Flying squirrels and aye-ayes: convergent with multituberculates

For those in a hurry, a two-part summary:
1. By convergence, basal multituberculates in the Jurassic (Figs. 1, 4), had a distinct  flying squirrel (Glaucomys, Figs. 2, 3)-like patagial (= gliding membrane) morphology.
2. Also by convergence, multituberculates in the Jurassic had a short post-dentary skull length with a sliding jaw joint and a nearly absent angular process as seen in the extant aye-aye (Daubentonia, Figs. 5, 6).

Figure 2. The paratype specimen of Arboroharamiya HG-M018, in situ. DGS color tracing added. The skull is in poor shape.

Figure 1. The paratype specimen of Arboroharamiya HG-M018, in situ. DGS color tracing added. The skull is in poor shape.

Today’s blogpost had its genesis
when I finally noticed several basal multituberculates that preserved soft tissue had flying-squirrel-like patagia preserved in the sediment (Fig. 1)… and squirrels nested more or less close to the origin of multituberculates. So, I added a flying squirrel, Glaucomys (Fig. 1) to the large reptile tree (LRT, 1810+ taxa) to see what would happen.

It should come as no surprise
that Glaucomys nested with the extant red squirrel Sciurus, NOT any closer to multituberculates. Thus, the ability to glide in the manner of a flying squirrel turned out to be by convergence in basal multituberculates of the Jurassic.

Figure 2. Glaucomys gliding.

Figure 2. Glaucomys gliding.

Figure 2. Multituberculates to scale. Carpolestes is the proximal outgroup taxon.

Figure 3. Multituberculates to scale. Carpolestes is the proximal outgroup taxon.

Based on the phylogenetic position
of squirrels and other rodents as sisters to multituberculates, either flying squirrels were also gliding from tree-to-tree during the Mesozoic, or they took their time and only appeared after the Mesozoic. That is the current paradigm based on present evidence.

End of part 1. Scroll down for part 2.

Figure 1. Subset of the LRT focusing on basal placentals, including multituberculates.

Figure 4. Subset of the LRT focusing on basal placentals, including multituberculates.

Part 2.
By convergence, the aye-aye, Daubentonia

(Fig. 5) has a multituberculate-like mandible lacking an angular process along with a large circumference, sliding jaw joint and reduced post-dentary skull.

Figure 1. Taxa in the lineage of Daubentonia and multituberculates.

Figure 5. Taxa in the lineage of Daubentonia and multituberculates. Note the loss of the angular process and the sliding jaw joint.

By convergence, Carpolestes
has an enlarged posterior lower premolar, as in multituberculates. So, lots of convergence surrounds the multituberculates.

The aye-aye is a traditional basal primate,
based on gene studies (Dene et al1980; Rurnpler et al 1988; Del Pero et al 1995; Porter et al 1995).

By contrast
the large reptile tree (LRT, 1810+ taxa; subset Fig. 4) nests the aye-aye (Daubentonia) with rodents, plesiadapiformes, carpolestids and multituberculates. We’ve seen how genomic studies produce false positives. Add Daubentonia to that list of flubs. Note that both lemurs and aye-ayes are both from Madagascar, lending more evidence to the hypothesis that geography and geology (e.g. Afrotheria, Laurasiatheria) affect genomics to a greater degree than professionally realized over deep time.

Like rodents:
The aye-aye does not have mammary glands on the chest, as in primates, but along the groin, as in non-primates. The aye-aye has a large diastema between the incisors and molars, as in plesiadapiformes and rodents, distinct from primates.

Like primates:
The aye-aye has a postorbital bar, stereoscopic vision and an opposable hallux. Owen 1863 considered such traits ‘must be ordained’ in arguments for God and against Darwin’s then novel hypothesis of natural selection and evolution.

Like rodents,
Perry et al. 2014 report: “the single pair of incisors consists of continuously growing, elongate, open-rooted chisels, both upper and lower incisors.”

Based on the LRT
mutltuberculates are netonous rodents, growing to adulthood without ontogenetically incorporating post-dentary bones into the tympanic and periotic (inner ear enclosing bones), as we learned earlier here.

Figure 6. The aye-aye, Daubentonia in vivo. This is the closest living relative of multituberculates and is itself a plesiadapiform member of Glires, close to rodents, not primates.

Figure 6. The aye-aye, Daubentonia in vivo. This is the closest living relative of multituberculates and is itself a plesiadapiform member of Glires, close to rodents, not primates.

By convergence
the aye-aye (Daubentonia. Fig. 6) likewise reduces the tympanic and periotic along with the angular process of the dentary, producing a sliding joint that would have interfered with the ear bones if allowed to develop as in most placentals.

Carter 2009 notes
(while mistakenly assuming a lemur affinity for Daubentonia), “The overall dimensions of the D. madagascariensis auditory ossicles are large and they have a unique morphology.” Carter also reports on the elongate manubrium of the malleus (the former articular). This is in accord with similar structures in the neotonous (not primitive!) multituberculate auditory bone chain you can see here.

What does the angular process of the plancental dentary do?
According to Meng et al. 2003, a huge angular process was present in Rhombomylus, an extinct gerbil. Meng et al. mapped insertions for the deep masseter and superficial masseter externally. Then they mapped insertions for the medial pterygoid and superficial masseter internally. The Rhomboylus glenoid has a small diameter and rotates. It does not slide.

Meng et al. write: “As the major muscle to move the mandible forward, the superficial masseter must be long enough so that it can work to bring the jaw forward at least the minimum working distance. In general, the action line of the anterior deep masseter is nearly perpendicular to the moment arm of the mandible, while the posterior one has an acute angle to the moment arm and, therefore, less mechanical advantage. the deep masseter must have been sizable and supplies the main force for mastication as in rodents.”

The point of which is: multituberculates and the aye-aye reduce and eliminate the angular process. So we can imagine the muscles listed by Meng et al. either migrate or are lost in multituberculates and the aye-aye.

Figure 1. Maiopatagium in situ in white and UV light. The X marks an area surrounded by fur lacking proptagial data. Is the propatagium wishful thinking?

Figure 7. Maiopatagium in situ in white and UV light. The X marks an area surrounded by fur lacking proptagial data. Is the propatagium wishful thinking? Yes. Those are long guard hairs, precursors to porcupine quills. There is no patagium here.

We can’t leave Jurassic flying squirrels
without a quick review of Maiopatagium (Early Jurassic, Fig. 7, Meng et al. 2017), which was hailed ever since as a gliding mammal or mammaliaform.

Contra Meng et al. 2017
phylogenetic analysis nested Maiopatagium with the extant porcupine (Coendou), not with gliding multituberculates, like Vilevolodon. Maiopatagium has long straight hairs and lacks any trace of a patagium. Those long straight hairs are the precursors to porcupine quills according to the LRT.

Phyogenetic analysis puts rodents and all their precursors
(Tupaia, Henkelotherium, Nasua) squarely and clearly in the earlier part of the Early Jurassic, though not yet recovered in fossils.

