Origin of the pterygoid bone and pharyngeal musculature in mammals

The following is adapted from a presentation given at the Berlin meeting of the Society of Vertebrate Paleontology in November 2014 by Dr. AW Crompton.  

 

Living reptiles lack pharyngeal muscles. This was probably also true for primitive synapsids, or "mammal-like reptiles". Mammals on the other hand possess a complex array of pharyngeal muscles that play an important role in feeding, suckling, and control of water and heat.Presentation to Berlin meeting of Society of Vertebrate Paleontology, November, 2014

Before launching into our findings, a brief discussion of the anatomy and function of three pharyngeal muscles will be helpful. These muscles are illustrated below in a sagittal section through the head of an opossum.

First, the palatopharyngeus (shown in bright red) originates in the hard palate and pterygoid hamulus region and embeds in the soft palate to form the floor of the nasopharynx. The nasopharyngeal sphincter in this muscle surrounds the larynx, holding it in an intranarial position (except in humans).  The larynx withdraws from this position during swallowing, vocalization, or panting. At rest, inhaled and exhaled air to and from the lungs follows the same path, sealed off from the oral cavity (shown by the double arrows). This single passage for both inhaled and exhaled air is an essential aspect of endothermy.  Maxilloturbinates act as temporal counter-current exchange sites and thereby conserve water and heat in terrestrial mammals inhabiting dry or cold environments.  Pharyngeal muscles in an opossum

Second, the tensor veli palatini  (shown in blue), embeds in the soft palate between the pterygoid hamuli.

Third, the palatoglossus muscle (shown in yellow) links the lateral surface of the tongue to the soft palate. It forms the palatopharyngeal arch at the fauces (black ring).  The tensor veli palatini and palatoglossus act, together with the tongue, to form a variable seal that controls transport of liquid and solid food from the oral cavity to the oropharynx and then to the esophagus. 

These muscles play an essential role in suckling. 

It is important to note that the oropharyngeal region is divided into several compartments: oral cavity, oropharynx, nasopharynx and Eustachian tube.

The first sign of pharyngeal muscles occurs in an early Triassic non-mammalian cynodont.  The image above compares the palatal region of one such cynodont and a mammal, the opossum. There is some controversy as to the homologies of the large pterygoid, that contacts the lower jaw in therapsids, and the delicate pterygoid hamulus in mammals. It has been suggested that the dorsal part of the pterygoid is a remnant of the cynodont pterygoid, and the ventral part is a surviving ectopterygoid. This view has been widely accepted, but as the ectopterygoid is lost in all advanced cynodonts, it is unlikely. Others have suggested that the hamulus is a remnant of the transverse process of the pterygoid. Our view is that the mammalian pterygoid hamulus derives from the prominent pterygo-palatine ridges on the roof of the large internal nares. These extend backward and converge from the lateral edges of the hard palate. The steep medial wall of these ridges form the lateral walls of a dome shaped nasopharynx similar to the role played by the hamuli in mammals. We agree that pterygopalatine ridges supported a soft palate that covered the large internal nares, as shown in yellow in this slide.

Mid-sagittal section through the skull of an early cynodont

In this mid-sagittal section through the skull of the same early cynodont (above, top right), the pterygo-palatine ridge (red) is shown supporting a soft palate  (shown in yellow) that formed the floor to a relatively shallow nasopharynx. A foramen must pass through such a soft palate, here seen in ventral view (above, left), for communication between the nasopharynx and the oral cavity.  In birds this foramen manifests simply as a slit in the non-muscular soft palate, but there is an obvious advantage if the opening and closing of the aperture can be controlled (open during breathing and closed during a swallow). We suggest fibers of a palatopharyngeal muscle were added to the soft palate at this stage. Fibers of this muscle shown in red probably surrounded a palatopharyngeal sphincter as they do in extant mammals. This sphincter was situated below the converging end of the pterygopalatine ridges and a glottis was positioned below this point. A comparison of a mid-sagittal section through the head of a mammal and a lizard (above, bottom right) supports this view.

In the squamates, the oral cavity, pharynx and tympanic cavity medial to the eardrum form a continuous space. In cynodonts the large post dentary bones were involved in sound conduction and they therefore formed  a lateral wall to a large tympanic cavity opening into a communal pharynx/oral cavity.  A division of the oro-pharyngeal area had not yet occurred.

