Wang et al. 2021: Vilevolodon had monotreme-like ear bones

We’ve heard this before.
Links below.

From the Wang et al. 2021 abstract:
“Recent discoveries of well-preserved Mesozoic mammals have provided glimpses into the transition from the dual (masticatory and auditory) to the single auditory function for the ossicles, which is now widely accepted to have occurred at least three times in mammal evolution.”

Wang et al. are not working from a valid phylogenetic context. They are not considering the possibility, hypothesized in the large reptile tree (LRT, 1593+ taxa) of a phylogenetic reversal in which the inner ear bones, which recapitulate phylogeny during embryonic ontogeny in placentals, could have stopped developing and stopped migrating to the typical placental position posterior to the mandible.

“Here we report a skull and postcranium that we refer to the haramiyidan Vilevolodon diplomylos (dating to the Middle Jurassic epoch (160 million years ago)) and that shows excellent preservation of the malleus, incus and ectotympanic (which supports the tympanic membrane).

See figure 1. We covered this issue earlier here, here and here.

Figure 1. Basal mammals and Vilevolodon as figured by Meng et al. Note in the other taxa the two jaw joints are nearly coincident. Not so in Vilevolodon.

Figure 1. Basal mammals and Vilevolodon as figured by Meng et al. Note in the other taxa the two jaw joints are nearly coincident. Not so in Vilevolodon.

From the Wang et al. abstract (continued)
“After comparing this fossil with other Mesozoic and extant mammals, we propose that the overlapping incudomallear articulation found in this and other Mesozoic fossils, in extant monotremes and in early ontogeny in extant marsupials and placentals is a morphology that evolved in several groups of mammals in the transition from the dual to the single function for the ossicles.”

Unfortunately
Wang et al. are pinning all their phylogenetic hopes on the inner ear bones. Therefore they are  “Pulling a Larry Martin.” Don’t do that. When placed into a phylogenetic analysis that considers traits from the entire skeleton and a wide gamut of mammals and pre-mammals, Vilevolodon nests within the placental clade Glires (the gnawers = rodents, rabbits, shrews, aye-ayes, multituberculates, etc.) We’ve known this for several years.

Wang et al. 2021 provide four prior analyses
in their SuppData, (references below) all of which employ suprageneric taxa, none of which test pertinent members of Glires.

In summary:
When tested against more taxa Vilevolodon is recovered as a derived member of Glires (rodents, rabbits, shrews, etc.) sharing with other multituberculates a neotonous retention of the embryonic condition, prior to the migration of the inner ear bones to the base of the skull, posterior to the mandibles. Evidently in their typical adult placental position typical ear bones interfered with the long slide of the mandible during gnawing and mastication, so retained the embryonic condition. The authors noted this ‘transition” in placentals in their abstract, but did not consider the possibility of a reversal or neotony.


References
Han G, Mao F, Bi S., Wang Y and Meng JA2017. Jurassic gliding euharamiyidan mammal with an ear of five auditory bones. Nature 551, 451–456.
Luo Z.-X. et al. 2017. New evidence for mammaliaform ear evolution and feeding adaptation in a Jurassic ecosystem. Nature 548, 326–329.
Wang H, Meng J and Wang Y 2019. Cretaceous fossil reveals a new pattern in mammalian middle ear evolution. Nature 576, 102–105.
Wang J, Wible JR, Guo B. et al. 2021. A monotreme-like auditory apparatus in a Middle Jurassic haramiyidan. Nature. https://doi.org/10.1038/s41586-020-03137-z

Hyomandibular evolution + Introducing the postsquamosal

Revised July 19, 2020
with new bone identities given to several lobefin fish, correcting the mistakes of Thomson 1966.

The hyomandbular is the largest bone
in the entire body of the basal ray-finned fish Trachinocephalus (Fig. 1). Over time and phylogeny it evolves to become the smallest bone in the human body, the stapes (Fig. 3), one of the ultra tiny sound-conducting bones of the middle ear.