The myth about the patagium surrounding Maiopatagium
seems to have had its genesis in the fact that Vilevolodon was described at the same time,  by the same authors, in the same publication. Vilevolodon (Fig. 1) has a no-doubt, flying sqirrel-like patagium. Maiopatagium (Fig. 7) was described with a misidentified patagium and a misidentified bat-like calcar. No patagium is present, but long straight hairs are. As noted above, these are precursors to porcupine quills. Getting taxa into a proper phylogenetic context is the key to understanding soft tissue and taxonomy.


References
Carter Y 2009. Monkey Hear: A morphometric analysis of the primate auditory ossicles. Master of Arts thesis, The U of Manitoba.
Del Pero M et al (4 co-authors) 1995. Phylogenetic relationships among Malagasy lemuls as revealed by mitochrondrial DNA sequence analysis. Primates 36: 43I-440.
Dene H, Goodman M and Prychodlco V 1980. Immunodiffusion systematics of the primates. Mamalia 44:27-31.
Luo Z-X, (6-co-authors) 2017. New evidence for mammaliaform ear evolution and feeding adaptation in a Jurassic ecosystem. Nature. in press (7667): 326–329. doi:10.1038/nature23483
Meng et al. 2003. The osteology of Rhombomylus (Mammalia, Glires): Implications for phylogeny and evolution of Glires. Bulletin of the American Museum of Natural History 275: 1–247.
Meng Q-J, Grossnickle DM, Liu D, Zhang Y-G, Neander AI, Ji Q and Luo Z-X 2017.
New gliding mammaliaforms from the Jurassic. Nature (advance online publication)
doi:10.1038/nature23476
Owen R 1863. On the characters of the aye-aye as a test of the Lamarckian and Darwmian hypothesis of the transmutation and origin of the species. Rep Br Assoc Adv Sci 1863: 114-116.
Perry JM et al. (4 co-authors) 2014. Anatomy and adaptations of the chewing muscles in Daubentonia (Lermuriformes). The Anatomical Record 297:308–316.
Porter CA et al (5 co-authors) 1995. Evidence on primate phylogeny from e-globin gene sequences and flanking regions. Journal of Molecular Evolution 40: 30-55.
Rurnpler Y et al (4 co-authors) 1988. Chromosomal evolution of the Malagasy lemurs. Folio Primatologica 50 124-129.
Sterling EJ 1994. Taxonomy and distribution of Daubentonia madagascariensis: a historical perspective. Folio Primatologica 62: 8-I3.

wiki/Maiopatagium
wiki/Coendou
wiki/Multituberculata

https://pterosaurheresies.wordpress.com/2019/01/06/a-post-dentary-reversal-between-rodents-and-multituberculates/

Evolution and synonyms of the hyomandibular and intertemporal

A major issue still facing paleontology and comparative anatomy
is the different names given to homologous bones in fish, reptiles and mammals. For example:

  1. the hyomandibular of fish is the stapes in tetrapods;
  2. the sphenotic in fish is the intertemporal in basal tetrapods, the prootic + opisthotic in reptiles and mammals;
  3. in fish the supraoccipital is the postparietal in stem tetrapods. That bone splits transversely to produce a postparietal and a supraoccipital in reptiles (Fig. 9);
  4. sometimes the jugal, lacrimal, nasal, maxilla and other bones also split into two or more bones. Other times they fuse together;
  5. some bones do not appear until later, de novo or by the product of a split;
  6. likewise, marginal teeth appear, disappear, fuse, unfuse, become more complex and simpler during evolution.
  7. … and that’s not counting the bones that have been traditionally mislabeled (Fig. 10).

From the genesis of the vertebrate skeleton
in Middle Silurian Birkenia (Fig. 1), a tiny hyomandibular articulates with the intertemporal dorsally and the tiny quadrate ventrally. The hyomandibular, a former dorsal gill arch segment, would ultimately evolve to become the most robust bone in the architecture of certain basal bony fish (Fig. 2) before shrinking in stem tetrapods (Fig. 6), ultimately becoming the stapes in basal reptiles (Fig. 9), and a tiny middle ear bone in mammals and humans.

Figure 2. Birkenia in situ with precursor facial bones labeled. This Middle Silurian taxon is basal to Furcacaudiformes and all other vertebrates.

Figure 1. Birkenia in situ with precursor facial bones labeled. This Middle Silurian taxon is basal to Furcacaudiformes and all other vertebrates.

In the first fish with jaws,
Chondrosteus (Fig. 2) the hyomandibular pivots to thrust the jaws forward during a bite, an action originated in tube-mouth osteostracans and sturgeons.

Figure 1. Chondrosteus animation (2 frames) in situ and reconstructed in lateral view. This is the transitional taxon linking sturgeons to bony fish + sharks.

Figure 1. Chondrosteus animation (2 frames) in situ and reconstructed in lateral view. This is the transitional taxon linking sturgeons to bony fish + sharks.

In the paddlefish ancestor,
Tanyrhinichthys (Fig. 3), the hyomandibular (deep green again) is no longer as mobile.

Figure 2. Tanyrhinichthys face after color tracing.

Figure 2. Tanyrhinichthys face after color tracing.

The hyomandibular becomes a massive immobile element
in the Early Devonian bony fish and spiny shark  Homalacanthus (Fig. 4). It continues to link the intertemporal with the quadrate.

Figure 4. Homalacanthus in situ and reconstructed.

Figure 4. Homalacanthus in situ and reconstructed. The massive hyomandibular is dark green.

In the fish portion
of the large reptile tree (LRT, 1710+ taxa; Fig. x) we’ve just crossed the major dichotomy separating stem lobefins (many of which are still ray fins) from stem frog fish + mudskippers, sea robins and tripod fish, which also use their pectoral fins to walk along the sea floor. (Let’s save that bit of interest for another blogpost).

Figure x. Subset of the LRT, focusing on fish for July 2020.

Figure x. Subset of the LRT, focusing on fish for July 2020.

Just across the dichotomy,
the tiny (3cm) spiny shark, Mesacanthus (Fig. 5) has a slender hyomandibular with forked tips. Thereafter the hyomandibular is largely covered up by cheek bones.

Figure 1. Early Devoniann Mesacanthus in situ. This 3 cm fish is a typical acanthodian here traced using DGS methods and reconstructed. Distinct from other spiny sharks, this one lacks large cheek plates, as in the extant Notopterus (Fig. 3).

Figure 5. Early Devoniann Mesacanthus in situ. This 3 cm fish is a typical acanthodian here traced using DGS methods and reconstructed. The hyomandibular is dark green.

In the stem tetrapod and large osteolepid,
Eusthenopteron (Fig. 6) the hyomandibular (dark green) attaches to a largely submerged intertemporal (yellow-green) with little dorsal exposure. The quadrate (red) contact with the hyomandibular is only tentative.

Figure 5. Eusthenopteron hyomandibular (dark green) still linking a largely submerged intertemporal (yellow-green) and a small quadrate (red).

Figure 6. Eusthenopteron hyomandibular (dark green) still linking a largely submerged intertemporal (yellow-green) and a small quadrate (red). Here the pterygoid (dark red) is essentially vertical, distinct from most tetrapods (e.g. Figs. 7-9).

In the flattend skull of a basal tetrapod, like
Laidleria (Fig. 7), the hyomandibular / stapes is horizontal and the intertemporal does not have a dorsal exposure. The quadrate connection is broken as the stapes contacts the small posterior tympanic membrane.

