c). This suggests the possibility that, in contrast to epi- and eucynodonts, a slip of the medial part of the pterygoideus muscle may have migrated onto the lateral surfaces of the pterygopalatine ridges. The medial edges of the pterygoid form the lateral borders of a large interpterygoid vacuity divided in the midline by the parasphenoid. The pterygopalatine ridges are tall and slender. As in eucynodonts, they terminate just anterior to the palatine-pterygoid border and continue forward in the form of gently rounded edges. The choanal crest is prominent and terminates posterolaterally before a small foramen within the palatine, identified by Sues (1986) as the exit of the lesser palatine nerve. We submit that the velum did not extend posteriorly beyond this point. Small remnants of interpterygoid vacuities are retained in the adult skull of

Kayentatherium (MCZ 8812, AWC, personal observation). A prominent dentary angle and rod of postdentary bones served as areas of insertion of the pterygoideus muscle.

Ictidosauria

The infraorder Ictidosauria was established by Broom (1932). Subsequently several taxa have been included in this clade (Crompton 1958; Sidor and Hancox 2006; Martinelli and Rougier 2007; Liu and Olsen 2010). Martinelli et al. (2016) place all the late Triassic non-mammalian eucynodonts within the clade Prozostrodontia. These authors agree that the prozostrodont, Brasilitherium is closely related to Mammaliaformes. Bonaparte and

Crompton (Bonaparte and Crompton 2018) retain the clade Ictidosauria and divide it into two families, Tritheledontidae and Therioherpetidae. The former encompasses the classic 27

ictidosaurs or “tritheledonts” while the latter includes a series of small slender forms such as Prozostrodon, Therioherpeton, Brasilodon, and Brasilitherium.

Brasilitherium (Fig. 11)

The description and reconstruction of the palate of Brasilitherium given below is based upon CT scans of UFRGS-PV1043-T (Bonaparte et al 2012) and figures and descriptions of UFRGS-PV 0929T (Bonaparte et al 2003; Bonaparte et al 2005).

Tall bulbous pterygoid bosses are a distinctive feature of the palate of

Brasilitherium. In contrast to those of non-mammalian cynodonts and tritylodontids, they extend forward in the form of ridges all the way to the lateral edges of the internal choana.

The medial edge of the pterygoid forms the lateral border of a small interpterygoid vacuity.

In Brasilitherium, in contrast to epi- and eucynodonts, the lateral surface of the pterygoid boss is contiguous with the lateral surface of the pterygoid posterior to the transverse process of the pterygoid. A series of transverse sections through the pterygoid region (Fig.

10d) illustrates this continuity. Section i cuts through the transverse process of the pterygoid and shows the anterior portion of the pterygopalatine ridges on the sloping medial wall of the transverse process of the pterygoid. Section ii cuts through the pterygoid bosses and shows that their lateral surfaces are contiguous with the ventrolateral surfaces of the pterygoid. 28

We suggest that a soft palate extended back from the palatine, supported laterally by the pterygopalatine bosses and ridges, and formed a floor to the nasopharynx. A slip of the medial portion of the reptilian pterygoideus muscle could have migrated unimpeded onto the boss’ lateral surface. Fibers of this slip (Fig. 10, mppp) may have extended around the ventral edge of the boss and entered the soft palate. Though these may not have functioned as the tensor veli palatini does in therians, this slip may have passed medially over the ventral surface of the boss similar to the way in which the tensor veli palatini in therians passes under the pterygoid hamuli to enter the soft palate.

The airway passed into the pharynx between the pterygopalatine bosses and above the soft palate (arrow labeled af in Fig. 10a). We propose that the bulk of the lateral portion of the pterygoideus muscle retained its origin on the tall descending flange of the transverse process and inserted on the reduced postdentary rod and the angle of the dentary (Fig. 8), whereas the posterior slip of the medial portion inserted on the retroarticular process.

Mammaliaformes

Morganucodon (Fig. 12)

The median region of the palate of Morganucodon oehleri, (Kermack et al 1981, Fig.