Along the way,
the large reptile tree (LRT, 1656+ taxa) presents a new (and heretical) lineage of tetrapod ancestry, distinct from the traditional one that includes Ichthyostega and Acanthostega. Today we go below the surface and formally introduce ‘the lineup.’

Figure 1. Hyomandibular evolution from the first dichotomy of bony fish to Gephyrostegus. The hyomandibular evolves to become the stapes. Note the hyomandibula contact with the intertemporal, quadrate and pterygoid, sometimes fused to these bones. The hyomandibular is poorly ossified in Onychodus, so it restored here. Note how the maxilla splits to produce the quadratojugal.

Figure 1. Hyomandibular evolution from the first dichotomy of bony fish to Gephyrostegus. The hyomandibular evolves to become the stapes. Note the hyomandibula contact with the intertemporal, quadrate and pterygoid, sometimes fused to these bones. The hyomandibular is poorly ossified in Onychodus, so it restored here. Note how the maxilla splits to produce the quadratojugal.

Some bones are relabeled
from the diagram found in Thomson 1966 (modified in Fig. 2), who presented several layers of skull bones (cranial, palatal and dermal) in the the Permian megalichthyid rhipidistian fish, Ectosteorhachis, a late-survivor of an earlier (Mid-Devonian) radiation that ultimately produced tetrapods and humans. Thomson mislabeled the dentary as a maxilla (mx) in his diagram, but all other labels are traditional.

In most fish 
the hyomandibular is roofed over by the otherwise unremarkable intertemporal, which anchors it dorsally.

That brings up a problem in Thomson’s diagram
(Fig. 2). To remedy that problem, here the dorsal rim of the traditional palatoquadrate is relabeled as the hyomandibular fused to the pterygoid and other palatal elements. Second, the labeled hyomandibular (h) is now the preopercular. Third, the traditional preopercular (pop) requires a new name: the postsquamosal. It is not homologous with the preopercular of teleost fish.

The disappearance of the traditional preopercular
Trachinocephalus (Fig. 1) retains a traditional preopercular. Pteronisculus (Fig. 1) has a postsquamosal and lacks a traditional preopercular on the surface. Cheirolepis (Fig. 1) lacks both. The squamosal and postsquamosal appear to be fused or else the tiny postsquamosal is overwhelmed by the advancing squamosal. The traditional rhipidistians have a postsquamosal. The tetrapods (Fig. 1) lack a postsquamosal.

The more derived traditional transitional tetrapods,
Acanthostega and Ichthyostega, have a postsquamosal, but this appears as a reversal, a neotonous trait. These two are secondarily more aquatic than their ancestor, Ossinodus.

Figure 2. Ectosteorhachis skull from Thomson 1966 with layers to show the brain case and palatoquadrate. Some bones are relabeled in the revised view.

Figure 2. Ectosteorhachis skull from Thomson 1966 with layers to show the brain case and palatoquadrate. Some bones are relabeled in the revised view.

The hyomandibular decreases in size
in most later tetrapods (Fig. 3), where it continues to shrink into the auditory channel where it is then known as the stapes.

At the same time, the intertemporal
disappears or fuses to nearby skull bones in several derived basal tetrapods and basal reptiles, all by convergence.

Figure 4. Evolution of the tetrapod mandible and ear bones leading to humans.

Figure 4. Evolution of the tetrapod mandible and ear bones leading to humans in lateral and medial views, first printed in From The Beginning, the Story of Human Evolution (Peters 1991), colors added here.

The quadratojugal first appears in the tetrapod lineage
in Gogonasus (Fig. 1) after the elongate maxilla of Onychodus splits in two.

Finally,
sharks also have a palatoquadrate, but it is composed of a fused lacrimal, jugal and squamosal with a tooth-bearing premaxilla and maxilla fused to the ventral rim. The pseudo- or plesio-palatoquadrate illustrated by Thomson 1966 in Ectosteorhachis and other rhipidistians,is not homologous and is comprised of different bones. 


References
Thomson KS 1966. The evolution of the tetrapod middle ear in the rhipidistian-amphibian transition. American Zoologist 6:379–397.