Figure 6. Early tetrapod Laidleria. The intertemporal disappears from the dorsal skull and the hyomandibular / stapes dark green)  is oriented horizontally here without a quadrate connection.

Figure 7. Early tetrapod Laidleria. The intertemporal disappears from the dorsal skull and the hyomandibular / stapes dark green)  is oriented horizontally here, perhaps without a quadrate connection, but note the extent of the stapes in palate view vs. occiput view.

In the aquatic reptilomorph,
Kotlassia (Fig. 8), the hyomandibular / stapes is tiny and oriented dorsolaterally in contact with a large tympanic membrane filling a posterior notch. The intertemporal reappears on the dorsal surface of the skull and expands internally to form the paraoccipital process (opisthotic).

Figure 7. The reptilomorph, Kotlassia, skull. Note the reappearance of the intertemporal here called the prootic. The hyomandibular / stapes is tiny and dark green.

Figure 8. The reptilomorph, Kotlassia, skull. Note the reappearance of the intertemporal here called the opisthotic in occipital view. The hyomandibular / stapes is tiny and dark green. The stapes contacts the tympanic membrane laterally.

In the basal and fully terrestrial archosauromorph,
Paleothyris (Fig. 9), the intertemporal is no longer exposed on the dorsal surface, but is exposed in occipital view, where it is called the opisthotic. The otic notch is now absent as the eardrum is reduced and relocated posterior to the jaw hinge. The former robust hyomandibular continues thereafter to shrink, becoming more sensitive to eardrum vibrations enabling a greater range of sound frequencies to be transmitted to the inner ear and brain.

Figure 8. The early archosauromorph, Paleothyris. Here the hyomandibular / stapes is oriented ventrolaterally. The intertemporal is not exposed dorsally.

Figure 9. The early archosauromorph, Paleothyris. Here the hyomandibular / stapes is oriented ventrolaterally. The intertemporal is not exposed dorsally, only occipitally where it is called the opisthotic.

On a slightly different subject:
bone misidentification by Thomson 1966

has been something of a problem ever since that publication. Here (Fig. 10) are the original bone IDs along with revised IDs on separate frames. Principally the relabeled intertemporal and parietal move behind the dorsal braincase division (Fig. 11).

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 10. Ectosteorhachis skull from Thomson 1966 with layers to show the brain case and palatoquadrate. Some bones are relabeled in the revised view. Note the intertemporal becomes the prootic + opisthotic at this point.

Thomson 1966 erred
when he put these elements anterior to the split, probably in order to locate the pineal opening between the parietals, which is typical of tetrapods. In osteolepids and their kin the pineal opening is between the relabeled frontals anterior to the transverse cranial split (Fig. 11).

Figure 11. Eusthenopteron and Osteolepis with skull bones relabeled.

Figure 11. Eusthenopteron and Osteolepis with skull bones relabeled.

Why is this so?
Under this new labeling system the contact between the intertemporal and hyomandibular is maintained (Figs. 6, 10). Outgroups to these taxa, like Cheirolepis (Fig. 12) likewise run a portion of the postorbital over the orbit, separating the postfrontal from the orbit margin. Now the ostelepids follow that trait despite the two-part postorbital.

Figure 11. Cheirolepis is an outgroup taxon to the ostelepids that includes a postorbital that extends over the orbit, separating the postfrontal from the orbit margin.

Figure 12. Cheirolepis is an outgroup taxon to the ostelepids that includes a postorbital that extends over the orbit, separating the postfrontal from the orbit margin.

In earlier posts
on hyomandibular evolution. and juvenile Eusthenopteron (Fig. 13; Schultze 1984) corrections have now been made. This bit of relabeling is a new hypothesis awaiting confirmation from others. At present phylogenetic bracketing (Fig. 12) supports this interpretation.

Figure 1. Eusthenopteron juvenile in situ from Schultze 1984. Large plate ventral to the mandible overlaps a convex ventral margin. The quadratojugal is not labeled here. Several bones are re-labeled here.

Figure 1. Eusthenopteron juvenile in situ from Schultze 1984. Large plate ventral to the mandible overlaps a convex ventral margin. The quadratojugal is not labeled here. Several bones are re-labeled here.

For those interested,
these changes affected only 4 character traits out of 238. These scoring changes did not affect the tree topology.


References

Schultze H-P 1984. Juvenile specimens of Eusthenopteron foordi Whiteaves, 1881 (Osteolepiform Rhipidistian, Pisces) from the Late Devonian of Miguasha, Quebec, Canada. Journal of Vertebrate Paleontology 4(1):1–16.
Thomson KS 1966. The evolution of the tetrapod middle ear in the rhipidistian-amphibian transition. American Zoologist 6:379–397.
Westoll TS 1943. The hyomandibular of Eusthenopteron and the tetrapod middle ear. Transactions of the Royal Society B 131:393–414.

Can an Early Cretaceous ‘stem mammal’ be considered ‘transitional’?

The transition from pre-mammals to early mammals
occurred during the Triassic era, despite the fact that many extremely rare pre-mammals, are known from post-Triassic strata (Fig. 1), but, so far, not post-Cretaceous strata.

Figure 1. Pre-mammal synapsids in the LRT colorized chronologically.

Figure 1. Pre-mammal synapsids in the LRT colorized chronologically. The extreme rarity of these often late-surviving fossils is indicated by the scattershot chronology of sister taxa.

The new tiny Origolestes (Mao et al. 2019; Fig. 2) is an Early Cretaceaous late survivor of a Triassic radiation of pre-mammals. Therefore it is NOT in the lineage of the Mammalia, but retains traits from that clade.

Figure 1. Origolestes in situ with colors added using DGS methods.

Figure 1. Origolestes in situ with colors added using DGS methods. Note the tiny canines and odd coronoid process. These are indicators of a parallel evolution.

From the Mao et al. abstract:
“Based on multiple 3D skeletal specimens we report a new Cretaceous stem therian mammal that displays decoupling of hearing and chewing apparatuses and functions.

Just three days ago we looked at a similar situation in Jeholbaatar, only in that case the loose ear bones represented a reversal. Similar morphologies MUST be seen in a phylogenetic context.

“The auditory bones, including the surangular, have no bone contact with the ossified Meckel’s cartilage; the latter is loosely lodged on the medial rear of the dentary.”

“This configuration probably represents the initial morphological stage of the definitive mammalian middle ear.

Except that it arrives way too late in the fossil record.

Evidence shows that hearing and chewing apparatuses have evolved in a modular fashion. Starting as an integrated complex in non-mammaliaform cynodonts, the two modules, regulated by similar developmental and genetic mechanisms, eventually decoupled during the evolution of mammals, allowing further improvement for more efficient hearing and mastication.”

This represents a parallel evolution of the decoupling of the middle ear bones. Let’s see how the popular press represented this finding, led by the authors.

From an online ScienceNews.org article by Carolyn Gramling:
“Exceptionally preserved skulls of a mammal that lived alongside the dinosaurs may be offering scientists a glimpse into the evolution of the middle ear.”