51, p. 59) is relatively well preserved, while the ventral surface of the specimen we studied

(IVPP 8682) is slightly damaged by mechanical preparation. Our reconstruction combines the best-preserved features of the two specimens. 29

The structure of the palate of Morganucodon closely resembles that of

Brasilitherium. Tall pterygopalatine ridges reach the lateral corners of the internal choana and form the lateral borders of the nasopharynx. They extend further back than in

Brasilitherium and the basisphenoid extends further forwards between them. We agree with Kermack et al. (1981) that the posterior edge of the hard palate and the pterygopalatine ridges together supported a soft palate. A foramen for the lesser palatine nerve is present lateral to the choanal ridge on the palatine. A midline crest is also present, that Kermack et al. (1981) suggested is formed by a parasphenoid. The transverse processes of the pterygoid—to which Kermack et al. (1981) referred as pterygoid flanges— are, relative to those of ictidosaurs, reduced, and lack their tall descending flanges. Each has a concave lateral surface that abuts the coronoid bone. The large and slightly concave posterior surface of the transverse process most likely served as the origin for the lateral part of the pterygoideus muscle, with the medial portion originating on the lateral surface of the pterygopalatine ridge and a slip of this muscle extending into the soft palate. We could not recognize an ectopterygoid, but Kermack et al. (1981) associated it with a fragment of bone covering the lesser palatine foramen in Morganucodon oehleri .

DISCUSSION and CONCLUSIONS

Our thesis depends on a previously unrecognized homology between the pterygopalatine ridge of stem mammals and pterygoid hamulus in later mammals, which among other insights provides a more parsimonious transition from the reptilian 30

pterygoideus to the mammalian lateral and medial pterygoid, tensor veli palatini and tensor tympani muscles.

In the transition to mammals the transverse process of the pterygoid was reduced in size, eventually disappearing. The medial pterygoid muscle arose when the origin of lateral portion of the reptilian pterygoideus shifted its origin from the transverse process of the pterygoid to the lateral surface of the palatine in therians, and onto the basisphenoid in monotremes. In both clades its insertion remained on the mandibular angle.

The medial portion of the reptilian pterygoideus is retained as the tensor veli palatini and tensor tympani. The same branch of the mandibular nerve innervates these muscles and the medial pterygoid, supporting their derivation from a single muscle, i.e., the reptilian pterygoideus. The reptilian pseudotemporalis retained its origin on the alisphenoid and shifted its insertion from the surangular and medial surface of the coronoid process onto the articular process of the dentary when this process was formed in early mammals.

The palates of Brasilitherium, Morganucodon and the therian mammal Didelphis show some remarkable similarities. In Didelphis, the pterygoid hamulus and palatine form the lateral wall of the nasopharynx, and the soft palate stretches between the hamuli. The tensor veli palatini enters the soft palate below the ventral borders of the hamuli. In

Brasilitherium and Morganucodon the pterygopalatine bosses and ridges also form the lateral border of the nasopharynx. A soft palate was probably present between the ridges and bosses. 31

We propose that in early mammals, fibers of the medial portion of the reptilian pterygoideus extended its origin into the soft palate below the ridges, forming the tensor veli palatini. The rest of the medial portion of the pterygoideus was lost together with a massive reduction of the pterygoid, as the transverse processes receded and only the palatopharyngeal ridges remained. These ridges acted as a pulley for the new tensor; and the resulting stress, we suggest, led to the addition of a hook shaped hamulus on the ventral edge of the pterygopalatine ridge.

The ontogenetic profile of the pterygoid hamulus tends to support its evolution from the pterygopalatine ridges. The presence in some therians of two primordia during ontogeny, one for the pterygoid and one for the hamulus, probably represents the late addition of a hamulus to the ventral surface of the pterygoid rather than the migration of a separate membrane bone such as the ectopterygoid onto the ventral surface of a greatly reduced pterygoid. There is no evidence for an ectopterygoid in eucynodonts, tritylodontids, ictidosaurs or mammaliaforms.

Early mammals probably possessed pharyngeal constrictors as well as palatoglossus and palatopharyngeus muscles, all innervated by the vagus nerve.

A large gap in time separates early Norian Brasilitherium from the early mammals of the Jurassic. The split between placentals and marsupials must have occurred before the appearance of the earliest known placental, Juramaia, from the late to middle Jurassic (Luo et al 2011). As both marsupials and placentals suckle their young, this must have also been true for their common ancestor, which, we conclude, possessed a pterygoid hamulus, as 32

well as the tensor veli palatini and palatoglossus muscles required for the formation of a tight seal in the fauces region.