Where are the auditory bullae in desmostylians?

A reader wondered about
tympanic (auditory) bullae (ear container bones) in desmostylians. Then I wondered, too. All whales are famous for having them. Nobody talks about them in desmostylans. So what gives? Here are the data:

Short answer:
apparently bullae are easily knocked off and/or ignored during the process of fossilization and extraction, both in mysticetes and desmostylians. Some examples follow:

Gray whale (Eschrichtius)
Bullae were present, but somehow got knocked off when it came time to draw the diagram (Fig. 1).

Figure 1. Gray whale (genus: Eschrichtius) in which bullae were present, but omitted from a palate diagram.

Figure 1. Gray whale (genus: Eschrichtius) in which bullae were present, but omitted from a palate diagram.

Cornwallius (a pre-desmostylian cambaythere) — overlooked bulla, called a ‘mass’ in the text.

Figure 3. The pre-desmostylian Cornwallius. Here the tympanic bulla (bright green) was considered "a mass" in the text and otherwise was not labeled.

Figure 3. The pre-desmostylian Cornwallius. Here the tympanic bulla (bright green) was considered “a mass” in the text and otherwise not labeled.

Neoparadoxia (basal desmostylian)
Here you can see the depression that receives the bullae, but the bullae became missing at some stage in the process.

Figure 3. Palate of Neoparadoxia, a basal desmostylian, apparently missing the tympanic bullae (ear bones).

Figure 3. Palate of Neoparadoxia, a basal desmostylian, apparently missing the tympanic bullae (ear bones). Note the ear canal bones extending laterally, as in the hippo (figure 6).

Desmostylus, a derived desmostylian close to right whales
Same here. Bulla not published. Depression for the reception still present.

Figure 4. Desmostylus with missing bullae replaced in the empty spots left behind.

Figure 4. Desmostylus with missing bullae replaced in the empty spots left behind. Skull is obviously distorted and missing a big part of the cranium.

Caperea, a basal right whale
Here’s an odd one. Not sure what happened to the bulla in ventral view. They seem to appear in occiput view.

Figure 6. Caperea, a basal right whale, apparently missing the bullae in palate view that it had in occipital view.

Figure 5. Caperea, a basal right whale, apparently missing the bullae in palate view that it had in occipital view. If not, please advise.

Hippopotamus
This goes back somewhat on the tree, but hippos are in the lineage of baleen whales in the LRT and their auditory bones are present.

Figure 7. Hippopotamus with auditory meatus (ear canal) in green, bulla (ear bone container bones) in yellow.

Figure 6. Hippopotamus with auditory meatus (ear canal) in green, bulla (ear bone container bones) in yellow.

Ear bones compared
Baleen whale bullae greatly resemble toothed whale bullae. It’s true. Based on phylogeny, we’ll have to call this convergence. So is the loss of teeth in the rostrum of the sperm whale and blue whale. Convergence happens, but let’s keep an eye out for those bullae, now that we know what should be there.

The comings and goings of archosauromorph ears

You may recall that all living and extinct reptiles can be divided into two clades, the new Archosauromorpha and the new Lepidosauromorpha. Yesterday we looked at lepidosauromorph ears. Today we’ll examine archosauromorph ears.

The ear in three living archosauromorphs, crocs, mammals and birds.

Figure 1. The ear in three living archosauromorphs, crocs, mammals and birds. The ear flap seen in crocs and the platypus is by convergence, perhaps to keep the water out.

Living members of the new Archosauromorpha (Fig. 1, crocs, birds and mammals) all have well-developed ears, but only higher mammals have the erect external ears we typically think of.

At the base of the Archosauromorpha we don’t see evidence for ears. The stapes, the first and typically (except in mammals) the only ear bone, tends to be robust, helping to support the jaws. That evidence for an eardrum frame first appears in basal therapsids as a creation of an angular flange that thereafter thins to become a gracile encircling eardrum frame (Fig. 2). In higher mammals the

Reptile Ears, basal Archosauromorpha. If external ears were present, they did not leave any obvious frame, as in lepidosauromorpha.  Basal therapsids developed an eardrum frame derived from the angular bone.