We don’t need another ‘glimpse’. We know exactly how this happened in the pre-Late Triassic ancestors of mammals.

“The separation of the three tiny middle ear bones — known popularly as the hammer, anvil and stirrup — from the jaw is a defining characteristic of mammals. The evolutionary shift of those tiny bones, which started out as joints in ancient reptilian jaws and ultimately split from the jaw completely, gave mammals greater sensitivity to sound, particularly at higher frequencies. But finding well-preserved skulls from ancient mammals that can help reveal the timing of this separation is a challenge.”

All true and good background for a popular article.

“Now, scientists have six specimens — four nearly complete skeletons and two fragmented specimens — of a newly described, shrew-sized critter dubbed Origolestes lii that lived about 123 million years ago. O. lii was part of the Jehol Biota, an ecosystem of ancient wetlands-dwellers that thrived between 133 million and 120 million years ago in what’s now northeastern China.”

“The skulls on the nearly complete skeletons were so well-preserved that they were able to be examined in 3-D, say paleontologist Fangyuan Mao of the Chinese Academy of Sciences in Beijing and colleagues. That analysis suggests that O. lii’s middle ear bones were fully separated from its jaw, the team reports online December 5 in Science.”

So they’re setting up a narrative without the proper background that mammals with this configuration first appeared in the Late Triassic, tens of millions of years earlier. Then they talk to another expert.

“This paper describes a spectacular fossil,” says vertebrate paleontologist Zhe-Xi Luo of the University of Chicago, who was not involved in the new study. But he’s not convinced that O. lii represents an evolutionary leap forward in mammalian ear evolution.

“Luo notes that O. lii is closely related to the mammal genus Maotherium, which lived around the same time and in roughly the same location. In Science in July, Luo and colleagues reported that a new analysis of Maotherium revealed that its middle ear bones were still connected to its jawbones by a strip of cartilage (SN: 7/18/19).

That finding, Luo says, was expected. Maotherium is well-known as a transitional organism, in which the middle ear bones had begun to rotate away from the jaw but were still loosely connected by that cartilage. There are numerous branches and twigs on the mammal family tree, Luo says, and evolution occurred at a different pace on them. But, he says, it’s unlikely that O. lii would have had separated ear bones when Maotherium didn’t, given the pair’s close positioning on the tree.”

Still no mention of the Late Triassic origin for mammals and the parallel development in this late survivor.

“Luo says he also doesn’t find the study’s evidence that the separation was complete in O. lii convincing. Three of the four skulls in the study were missing all or part of the middle ear, and the gap between the middle ear bones and jaw in the fourth skull may have been a break that occurred during fossilization, he adds.”

See how paleontologists try to put the brakes on the work of their colleagues?

“However, the new study’s researchers reject this idea. “It’s common that different interpretations may exist for a discovery in paleontology,” says vertebrate paleontologist Jin Meng of the American Museum of Natural History in New York, a coauthor of the study. But, Meng says, none of the ear bones or the cartilage in any of the skulls show fractured or broken edges. That, he says, suggests that these features were already separated in the animals before their demise.”

See how paleontologists try to bounce back from criticism? Meng is correct. Such ‘different interpretations’ are common. I have them. Others have them. You have them. In any case, the indisputable late appearances of Origolestes and Maotherium attest to their removal from the origin of the Mammalia. What they can offer us is a parallel look at this chapter in synapsid evolution. In other words, they are not the main attraction. They are a side show.


References
Mao F, Hu Y-M, Li C-K, Wang YQ, Chase MH, Smith AK and Meng J 2019. Integrated hearing and chewing modules decoupled in a Cretaceous stem therian mammal. Science eaay9220 (advance online publication). online here

An ancient critter may shed light on when mammals’ middle ear evolved

wiki/Zhangheotheriidae

Early Cretaceous Jeholbaatar kielanae: middle ear origin or reversal?

FIgure 1. Tiny Jeholbaatar in situ, full scale.

FIgure 1. Tiny Jeholbaatar in situ, full scale.

Wang, Meng  and Wang 2019 introduce us 
to a tiny new multituberculate, Jeholbaatar kielanae (Figs. 1, 2), in which the much tinier and displaced middle ear bones are found in articulation (Figs. 3, 4) along with a displaced surangular!

Figure 2. Jeholbaatar with certain bones colorized using DGS methods.

Figure 2. Jeholbaatar with certain bones colorized using DGS methods.

Figure 5. Jeholobaatar images from Wang, Meng and Weng 2019. Rat ear bones photo from Li, Gao, Ding and Salvi 2015. Correction label added here. The rat middle ear, no surprise, is phylogenetically similar to that of the multituberculates, Jeholbaatar and Arboroharamiya.

Figure 3. Jeholobaatar images from Wang, Meng and Weng 2019. Rat ear bones photo from Li, Gao, Ding and Salvi 2015. Correction label added here. The rat middle ear, no surprise, is phylogenetically similar to that of the multituberculates, Jeholbaatar and Arboroharamiya.

Figure 4. The tiny displaced middle ear bones of Jeholbaatar colorized

Figure 4. The tiny displaced middle ear bones of Jeholbaatar colorized

Wang, Meng and Wang present two cladograms
(Fig. 3) of multituberculate relationships. The LRT agrees with the ‘a’ oversimplified cladogram, the one that does not split Arboroharamiya from Jeholobaatar. 

In similar fashion,
the large reptile tree (LRT, 1612+ taxa) nests multituberculates as derived rodents, despite what appears to be, in this phylogenetic context, a more primitive middle ear morphology than found in extant rats (Rattus, Fig. 4), mice (Mus) and their closest living relatives, the aye-aye (Daubentonia). In the LRT Jeholbaatar nests at the base of the Villevolodon + Shenshou clade.

Tradition continues in Wang, Meng and Wang
as they omit rodents from multituberculate studies while force fitting multis into a dissimilar nesting with basal mammals, including prototheres, the egg-laying mammals.

It is worthwhile comparing the skulls
of the rodent, Rattus (Fig. 6), and the multituberculate, Kryptobaatar (Fig. 5). This is much more than convergence. That is why they nest close to one another in the LRT, but not as sisters.

Figure 1. Animation of the mandible of the multituberculate Kryptobaatar showing the sliding of the jaw joint producing separate biting and grinding actions, just like rodents, their closest relatives in the LRT.

Figure 5. Animation of the mandible of the multituberculate Kryptobaatar showing the sliding of the jaw joint producing separate biting and grinding actions, just like rodents, their closest relatives in the LRT. In multis the middle ear bones remain attached to the posterior dentary and ride along with jaws as they slide distinct from most placental taxa. Note the lack of a middle ear (tympanic) bulla. Compare to figure 1.

Figure . Skull of Rattus, the rat. Note the similarities to Megaconus. Not identical but similar.

Figure 6 The brown rat (Rattus norvegicus) skull has a mandible glenoid separate from the retroarticular process. Whenever the jaw slides back and forth, these two processes slide above and below the middle ear (tympanic) bulla without interfering with the ear canal. Compare to figure 2.

From the Wang, Meng and Wang 2019 abstract:
“The evolution of the mammalian middle ear is thought to provide an example of ‘recapitulation’—the theory that the present embryological development of a species reflects its evolutionary history.”