The earliest known monotreme is the Early Cretaceous Teinolophus trusleri (Rich et al 2016). Identification of this form as a monotreme is based upon the structure of the lower jaw and middle ear. These features in T. trusleri more closely resemble those of mammaliaforms and early therians than they do the homologous structures in extant monotremes. Brusatte and Luo (Brusatte and Luo 2016) determined that monotremes branched off from the mammalian tree before multituberculates and therians. This view is supported by the fact monotremes and therians modified the primitive cranial sidewall of ancestral mammaliaforms in fundamentally different ways (Crompton et al 2017a). In addition, evidence suggests (Rich et al 2005) that in the basal monotreme Teinolophos trusleri, the angular and articular/prearticular bones (homologous to the ectotympanic and malleus bones of the mammalian middle ear, respectively) retained their attachment to the lower jaw. This indicates that the definitive mammalian middle ear evolved independently in monotremes and therians (Rich et al 2005).

Miocene ornithorhynchids (Obdurodon, Archer et al 1993) possessed molars. These appear during the ontogeny of extant ornithorhynchids, but are replaced in adults by horny plates. This and the addition of keratinized pads on the back of the tongue and ventral surface of their long palatine provide a unique mechanism for breaking down small invertebrates. 33

Monotremes also lack features associated with suckling: nipples; pterygoid hamuli; and the fauces closing muscles, tensor veli palatini, and palatoglossus. They rely on licking rather than suckling to ingest milk.

Despite their lack of a tensor veli palatini, monotremes retain the tensor tympani. As both the tensor veli palatini and tensor tympani are present in therians, both are innervated by the same branch of the mandibular nerve, and both arose from the medial portion of the reptilian posterior pterygoideus, we suggest that both muscles were present in the common ancestor of monotremes and therians. This, in turn, would imply that the common ancestor of mammals and monotremes suckled their young. The loss of this ability in monotremes is related to the evolution of their unique feeding mechanism.

The diphyodont replacement pattern of mammals (single replacement of the milk dentition by incisors, canines and premolars, but no replacement of the molars) correlates with suckling in extant therians. Early ingestion of milk permits rapid cranial growth before the eruption of deciduous teeth (Hopson 1973; Luo et al 2004). Luo et al. have determined that the molars of Morganucodon were not replaced (Luo et al 2004).

The tooth replacement patterns of other mammaliaforms such as Sinoconodon vary, but all show a reduction in molar replacement, suggesting ingestion of maternal milk by the young. We hypothesize that they did not suckle, but rather ingested milk by sucking or licking. Because they lacked a pterygoid hamulus and retained the transverse process, we propose that the tensor veli palatini, tensor tympani, and medial pterygoid had not yet fully differentiated from the reptilian pterygoideus. Although in mammaliaforms a slip of the 34

lateral portion of the pterygoideus originated on the lateral surface of the pterygopalatine ridge, the bulk of the pterygoideus still originated on the transverse process and lateral surface of the pterygoid behind the transverse process.

Suckling first arose in mammals when the tensor veli palatini, tensor tympani, and medial pterygoid differentiated into individual muscles; and when the massive pterygoid bone of mammaliaforms was reduced to a small plate supporting a pterygoid hamulus.

These changes appear to have occurred in forms more advanced than mammaliaforms, and certainly in the common ancestor to Mammalia.

Monotremes either lost or never possessed the ability to suckle, and they modified the fauces region for the breakdown of small invertebrate prey. Backward expansion of the palatine separated the pterygoid hamulus from the remainder of the pterygoid. The tensor veli palatini together with the palatoglossus and long soft palate between the hamuli were lost or never developed. Monotremes employ a unique suction mechanism to ingest milk.