 

Adductor muscles

"What about the adductor muscles?" you may ask. In squamates, the pterygoideus muscle is made up of several sub-sections. We suggest that this was also true for early cynodonts with one section originating from the posterior edge of the transverse process of the pterygoid and the other from the lateral surface of the pterygoid (shown above, in orange and red in this figure). There is general agreement that in the mammal-like reptile/mammalian transition the massive reptilian pterygoideus muscle is reduced to a tensor veli palatini, which hooks around the ventral edge of hamulus to insert in the anterior part of the soft palate, and a tensor tympani that inserts on the malleus. The first step in this transition is preserved in late Triassic mammal-like reptiles.

Ictidosaur features

An advanced group of therapsids, now relatively well-known, come from the late Triassic and early Jurassic of South Africa and South America.  For convenience we refer to them as “Ictidosaurs”, but they are also often referred to as Trithelodonts or Brasilidonts. The taxon illustrated above is Pachygenelus. They all share several distinguishing features:

  1. They retain a contact between the lower jaw and the transverse process of the pterygoid (black circle);
  2. They show a marked reduction in size of the postdentary bones and reduced space for pterygoideus musculature;
  3. The pterygopalatine ridges are long, slender and tall and are directed towards the medial edge of the internal nares;
  4. These form lateral walls to a deep nasopharynx as the hamulus does in mammals;
  5. There is a deep concavity between the transverse process and the hamulus, as shown in the transverse section above.

We suggest that the medial part of the reptilian pterygoideus migrated from the posterior edge of the transverse process of the pterygoid into this concavity and probably lapped over the ventral edge of the pterygopalatine ridge to enter a soft palate as the tensor veli palatini muscles as it does in mammals.

Mammal vs Pachygenelus transverseGiven how similar transverse sections (above) appear through the same region of the head in Ictidosaurs and mammals, we suggests a palatoglossus muscle contributing to a palatopharyngeal arch or fauces may also have been present. There is some additional support for this view. In mammals food is held in the oral cavity by the palatopharyngeal seal until it is masticated and broken down to a desirable consistency; and only then passes through the fauces to the oropharynx. This not true for typical reptiles where food is not broken down by repeated jaw closings. In carnivorous non-mammalian cynodonts such as Thrinaxodon, Probelesodon and Probainognathus, extensive wear facets are absent on the postcanine teeth. However, Pachygenelus and other “Ictidosaurs” show well developed wear facets on their postcanine teeth, that were repeatedly replaced. This suggests that food was masticated and a palatopharyngeal arch would have been necessary to control food transport through the fauces to the oropharynx. The palatoglossus may have arisen syncronously with mastication in advanced mammal-like reptiles. 

Morganucodon DVNew information has recently been obtained on the palatal region of the mammaliaform, Morganucodon (above). Here the pterygoid is reduced in size and still contacts the lower jaw while the pterygopalatine ridge or hamulus lies entirely within the pterygoid bone. This strengthens the view that it functioned as a hamulus. Other than this the palate essentially resembles that of Pachygenelus. Morganucodontids are characterized by a mammalian tooth replacement pattern (i.e. a single replacement incisors, canines and milk molars). As this is associated with definitive growth and suckling in mammals it suggests that mammaliformes suckled their young. Again, this would not have been possible without a full complement of mammalian pharyngeal muscles. 

Therapsid radiation

The forms we have discussed all date from the late Triassic (see Therapsid radiation, above).  Mammals diversified rapidly during the late Jurassic and early Cretaceous; but the earliest known bony palate dates from the middle to late Cretaceous, in a multituberculate known as Kryptobataar. Some 100 million years separates Kryptobataar from the late Triassic synapsids.

Kryptobataar vs modern mammal, DidelphisIn Kryptobataar (above), the palate is fully mammalian and all contact between the pterygoid and lower jaw is lost. I think it is fairly safe to predict that when the palates of earlier, middle Jurassic mammals are found they will also prove to be fully mammalian. This may also be found to be true of enigmatic Docodonts that lived at the same time as the early mammals.

Conclusions

  1. A palatopharyngeal muscle was incorporated in the soft palate in early Triassic nonmammalian cynodonts;
  2. In late Triassic ictidosaurs the pterygopalatine ridge increased in length and height;
  3. Tensor veli palatini and palatoglossal muscles were added and
  4. Differential transport of food through the fauces became possible.
  5. Suckling was introduced in late Triassic mammaliformes.
  6. Mammals of the middle Jurassic were characterized by a dramatic reduction in the size of the pterygoid bone. Maxilloturbinates ossified.  Water and heat loss were finally efficiently controlled.