This has been documented in embryo dissections.

“Accumulating data from both developmental biology and palaeontology have suggested that the transformation of post-dentary jaw elements into cranial ear bones occurred several times in mammals.”

In the LRT this happened once in crown mammals, and once again in Repenomamus, a pre-mammal, Cretaceous mammal-mimic

“In addition, well-preserved fossils have revealed transitional stages in the evolution of the mammalian middle ear. But questions remain concerning middle-ear evolution, such as how and why the post-dentary unit became completely detached from the dentary bone in different clades of mammaliaforms.”

The LRT does not recognize the clade Mammaliaformes, defined as, “the clade originating from the most recent common ancestor of Morganucodonta and the crown group mammals.” Morganucodon is a basal metatherian in the LRT.

“Here we report a definitive mammalian middle ear preserved in an eobaatarid multituberculate mammal, with complete post-dentary elements that are well-preserved and detached from the dentary bones. The specimen reveals the transformation of the surangular jaw bone from an independent element into part of the malleus of the middle ear, and the presence of a restricted contact between the columelliform stapes and the flat incus.”

Congratulations to the preparator. The middle ear bones are microscopic.

“We propose that the malleus–incus joint is dichotomic [= classification based upon two opposites] in mammaliaforms, with the two bones connecting in either an abutting or an interlocking arrangement, reflecting the evolutionary divergence of the dentary–squamosal joint. In our phylogenetic analysis, acquisition of the definitive mammalian middle ear in allotherians such as this specimen was independent of that in monotremes and therians.”

The LRT does not recover the clade Allotheria. Rather multituberculates nest within Glires, within Rodentia close to Rattus (Fig. 4), Carpolestes and the aye-aye, Daubentonia.

“Our findings suggest that the co-evolution of the primary and secondary jaw joints in allotherians was an evolutionary adaptation allowing feeding with unique palinal (longitudinal and backwards) chewing. Thus, the evolution of the allotherian auditory apparatus was probably triggered by the functional requirements of the feeding apparatus.”

Unfortunately,
the authors do not compare their find to rodents. Note the similarity of the middle ear bones in Rattus (Fig. 3) to those of multituberculates. So, once again: taxon exclusion spoils a perfectly grand discovery and description.

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

Figure 7. Evolution of the tetrapod mandible and ear bones leading to humans.

A little backstory:
As mentioned by Wang, Meng and Wang, a mammal embryo develops ontogenetically it more or less recapitulates its entire phylogenetic development, from one cell, to a ball of cells, to an embryo with gills, to an embryo with several primordial jaw bones. Three of these detach from the dentary in placentals, migrate posteriorly and become middle ear bones.

Multis are different.
Multis appear to have large, attached, more primitive middle ear bones, like those found in egg-laying pre-mammals. The question few appear to have asked is: why would this happen?

Multis are renown
for losing (or never developing in the tradition model) their cylinder and socket jaw joint to develop a sliding jaw joint, harnessed by large muscles. A sliding jaw joint is also present in rodents.

Here’s a thought:
Perhaps nature found it more important for the jaw joint to slide posteriorly in multis, over the spot where tiny ear bones are found in rodents, so the middle ear bones remained in a state of arrested development, more or less attached to the posterior dentary, moving along with the sliding jaw, never attaching themselves to the base of the braincase, as in other placental mammals. This can happen by a simple matter of stopping the development of primitive large ear bones to tiny ear bones. Evidently this reversal was a successful gambit, as multis survived from the Jurassic deep into the Tertiary before finally going extinct for reasons unknown.

For the general public (popular press),
the following online article describes the specimen and its authors.

“Researchers from the Institute of Vertebrate Paleontology and Paleoanthropology (IVPP) of the Chinese Academy of Sciences and the American Museum of Natural History (AMNH) have reported a new species of multituberculate – a type of extinct Mesozoic “rodent” – with well-preserved middle ear bones from the Cretaceous Jehol Biota of China. The findings were published in Nature on November 27.”

Note the use of quotation marks around the word “rodent” indicate their understanding that Jeholbaatar was not a rodent, but looked like one.

“The new mammal, Jeholbaatar kielanae, has a middle ear that is distinct from those of its relatives. WANG Yuanqing and WANG Haibing from IVPP, along with MENG Jin from AMNH, proposed that the evolution of its auditory apparatus might have been driven by specialization for feeding.”

According to the LRT, it is not the evolution of an auditory apparatus, but the reversal to to a more primitive state, because sisters all have tiny middle ear bones.

“Fossil evidence shows that postdentary bones were either embedded in the postdentary trough on the medial side of the dentary or connected to the dentary via an ossified Meckel’s cartilage in early mammals, prior to their migration into the cranium as seen in extant mammals.”

See figure 7 for an illustration of this trough and migration in several taxa.

“Detachment of the mammalian middle ear bones from the dentary occurred independently at least three times. But how and why this process took place in different clades of mammals remains unclear.”

It remains unclear in the Wang, Meng and Wang paper due to taxon exclusion, leading to an invalid tree topology. They why was likely due to the nocturnal and arboreal displacement of surviving mammals, requiring better hearing abilities, during the age of dinosaurs, which were their chief predators during the day.

“The Jeholbaatar kielanae specimen was discovered in the Jiufotang Formation in China’s Liaoning Province. It displays the first well-preserved middle-ear bones in multituberculates, providing solid evidence of the morphology and articulation of these bony elements, which are fully detached from the dentary.”

Fully detached and displaced, between the teeth.

“It reveals a unique configuration with more complete components than those previously reported in multituberculates. The new fossil reveals a transitional stage in the evolution of the surangular – a “reptilian” jawbone.”

Remember, ontogeny recapitulates phylogeny, and Jeholbaatar is a tiny specimen (Fig. 1), a precocial and phylogenetically miniaturized taxon, retaining juvenile traits, including a middle ear in an arrested state of development.

“In light of current evidence, scientists argue that the primary (malleus-incus) and secondary (squamosal-dentary) jaw joints co-evolved in allotherians, allowing a distinct palinal (anteroposterior) jaw movement while chewing.” 

In the LRT anteroposterior jaw movement was well established in more primitive taxa (Figs, 3, 4). The LRT does not recognize the traditional clade, ‘Allotheria’.

“Selective pressure to detach the middle ear bones could have been stronger in order to increase feeding efficiency, suggesting that evolution of the middle ear was probably triggered by functional constraints on the feeding apparatus in allotherians.”

Actually, just the opposite, according to the LRT.  Primitive placentals already had, for millions of generations, tiny middle ear bones. In multis alone neotony + phylogenetic miniaturization led to the arrested development of the middle ear bones, which moved along with the dentary during palinal (anteroposterior) jaw movement. I suggest workers add more taxa to their phylogenetic analyses. Test rodents and their relatives along with multituberculates and see what pops out.


References
Li P, Gao K, Ding D and Salvi R 2015. Characteristic anatomical structures of rat temporal bone. ScienceDirect Journal of Otology 10:118–124.
Wang H, Meng J and Wang Y-Q 2019. Cretaceous fossil reveals a new pattern in mammalian middle ear evolution. Nature  online

http://english.cas.cn/newsroom/research_news/life/201911/t20191127_226412.shtml

Evolution of multituberculates illustrated

Updated the next day, January 5, 2019 with new interpretations of the post-dentary bones in figure 3, detailed here.

