The following is adapted from a talk given by Catherine at the International Paleontology Conference in Paris, France, on July 10, 2018:
Tracing the shape of the pterygoid bone in the path leading to extant mammals reveals some intriguing stories about the evolution of suckling, the development of muscles from the reptilian pterygoideus, and key differences between the form and function of the fauces region in therians versus monotremes.
The fauces refer to a muscular arch that forms a variable seal between the oral cavity and the oropharynx, playing an important role in the transport of food through the oral cavity. Therian mammals close the fauces to form a seal between the oral cavity and oropharynx, essential for suckling. Suckling requires a tight seal closing the fauces. When the fauces’ seal is intact, depressing the tongue induces negative pressure and draws liquids into the oral cavity:
When the seal is broken, the tongue pushes liquid into the oropharynx.
The seal is established again and milk forced from the oropharynx into the esophagus by traveling either around the larynx in the piriform recesses or over the larynx by tilting the epiglottis to cover the entrance to the larynx. Milk can again be drawn into the oral cavity.
In mammals as this American opossum, a muscular soft palate stretches between the two pterygoid hamuli.
Four muscles participate in the sealing of the fauces in therians.
1. the tensor veli palatini tenses the soft palate
2. Shown below in yellow, the palatoglossus straddles and hoists the tongue up to the palate.
3. Intrinsic muscles of the tongue change its shape to elevate the posterior region against the soft palate
4. The mylohyoid stretches between hemimandibles around the base of the tongue, and serve to elevate the base of the tongue.
Incidentally, the medial pterygoid muscle (see below), originates on the lateral surface of the palatine above the pterygoid hamulus. This comes into play when we discuss the origin of the tensor veli palatini.
We wish to address the following questions:
1. When might suckling have become possible in the evolutionary path leading to mammals?
2. How and when did the tensor veli palatini and mammalian medial pterygoid muscles arrive in the line leading to mammals?
3. What are the main differences between the fauces regions of monotremes and therians?
In reptiles and non-mammalian cynodonts the jaw uses the transverse process of the pterygoid to guide its vertical opening and closing (see below right, left-most arrow). The fauces-closing muscles, tensor veli palatini and palatoglossus were still not present in a Triassic non-mammalian cynodont such as Thrinaxodon. But in reptiles the posterior pterygoideus is a major adductor that originates on the posterior surface of the transverse process of the pterygoid. In Thrinaxodon it similarly originated on the sharp ventral edge of the transverse process of the pterygoid. Close to the midline of the ventral surface of the pterygoid are two high bosses (circled in white, below), but no muscles could have attached to the ventral surface of the pterygoid bone. A sharp choanal crest on the posterior surface of the palatine supported a short non-muscular soft palate. It stopped short of the ectopterygoid (see below right, right-most arrow).
In Thrinaxodon, the pterygoideus does not reach the pterygo-palatine boss (see below, left) because there’s a sharp edge and a bony valley in the way. The first step in the origin of the muscles that close the fauces, and the pterygoid hamulus itself, occurs in Brasilitherium, the closest known relative to mammals (below, right). The pterygoid boss extends forward as a pterygopalatine ridge (below, right, outlined in red) all the way to the choana, and backwards beyond the transverse process. It has grown deep enough to support the lateral edge of a longer non muscular soft palate (shown on the opposite side in purple).
As the lateral surface pterygoid becomes contiguous with the lateral edge of the ridge, the origin of a slip of the medial portion of the pterygoideus migrates forwards onto the lateral surface of the pterygopalatine boss (below, circled in black). This is the critical step in the formation of the tensor veli palatini and the hamulus itself (the hamulus being preformed in cartilage as an result of the pressure placed upon it by the tensor veli palatini). The lateral portion of the pterygoideus still originates on the transverse process of the pterygoid, which is somewhat smaller than in Thrinaxodon but still contacts the lower jaw.
Tens of millions of years separated Brasilitherium from the first mammals, but it is clear how its palate was modified in therians (see below):
- The shape of the pterygo-palatine bosses and ridges are modified to form the hook shaped pterygoid hamulus (supporting the soft palate in purple, below right).
- The medial slip of the pterygoideus enters the soft palate to form the tensor veli palatini.
- As the transverse process of the pterygoid is lost, the origin of the lateral portion of the pterygoideus shifts on to the lateral surface of the palatine to form the mammalian medial pterygoid muscle. This view is in conflict with the current view that the reptilian pterygoideus was lost entirely except for a lateral slip claimed to have given rise to the tensor veli palatini; and the hamulus arose either from the lateral edge of the transverse process of the pterygoid or the ectopterygoid. We conclude that the tensor veli palatini was derived from a medial slip- not lateral- of the pterygoideus; and that the lateral slip gave rise to the medial pterygoid.
In a recent letter to Nature, Huttenlocker et al. described a haramiyid mammaliaform which shows a marked reduction of the transverse process and a large hamulus coming off the pterygoid. Presumably in that form there was already a transition of the lateral portion of the pterygoideus to the palatine. Brasilitherium could certainly have formed a tight seal at the fauces, and therefore it’s possible that they suckled already.
This whole region is fundamentally altered in monotremes.
Monotremes have radically changed the fauces region for the breakdown of food. The palatine has grown backwards, separating the hamulus from the pterygoid to form the echidna pterygoid, which remains connected to the soft palate but no longer is involved with tensing it. The tensor veli palatini is lost, and the palatoglossus is either lost or never was present. In addition, a process on the lower jaw supports an enormous posterior mylohyoid.
Below is a sagittal section through the fauces region of a platypus hatchling. Keratinous pads grow on both the tongue surface and on the ventral surface below the palatine. The stylohyoid is embedded in the tongue, unlike therians. The mylohyoid is huge. Together the mylohyoid and the stylohyoideus muscle attached to the stylohyoid, elevate the tongue’s keratinous pad to the palate’s for the effective break down of invertebrates. The exoskeletons are shifted laterally to the oral pockets, and what’s left moves into the oropharynx. When it is full, the food is then transported to the esophagus as in therian mammals.
In addition to the keratinous pads on the tongue and palate, the extant platypus has given up the classic way of breaking down food with molars, and replaced the molars with horny pads. Below are some scans of a hatchling with teeth (top), that in adults (bottom) are replaced by horny pads.
The effectiveness of the horny pads is augmented by the orientation of the medial pterygoid (see below). Its origin has migrated from the palatine onto the basisphenoid above the palatine. Unilateral activity of the medial pteryoid shifts the lower jaw sideways, enabling the horny pads to break down food.
- The reptilian pterygoideus gave rise to the tensor veli palatini and mammalian medial pterygoid.
- The pterygopalatine ridge gave rise to the pterygoid hamulus.
- Monotremes changed the whole fauces region for the breakdown of invertebrates, rather than forming a seal.
To make a long story short, monotremes don't suck!