Figure 2. Reptile Ears, basal Archosauromorpha. If external ears were present, they did not leave any obvious frame at the back of the skull, as in lepidosauromorphs. Basal therapsids developed an eardrum frame derived from the angular bone. Some workers think the large stapes in basal reptiles did not permit sound reception. Others think the large stapes supported a very large eardrum not otherwise supported (not sure how that could be kept taut).

There is likewise not much of a clue in basal diapsids with regard to their hearing. We skip the enaliosaurs, which were underwater creatures and don’t see a lepidosauromorph-like eardrum frame on any taxa before protorosaurs like Czatkowiella (Fig. 3) and perhaps some younginids, but data is sparse on them at present. Prehistoric crocs and dinosaurs probably developed like living crocs and birds.

Reptile eardrums - diapsids, crocs and birds.

Figure 3. Reptile eardrums – diapsids, crocs and birds. No marine reptiles of the clade Enaliosauria are included because no clear evidence for ears appears in that underwater clade. Crocs have ears higher on the skull than birds. All other eardrum placements are guesses. Like lepidosauromorphs the squamosal appears to have framed the eardrum at the back of the skull as shown.

Bird middle ear cross section. The stapes is the only bone in the link.

Figure 5. Bird middle ear cross section. The stapes is the only bone in the auditory link.

The more birdy or croc-like a taxon gets, the easier it seems to be able to imagine an eardrum framed at the back of the skull and deeper than at the surface.

Here, if anyone has additional data, I will gladly add it later.

The comings and goings of lepidosauromorph ears

Lepidosauromorph (lizard and turtle) eardrums
Sometimes the turtle or lepidosaur eardrum is flush with the surface. Sometimes there’s a deeper eardrum just below the surface or deeper still, almost invisible in a hole or in a slit. In snakes and other burrowing and marine reptiles there’s typically no trace of an external ear.

[We’ll talk about the archosauromorph (mammals, birds and crocs) eardrums in a later post.]

Back, back, back to the otic notch
The famous “otic notch”  has traditionally been considered the site of the eardrum of prehistoric amphibians like Silvanerpeton and Gephyrostegus. That’s where frog eardrums are located and it is assumed the same held true for many other prehistoric amphibians with this trait. (More below.)

Reptile eardrums - here the reduction of the otic notch is demonstrated from Silvanerpeton to Gephyrostegus and Cephalerpeton, a basal lepidosauromorph reptile.

Reptile eardrums – here the reduction of the otic notch is demonstrated from Silvanerpeton to Gephyrostegus and Cephalerpeton, a basal lepidosauromorph reptile.

Some prehistoric lepidosauromorphs also have an otic notch. Among other traits, this notch has caused some experts to consider, Diadectes, for instance, to be a pre-reptile. Now we know that Diadectes nests well within the Reptilia in the large reptile tree. Ironically a similar notch is found in the related and much later appearing Procolophon, which paleontologists universally consider a reptile. But the connection between the two has never been recognized except here.

Reptile eardrums in Diadectes and Procolophon

Figure 2. Reptile eardrums in Diadectes and Procolophon

Earliest reptile eardrums?
2007 news event following publication of Bashkyroleter, a macroleterid (not procolophonid!) with a very large eardrum frame, prompted this post.

In that case, Müller and Tsuji (2007)  reported, “the presence of true tympanic ears has never been recorded in a Paleozoic amniote, suggesting they evolved fairly recently in amniote history. The configuration of the tympanic ear in these parareptiles is unique for amniotes in that it is not the quadrate as in other reptiles, or the tympanic (angular) as in mammals, but the squamosal and the quadratojugal to which the main parts of the tympanum are connected.

To their point,
one of the hallmarks of early reptiles is the disappearance of the otic notch, as seen tentatively in Cephalerpeton and more fully in captorhinids. The squamosal posterior rim changes from concave with an overhanging supratemporal in Gephyrostegus to straight to slightly convex at the top in Concordia. Such a change signals the diminution of the large surface eardrum in taxa without an otic notch.