With the addition of four taxa
to the large reptile tree (LRT, 1370 taxa), a review of the Bremer scores helped cement relationships in the Primates + Glires clade (Figs. 1, 2). Yesterday we looked at plesiadapiform taxa (within Glires, Fig. 2) leading to the aye-aye, Daubentonia. Today we’ll look at a sister clade within Glires, one that produced the clade Multituberculata.

The traditional, but invalid outgroup taxon,
Haramiyavia, is a pre-mammal trithelodontid not related to the rodent-and plesiadapiform- related members of the Multituberculata in the LRT. More on that hypothesis below.

In Figure 1
look for the gradual accumulation of traits in derived taxa. Carpolestes (Late Paleocene) is a late survivor from a Jurassic radiation. Paulchoffatia is Latest Jurassic. Megaconus is Middle Jurassic. Vilevolodon, Xianshou and Rugosodon are Late Jurassic. Kryptobaatar is Late Cretaceous. Ptilodus is Paleocene. So this radiation had its genesis in the Early Jurassic and some clades, like Carpolestes, had late survivors.

Figure 1. LRT taxa in the lineage of multituberculates arising from Carpolestes and Paulchoffatia.

Figure 1. LRT taxa in the lineage of multituberculates arising from Carpolestes and Paulchoffatia. Carpolestes is a sister to Ignacius. The new taxon, Arboroharamiya, nests with Xianshou in the Han et al. cladogram.

It’s worth noting
that the one key trait that highlights many multituberculates, the oddly enlarged last premolar of the dentary, is also a trait found in the basal taxon, Carpolestes, but not in Paulchoffatia, (Fig. 1). Paulchoffatia has the odd mandible (dentary) without a distinct retroarticular process common to multituberculates, convergent with Daubentonia. That there is also no distinct glenoid process (jaw joint) in clade members made these jaw bones even harder to understand. Then I realized the jaw joints were mobile, slung in place by muscles, as in rodents and primates, rather than a cylindrical dentary/squamosal joint, as in Carnivorans.

There is one more elephant in the room
that needs to be discussed. Earlier we looked at the splints of bone at the back of the jaws in multituberculates identified as posterior jaw bones (Fig. 3), a traditional pre-mammal trait. Multis move the squamosal to the back of the skull and reduce the ear bone coverings (ectotympanics) that nearly all other placentals use to cover the middle ear bones. This reversal to the pre-mammal condition is key to the traditional hypothesis shared by all mammal experts that multis are pre-mammals. Embryo primitive therians have posterior jaw bones, but these turn into tiny middle ear bones during ontogeny. In multis their retention in adults is yet another example of neotony.

Why lose/reverse those excellent placental middle ear bones?
‘Why’ questions get into the realm of speculation. With that proviso, here we go.

Figure 2. Jaw muscles of the Late Cretaceous multituberculate, Catopsbaatar.

Figure 2. Jaw muscles of the Late Cretaceous multituberculate, Catopsbaatar.

The over-development of the lower last premolar
indicates some sort of preference or adaptation for food requiring such a tooth. The coincident and neotonous migration of the squamosals to the back of the skull (the pre-mammal Sinoconodon condition) enlarged the temporal chewing muscles (Fig. 2). The neotonous lack of development of tiny middle ear bones was tied in to that posterior migration. Evidently Jurassic and Cretaceous arboreal multis did not need the hearing capabilities provided by the tiny middle ear bones of most therians, but they needed larger jaw muscles. Evidently they were safe in the trees because there were few to no arboreal predators of mammals back then. Multis and rodents had the trees to themselves. Evidently that changed in the Tertiary, when multis became extinct, perhaps because birds of prey (hawks and owls) became widespread and only rodents could hear them coming. That’s a lot of guesswork. Confirmation or refutation should follow.

Figure 3. Images from Han et al. Color and white labels added. Here the malleus, incus and stapes have reverted to their pre-mammal states and configurations. Note the quadrate is in contact with the articular, as in pre-mammals as the dentary and squamosal become a sliding joint, carried by larger jaw muscles. Also note the various ectotympanic bones (yellow) also present, typical of Theria.

Figure 3. Images from Han et al. Color and white labels added. Here the malleus, incus and stapes have reverted to their pre-mammal states and configurations. Note the quadrate is in contact with the articular, as in pre-mammals as the dentary and squamosal become a sliding joint, carried by larger jaw muscles. Also note the various ectotympanic bones (yellow) also present, typical of Theria.

A recent paper by Han et al. 2017
on the Late Jurassic pre-mulltituberculate euharamiyidan, Arboroharamiya (Fig. 3), documents precisely the status of the middle ear/posteror jaw bones along with the phylogenetic reduction of the ectotympanic that frames the ear drum and forms a thin shell around the middle ear bones in more primitive members of the clade Glires (Fig. 4, evidently there is more variation in this, and I will take a look at that in the future). Han et al. report for Arboroharamiya, “The lower jaws are in an occlusal position and the auditory bones are fully separated from the dentary.” That is the mammal condition.

The Han et al cladograms
include a rabbit and a rodent, but suffer from massive taxon exclusion. As a result they mix up prototherians, metatherians and eutherians as if shuffling a deck of cards, as compared to the LRT. My first impression is that they use too many taxa known only form dental traits when they should have deleted those until a robust tree topology was created and established with a large suite of traits from more complete taxa, as in the LRT.  I will add Arboroharamiya to the LRT shortly.

Figure 2b. Subset of the LRT focusing on Primates + Glires.

Figure 4. Subset of the LRT focusing on Primates + Glires.

Unfortunately,
and I hate to report this, mammal experts have been guilty of depending on a short or long list of traits (which can and often do converge and reverse) to identify taxa and clades. As readers know, paleontologists should only depend on a phenomic phylogenetic analysis that tests a large suite of bone characters and a wide gamut of taxa. Analysis proves time and again to be the only way to confidently identify taxa and lump’n’split clades. Cladograms, when done correctly, weed out convergence. Otherwise, reversals, like the neotonous reappearance of post-dentary bones and the reotonous disappearance of ectotympanics, can be troublesome to deal with, causing massive confusion. A phylogenetic analysis quickly and confidently identifies reversals because all possible candidates are tested at one time. 

Unfortunately,
d
iscovering this little insight is yet another reason why other workers have dismissed the LRT, have attempted to discredit the LRT, and is causing confusion in yet another upcoming class of future paleontologists. Paleo students have to choose between relying on a short list of traits or performing a phenomic phylogenetic analysis. Only the latter actually works (see below) and avoids mixing in convergent traits.

If you don’t remember
‘amphibian-like reptiles,’ those are taxa, like Gephyrostegus, Eldeceeon and Silvanerpeton, that nest at the base of all reptiles in the LRT, but have no traditional reptile traits. Everyone else considers them anamniotes. In the LRT, based solely on their last common ancestor status/nesting, these taxa are known to have evolved the amniotic membrane, the one trait, by definition, that unites all reptiles (including birds and mammals) and labels the above basal taxa, ‘amphibian-lke reptiles.’