If the common ancestor of mammals lacked nipples, pterygoid hamuli and a fully differentiated tensor veli palatini, then their hatchlings relied on sucking to ingest milk as extant monotremes do. This in turn would imply that suckling arose for the first time in the common ancestor of therians. It will only be possible to resolve this issue when the palate of the earliest mammals has been discovered and described. 35

Captions to the Figures

Fig. 1 a, Midsagittal section through the head of Didelphis illustrates how liquid can be drawn into the oral

cavity when a seal is formed in the fauces region and intraoral pressure reduced through depression

of the tongue in front of the seal. b, When the seal is broken, the tongue moves liquid or food from the

oral cavity to the oropharynx. When the seal formed again milk is moved from the oropharynx to the

esophagus. c, Lateral view of the tongue and pharyngeal muscles in Didelphis

Fig. 2 a, Orientation of the of the tensor veli palatini (tvp), palatoglossus (pg) and medial pterygoid (mp)

muscles relative to the pterygoid hamulus (PH) in Didelphis. Stippled area indicates the origin of the

medial pterygoid. b, Ventral view of the palate of Didelphis to illustrate the origin of the tensor veli

palatini and medial pterygoid. The gap (ipv) between the presphenoid (PSP) and pterygoid may be a

remnant of the interpterygoid vacuity. The dentary (D) is not shown on the right side. c, Transverse

section through the anterior region of the soft palate of Monodelphis. The tensor veli palatini,

palatoglossus, and palatopharyngeus (pp) muscles enter the anterior soft palate (sp) between the

pterygoid hamuli. The mylohyoideus between the hemimandibles form a sling below the tongue (t)

Fig. 3 Monodelphis domestica. a, Transverse section through the bulbous cartilaginous pterygoid hamulus

(PH), nasopharyngeal passage (np), oral cavity (oc), tongue and basihyoid (BH) in a pouch-young

individual. b, Midline sagittal section of the same individual to illustrate a medial view of the

pterygoid, pterygoid hamulus, and tensor veli palatini. Vertical line (a) indicates the position of

section shown in a. c, Similar midline sagittal section in an adult Didelphis illustrates the pterygoid

hamulus in medial view

Fig. 4 a, Ventral view of the palate of a juvenile Ornithorhynchus. The pterygoid is covered by the long

palatine and lacks a pterygoid hamulus. The echidna pterygoid has no contact with the pterygoid but

its posterior dorsal edge articulates with the ventral edge of the descending flange of the

basisphenoid. The palatopharyngeus surrounds the posterior end of the nasopharynx (np). 36

b, transverse section through the soft palate and c, a more anterior transverse section through the

posterior soft palate of the same individual. Note that the pterygoid and descending flange of the

basisphenoid form the lateral wall of the nasopharyngeal passage

Fig. 5 a, Parasagittal section close to the midline through the pharyngeal region of a juvenile

Ornithorhynchus. Note the anterior portion of the stylohyoid is embedded in the posterior tongue and

the keratinized pad (ks) on the dorsal surface of the tongue. b, sagittal section through the anterior

pharyngeal region of an adult Ornithorhynchus. Vertical axis to scale but not the horizontal axis. Note

the deep oropharynx that extends backwards on either side of the soft palate that includes the

palatopharyngeus (sp/pp). The nasopharyngeal passage is divided by a bony septum (bd) that is

continued backwards by soft tissue (td), which only partially divides the nasopharyngeal passage. c

and d, transverse sections through the posterior pharyngeal region at the levels indicated by the two

vertical lines in vertical lines in b. Note the oropharynx on either side of the palatopharyngeus and

the stylohyoid within the body of the tongue

Fig. 6 Ventral view of the palate of Thrinaxodon after Barghusen (1986) illustrates his view of the position

of a velum (ve) that is supported by a ridge on the ectopterygoid and lateral edge of the transverse

process of the pterygoid; and the origin and insertion of the posterior pterygoideus muscle (ppm).

According to Allin (1975) and Barghusen (1986) the lateral edge of the pterygoideus muscle (dark

grey) gave rise to the tensor veli palatini and tensor tympani muscles while the medial portion (light

gray) was lost entirely in mammals. Dotted lines indicate the origin and insertion of the posterior

pterygoideus

Fig. 7 Thrinaxodon. a, Lateral view to illustrate the origin of the pterygoideus and pseudotemporalis

muscles (O1, O2, O3); b, ventral view to illustrate the position of the pterygopalatine bosses. Note that

the velum does not reach the ectopterygoid, that the bosses are separated from the sharp posterior

edge of the transverse process of the pterygoid by a shallow valley (v) and that the bosses are not

extended forward by a ridge but rather by a rounded edge; c, anterior view of the skull as seen as 37

seen from the position of the vertical dashed line (c) in a and b. Note that the bulk of the

pterygoideus muscle originates on the descending flanges (tp) of the transverse processes of the

pterygoid

Fig. 8 Medial views of the lower jaws of a, Thrinaxodon, b, Cynognathus, c, Brasilitherium, and d,