Reptile eardrums. Basal lepidosauromorphs in phylogenetic order.

Figure 3. Reptile eardrums. Basal lepidosauromorphs in phylogenetic order.

A tiny notch reappears at the base of the squamosal where it meets the rising quadratojugal in Milleretta and its descendants, Acleistorhinus and Eunotosaurus.

A more Concordia-like arrangement extends to TseajaiaSolenodonsaurus, and their chroniosuchid kin, along with Orobates and its descendants. An indentation of the squamosal reappears in Diadectes and the lineage of turtles and also in Macroleter and the above mentioned Bashkyroleter and kin.

Reptile eardrums Mid-lepidosauromorpha in phylogenetic order.

Figure 4. Reptile eardrums Mid-lepidosauromorpha in phylogenetic order.

Strangely a sister to Macroleter, Saurorictus, had virturally no identation. This appears to be an exception based on its small size, not the basal condition, contra Müller and Tsuji (2007). The phylogenetic tree provided by Müller and Tsuji (2007) does not match that of the large reptile tree.

Thereafter Macroleter and kin the embayment of the squamosal and quadratojugal remained deep moving through Emeroleter, Coletta, Sauropareion and other owenettids (not procolophonids!)

At the next step up the lepidosauromorph tree, with Paliguana the squamosal was greatly reduced and stayed that way within the clade of Kuehneosaurus through Xianglong, two of the gliding lizards. In these taxa the quadrate was concave posteriorly, perhaps taking over the function of the squamosal and quadratojugal.

Figure 5. Reptile eardrums among basal Lepidosauriformes

Figure 5. Reptile eardrums among basal Lepidosauriformes

Another lepidosauromorph branch leading to rhynchosaurs, trilophosaurs and sphenodontids retained a concave squamosal + quadratojugal and sometimes just a quadrate framing an eardrum (this is known only in the living Sphenodon, the rest are all extinct).

Reptile ears, living representatives

Figure 6 Reptile ears, living representatives.

A third branch of lepidosaurs leads to the tritosaurs and squamates including the living Iguana and Varanus. Living lizards demonstrate a wide variety of surface eardrums, slits, holes and the absence of external indications of ears (in Lanthanotus, snakes and burrowing lizards, for instance). In the Tritosauria, megalancosaurs and pterosaurs had straight quadrates so we imagine the external ear opening could only be a tall slit, perhaps bounded by the jaw adductor.

Figure 6. Reptile eardrums, Tritosaurs

Figure 6. Reptile eardrums, Tritosaurs, including tanystropheids and pterosaurs

A little more background from Wever 1978 on salamanders:
In vertebrates the auditory hair cels are immersed in fluid and are sensitive to displacements; in all vertebrates above the fishes, sound stimuli involve these cels only by mobilizing the inner ear fluids. This fluid mobilization ordinarily is achieved in one of two ways.

1. In birds and mammals and in a number of reptiles one wall of the inner ear capsule contains a round window, an opening covered by a thin membrane beyond which lies an air cavity. This window provides a place of pressure relief when vibratory sound pressures are exerted from the outside, usually by way of an external ear opening and a middle ear apparatus applied to the oval window of the cochlea. The fluid then is set in oscillation between oval and round windows: an inward displacement at the oval window is accompanied by an outward displacement of equal volume at the round window.

2. A second method of fluid mobilization is utilized in many of the reptiles, including turtles, snakes, amphisbaenians, Sphenodon, and a few species of lizards, which lack a round window. These use a reentrant fluidcircuit: a pathway leads inward from the footplate of the oval window and takes a roundabout course to the outer surface of this same foot plate, and the fluid surges back and forth along this pathway.

These two modes of fluid mobilization are both effective for their purpose, though the reentrant fluid circuit, because of the increased mass of fluid that must be set in motion, serves best for low tones and restricts the ear’s sensitivity to high tones.