References
Han G, Mao F-Y, Bi-SD, Wang Y-Q and Meng J 2017. A Jurassic gliding euharamiyidan mammal with an ear of five auditory bones. Nature 551:451–457.
Urban et al. (6 co-authors) 2017. A new developmental mechanism for the separation of the mammalian middle ear ossicles from the jaw. Proceedings of the Royal Society B: Biological Sciences https://doi.org/10.1098/rspb.2016.2416

Dual origin of the mammalian-type jaw joint

Today: we look at a new paper
by Lautenschlager et al. 2018, who tested transitional synapsid jaw joints evolving into mammal ear bones. Before we begin, let’s remember these five pertinent facts:

1- A monophyletic clade consists of two select members,
their last common ancestor and all of its descendants. A clade does not include taxa that share, by convergence, a particular trait, no matter how ‘key’ that trait is.

2- Linnaeus 1758 decided THE key trait in mammals
is the expression of milk for infants from dermal glands. Since milk glands almost never fossilize several skeletal traits are used instead as ‘lactation markers.’

3- These markers include
the single replacement of milk teeth with permanent teeth. This replacement pattern implies toothless hatchlings dependent on their mother’s milk, a trait common to all living mammals and presumably, all extinct ones. Hatchling and neonate basal mammals only develop teeth and the ability to locomote as they mature in their mother’s care. Derived mammals, like cattle and horses, are ready to locomote at birth, as we learned earlier here.  Sinoconodon, a proximal mammal outgroup, lacked permanent teeth.

4- Another traditional ‘key’ trait in mammals
is the mammalian jaw joint (dentary-squamosal) which gradually (both embryologically and phylogenetically) replaces the basal tetrapod jaw joint (articular-quadrate). For several transitional taxa, both jaw joints operate side-by-side. In mammals the former posterior jaw bones eventually become gracile splints, then tiny ear bones.

5- Ear bone location
in egg-laying mammals (Prototheria), these ear bones are below the jaw joint. In Theria these ear bones are posterior to the jaw joint, demonstrating yet another act of convergence from a common ancestor in which the posterior jaw bones were still connected to a trough in the posterior dentary and a tiny, but robust quadrate, as in Megazostrodon.

So that sets the stage
for today’s discussion. It’s time to reexamine what makes a mammal a mammal.

In the large reptile tree
(LRT, 1293 taxa; subset Fig. 1) the last common ancestor of all living mammals is Megazostrodon from the Latest Triassic. The first dichotomy splits egg-laying mammals (Prototheria) from live-bearing mammals (Theria). So that happened early,

The smallest mammals were not the first mammals.
In the LRT tiny Early Jurassic Hadrocodium nests at the base of a small clade of basal therians that includes Morganucodon and Volaticotherium. Following in the pattern of basal reptiles, which also had smaller taxa after the genesis of the clade, basal mammals slowly evolved new reproductive structures and made improvements following the first tentative appearances of novel reproductive membranes and structures.

Six traditional mammals,
Gobiconodon (Trofimov 1978), Maotherium (Rougier et al. 2003); Spinolestes (Martin 2015); Yanaconodon (Luo et al. 2007) Liaoconodon (Meng et al. 2011) and Repenomamus (Li et al. 2001; Hu et al. 2005) nest outside the clade of crown (all living) mammals in the LRT, despite the fact that they all had single tooth replacement and a dentary-squamosal jaw joint, as in mammals. Traditionally these traits have caused taxonomic confusion as workers assumed no convergence.

Figure 1. Subset of the LRT focusing on the Kynodontia and Mammalia. Non-eutherian taxa in red were tested in the LRT but not included because they reduce resolution. Eutherian taxa in red include a basal pangolin and derived xenarthran, clades that extend beyond the bottom of this graphic. The pink clade proximal to mammals was considered mammalian by Lautenschlager et al. due to a convergent mammalian-type jaw joint.

Figure 1. Subset of the LRT focusing on the Kynodontia and Mammalia. Non-eutherian taxa in red were tested in the LRT but not included because they reduce resolution. Eutherian taxa in red include a basal pangolin and derived xenarthran, clades that extend beyond the bottom of this graphic. The pink clade proximal to mammals was considered mammalian by Lautenschlager et al. due to a convergent mammalian-type jaw joint.

A new paper by Lautenschlager et al. 2018
discusses “The role of miniaturization in the evolution of the mammalian jaw and middle ear.” Phylogenetic miniaturization prior to the appearance of mammals (Fig. 3) has been widely known for decades and was discussed earlier here. Putting their own twist on this hypothesis, Lautenschlager et al. report, “Here we use digital reconstructions, computational modeling and biomechanics analyses to demonstrate that the miniaturization of the early mammalian jaw was the primary driver for the transformation of the jaw joint. We show that there is no evidence for a concurrent reduction in jaw-joint stress and increase in bite force in key non-mammaliaform taxa in the cynodont–mammaliaform transition, as previously thought.”

Unfortunately,
Lautenschlager et al. begin their paper with a false statement: “The mammalian jaw and jaw joint are unique among vertebrates.” No. The LRT documents that this happened twice in parallel near the genesis of the clade Mammalia (Fig. 1). The authors’ error appears due to taxon exclusion in their phylogenetic analysis, creating a tree topology (Fig. 2) different from the LRT (Fig. 1). A larger taxon list would have rearranged the taxa in the Lautenschlager et al. cladogram as it does as the LRT continues to grow.

Figure 1. Modified from figure 1 in Lautenschlager et al. 2018 with the addition of a cyan and magenta band keyed to pre-mammals and mammals in the LRT. Note the oddly large Repenomamus and Vincelestes in the original work. They don't belong where they are placed.

Figure 2. Modified from figure 1 in Lautenschlager et al. 2018 with the addition of a cyan and magenta band keyed to pre-mammals and mammals in the LRT. Note the oddly large Repenomamus and Vincelestes in the original work. They don’t belong where they are placed here.  Zhangheotherium is a pangolin ancestor. Vincelestes is a top predator marsupial. Rugosodon is a multituberculate rodent. Massive taxon exclusion is the problem here. Worse yet, the red dotted line indicating “Jaw-joint transition” really should have started at the top of the graph, as shown in figure 3.

In the Lautenschlaer et al. 2018 cladogram
(Fig. 2) the last common ancestor of all mammals is tiny Hadrocodium. In their cladogram Megazostrodon, Morganucodon and Brasilitherium are not mammals, but Mammaliaformes (= the most recent common ancestor of Morganucodonta and Prototheria + Theria). The current definition of Mammaliaformes turns out to be a junior synonym for Mammalia because in the LRT Morganucodon and kin are all mammals.

Figure 3. Kynodontia to scale. The miniaturization of the ancestors of mammals had its genesis long before the proximal ancestors of mammals.

Figure 3. Kynodontia to scale. The miniaturization of the ancestors of mammals had its genesis long before the proximal ancestors of mammals, like Therioherpeton.

The LRT
(Fig. 1) documents the final stages of the evolution of the dentary-squamosal joint actually occurred twice: once in the lineage of mammals that led to all extant mammals (Fig. 4) and again in the lineage that led to Repenomamus and kin (Fig. 5).