Morganucodon. Dotted areas indicate insertions of pseudotemporalis (ipst), pterygoideus lateral

(ilppm) and medial (imppm) portions of the posterior pterygoideus. Not to scale

Fig. 9 Massetognathus. a, lateral view of the orbital region. b, ventral view of the palate. Note that the

pterygopalatine ridge does not extend onto the ventral surface of the palatine. c, anterior view of the

skull as seen from a section marked with a dashed line in b. Note the sharp ridge (sr) between the

pterygopalatine ridge and the insertion of the posterior pterygoideus (O3) on the posterior surface of

the transverse process of the pterygoid

Fig. 10 Kayentatherium. a, lateral view of the pterygoid region. Note the lateral surface of both the pterygoid

and palatine (ccb) contact the coronoid of the lower jaw; b, ventral view. Note that the choanal crest

(chc) and velum (ve) terminate before the exit for the palatine nerve (pn); and the origin of the

posterior pterygoideus extends onto the ventral surface of the transverse process of the pterygoid

and lateral surface of the pterygopalatine ridge; c, view of the posterior surface of the transverse

process of the pterygoid looking forward

Fig. 11 Brasilitherium. a, Lateral view of the orbital region to indicate the origin of a median slip of the

pterygoideus (mppp) on the lateral surface of the pterygoid boss and the airflow medial to the

pterygoid boss (af). b, Ventral view to show the possible extension of a medial slip of the

pterygoideus (mppm) into soft palate (ve) between the pterygopalatine bosses and ridges. In

mammals this slip forms the tensor veli palatini. The lateral portion of the pterygoideus muscle

(lppm) originated on the descending flanges of the transverse process of the pterygoid. In mammals

this process is lost and its origin migrates onto the lateral border of the palatine to form the medial

pterygoid. c, Anterior view of the skull anterior to a section illustrated by a dashed line (c) in b. Note 38

the continuation of the insertion area for the medial slip of the pterygoideus (O3) from the

descending flange of the transverse process of the pterygoid onto the lateral surface of the

pterygopalatine boss (ptb). d, Three sections through the pterygoid. Sections ii and iii illustrate the

continuity of the lateral surface of the pterygoid bosses and lateral surface of the pterygoid behind

the transverse processes for the origin of a medial slip of the pterygoideus (mppp)

Fig. 12 Ventral view of the palate of Morganucodon

39

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Fig. 1 a palatine fauces

eustacian tube nasopharynx stylohyoid

larynx esophagus tongue oral cavity pterygoid hamulus oropharynx (=valleculae) hyoid bone b tensor veli palatini

palatopharyngeus

larynx esophagus tongue hyoid bone palatopharyngeal sphincter palatoglossus c 1 cm

hamulus tensor veli constrictor medial pterygoid palatini palato- palatoglossus pharyngeus digastric tongue stylohyoideus hyoglossus omohyoid genioglossus geniohyoid mylohyoid digastric thyrohyoid sternohyoid a c F emt OS

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Bone Bone (slice view) Connective tissue Muscle (lengthwise) Nerve/brain

Bone (cross-section) Cartilage Muscle (cross-fiber) Muscle origin Velum/Soft palate a b a

lp PS BO V t P PT np PT P m ppPH tvp tvp PH sp 1mm oc pg MC t c PS BS D mh t P tvp sm PH gh hp 1mm 1cm Fig. 4 a V b

AL

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MAL IN ST ECT SQ AL pit

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Fig. 5 Bone Muscle (lengthwise)

Tongue Cartilage Muscle (cross-fiber) or Connective tissue Fig. 6 chc P EC V P ve

PT lo ppr oppm ls ppm ippm qrp

AR Q ST Fig. 7 c a

P & PS

O1 qrp

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ppr PT tp ptb v sr c

O2 ppm PS

pa EP qrp

BO 1 cm Thrinaxodon Cynognathus

ipst ipst SA SA

SP rl PAR rp ippm ilppm Brasilitherium Morganucodon

itt imppm Fig 8 ilppm ilppm ma c Fig. 9 a b

OS EP P O2 ve tp chc PS PT P pf tp O 3 PT v c sr ppr O3 c OS O PS 2

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chc c

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