To the point of the Wever 1978 paper: The Anura (frogs and toads) posses a round window and use the first solution mentioned. The Gymnophiona (caecilians) use a reentrant fluid circuit. In Caudata (salamanders) sound literally goes in one ear and out the other, unique among tetrapods. Sounds applied to the oval window of one ear produce a path of vibratory motion that passes through the brain cavity to the oval window on the opposite side.

But this is a blog about reptiles, so we’ll stop this discussion on that interesting note.

As always, I encourage readers to see specimens, make observations and come to your own conclusions. Test. Test. And test again.

Evidence and support in the form of nexus, pdf and jpeg files will be sent to all who request additional data.

References
Müller J, Tsuji LA 2007. Impedance-Matching Hearing in Paleozoic Reptiles: Evidence of Advanced Sensory Perception at an Early Stage of Amniote Evolution. PLoS ONE 2(9): e889. doi:10.1371/journal.pone.0000889
Wever EG 1978. Sound transmission in the salamander ear. PNAS 75(1):529-530.

Freed from their primitive function: posterior jaw bones become ear ossicles

 series of jaw bones demonstrating the gradual accumulation of traits that changed them into ear ossicles and an eardrum frame.

Figure 1. Click to enlarge. A series of jaw bones demonstrating the gradual accumulation of traits that changed them into ear ossicles and an eardrum frame. Largely from Allin 1975.

Today we’ll start a new series: Freed from their primitive function” in which we’ll look at various parts of the vertebrate anatomy that started off doing one thing, but ended up doing another. These are excellent examples of evolution.

Today we’ll look at the posterior jaw bones that started off articulating with the skull and ended up transmitting sound in mammals. It was first recognized as early as Reichert (1837) 20 years before Darwin’s “On the Origin of Species’ (1859) and subsequently confirmed and elaborated by several workers (e.g. Allin 1975, Kemp 2007). Reichert employed embryology and comparative anatomy as he reported in the developing mammalian embryo that the incus and malleus arise from the same first pharyngeal arch as the mandible and maxilla. (Which reminds us that before these were jaw bones they were gill rims!)

Allin (1975) drew on the several paleontological examples then known to more fully fill in the story (Fig. 1) demonstrating graphically the gradual rise and expansion of the coronoid process along with the reduction of the postdentary jaw bones. This series also demonstrates the evolution of the canine and molar teeth. The evolution of the angular (lower postdentary jaw bone) into a thin flange that encircled an open space then continued to reduce until it ultimately framed the eardrum. Allin (1975) suggested at an early stage the angular framed a very large eardrum. Later, Kemp (2007) thought the postdentary bones were too large and still functioning as jaw bones to allow this, suggesting instead that the eardrum formed in the earliest mammals when the articular became very much more gracile and smaller. The unusual anatomy of the postdentary bones would have supported ventral jaw muscles acting to open the jaws.

The moment of direct contact between the dentary and squamosal marks the origin of the Mammalia and permitted the postdentary bones to continue their evolution to become ear ossicles. Note that even in primitive mammals, like Asioryctes (Fig. 1), the postdentary bones continued a tenuous connection to the dentary that was finally disconnected in eutherian mammals.

It’s interesting to note that even as late as Homo sapiens the mandible was still evolving a chin, a feature not seen in prior taxa, including pre-human anthropoids.

As always, I encourage readers to see specimens, make observations and come to your own conclusions. Test. Test. And test again.

Evidence and support in the form of nexus, pdf and jpeg files will be sent to all who request additional data.

References
Reichert KB 1837. Über die Visceralbogen der Wirbelthiere im Allgemeinen und deren Metamorphosen bei den Vögeln und Säugethieren. Archiv für Anatomie, Physiologie und wissenschaftliche Medicin: 120-222.

Allin EF 1975. Evolution of the mammalian middle ear. Journal of Morphology 147 (4): 403–437. 

Kemp TS 2007. Accoustic transformer function of the postdentary bones and quadrate of a nonmammalian cynodont. Journal of Vertebrate Paleontology 27(2): 431-441.