Take away thought:
One cannot determine what a taxon is by identifying a key trait. That would be ‘pulling a Larry Martin.’ ‘Turtles’, ‘cetaceans’ and ‘pinnipeds’ all have a dual origins, as we learned earlier here, here and here. Only after a wide gamut phylogenetic analysis that tests all possibilities and opportunities can one determine the last common ancestor of a clade. That’s how we identify and guard against the specter and real possibility of convergence.

Figure 5. Basal mammals and their proximal ancestors. Here taxa below Megazostrodon are mammals. Those above are not. Hadrocodium is uniquely reduced, but this occurs within the Mammalia.  The dual jaw joint was tentatively present in Pachygenelus.

Figure 4. Basal mammals and their proximal ancestors. Here taxa below Megazostrodon are mammals. Those above are not. Hadrocodium is uniquely reduced, but this occurs within the Mammalia.  The dual jaw joint was tentatively present in Pachygenelus.

Lautenschläger et al. acknowledge convergence when they report: “New fossil information has suggested that a definitive mammalian middle ear (DMME) evolved independently in at least three mammalian lineages by detachment from the mandible, but the emergence of a secondary jaw joint is a key innovation that unites all mammaliaforms. However, a central question exists as to how, during this transformation, the jaw hinge remained robust enough to bear strong mastication forces while the same bones were becoming delicate enough to be biomechanically viable for hearing.”

That’s a good question,
and the authors did a good job of showing how they tested specimens.

Figure 5. Theriodont pre-mammals to scale. Note the dentary-squamosal jaw joint developed by convergence in this clade.

Figure 5. Theriodont pre-mammals to scale. Note the dentary-squamosal jaw joint developed by convergence in this clade.

Lautenschlager et al continue: “Here we integrate a suite of digital reconstruction, visualization and quantitative biomechanical modelling techniques to test the hypothesis that reorganization of the adductor musculature and reduced stress susceptibility in the ancestral jaw joint facilitated the emergence of the mammalian temporomandibular jaw joint. Applying finite element analysis, we calculated bone stress, strain and deformation to determine the biomechanical behaviour of the mandibles of six key taxa across the cynodont–mammaliaform transition.” (See Fig. 2, but also see Fig. 1)

Lautenschlager et al conclude:
“In our analyses, reduction in mandibular size—rather than alterations of the osteology and the muscular arrangement—produced the most notable effects on minimizing absolute jaw-joint stress. Our results demonstrate that changes to joint morphology and muscle (re)organization have little effect on joint loading.

Key to understanding the situation
and perhaps somewhat overlooked by the authors, is the fact that most of the changes to the posterior jaw bones were already in place in the last common ancestor of Repenomamus and Megazostrodon. a taxon close the Therioherpeton and Pachygenelus (Fig. 4). After these taxa, there was just a little bit left to do. Certainly size reduction had a great impact on all the changes that split mammals and their kin apart from their ancestors. Even so, a correct phylogenetic framework is necessary to build a valid case and not mix up mammals with non-mammals as Lautenschlager et al. did. They did not allow for the possibility of convergence which the inclusion of more taxa uncovered.

The multituberculate issue
Multituberculates, like Kryptobaatar, also have a low, robust jaw joint, just like Repenomamus and kin. So are they related? Not yet. In the LRT multituberculates are still more attracted to rodents and their kin than to pre-mammals.

Side note: While reexamining the data in the LRT, Liaoconodon shifted in the LRT to nest with Gobiconodon and Repenomamus, adding to the long list of corrections I’ve made here over the last seven years. As I’ve said many times before, I’m learning as I go. Sometimes that learning happens a little too long after a taxon’s insertion.

One final question: 
Did Repenomamus and Gobiconodon have tiny toothless neonates? Were the neonates helpless? Did their mothers provide milk to them? Which means, ultimately, did they represent an extinct clade of primitive mammals? Present data indicates the answer to all the above is ‘no’, despite the presence of two ‘key’ mammalian traits: permanent teeth and a dentary-squamosal jaw joint.

This is heretical,
but once discovered needs to be reported and later confirmed and/or refuted.

References
Hu Y, Meng J, Wang Y-Q and Li C-K 2005. Large Mesozoic mammals fed on young dinosaurs. Nature 433:149-152.
Lautenschläger S et al. (4 co-authors) 2018. The role of miniaturization in the evolution of the mammalian jaw and middle ear. Nature.com
Li J-L, Wang Y, Wang Y-Q and Li C-K 2001. A new family of primitive mammal from the Mesozoic of western Liaoning, China. Chinese Science Bulletin 46(9):782-785.
Meng J, Wang Y-Q and Li C-K 2011. Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont. Nature 472 (7342): 181–185.
Trofimov BA 1978. The first triconodonts (Mammalia, Triconodonta) from Mongolia. Doklady Akademii Nauk SSSR. 243 (1): 213–216.

wiki/Repenomamus
wiki/Gobiconodon

Reptile stapes evolution part 2: marine reptiles

Yesterday we looked at a report by Sobral et al. 2016 describing the stapes in several basal reptile terrestrial clades. You may recall that the summary data on the stapes was gratefully accepted, but the cladogram they produced was not a match for the large reptile tree (LRT). Today we’ll look at the Sobral et al. report on the stapes of marine diapsid reptiles.

Figure 1. From Sobral et al. 2016, their cladogram of marine diapsid reptiles nests turtles as diapsids between Youngina and Lepidosauria. I added the pink arrows and image of Mesosaurus to show relationships the LRT found based on similar morphologies. Turtles as diapsids is ludicrous and totally without supporting morphological evidence.

Figure 1. From Sobral et al. 2016, their cladogram of marine diapsid reptiles nests turtles as diapsids between Youngina and Lepidosauria. I added the pink arrows and image of Mesosaurus to show relationships the LRT found based on similar morphologies. Turtles as diapsids is ludicrous and totally without supporting morphological evidence. They are pareiasaurs. The basal split among reptiles separates lepidosauromorphs from archosauromorphs.

Sobral et al. 2016 report

  1. “The systematic position of these three major marine groups (Fig. 1) among Neodiapsida is still debated, mainly because of the high degree of morphological convergences among aquatic taxa.” In the large reptile tree (LRT) there is no controversy and no high degree of morphological convergence among aquatic taxa. Those that look alike down to the smallest detail are indeed related to one another.
  2. “All three lineages, the Ichthyosauromorpha, the Sauropterygia, and the Thalattosauriformes, appeared in the Early Triassic with overall body plans already adapted in various degrees to aquatic life, without hinting at their terrestrial ancestors.” In the LRT those aquatic and terrestrial ancestors are clearly presented.
  3. “It was only recently that a putative new stem turtle, Pappochelys from the Middle Triassic of southern Germany, was described that might shed light on the issue. These small (20 cm) animals not only had broadened ribs and a massive gastral apparatus that may be considered a precursor of a fused shell, but they also had a lizard-like diapsid skull with teeth.” In the LRT Pappochelys nests with Palatodonta, basal to placodonts and distant from turtles.
  4. As a side point, In their figure 8.12 the authors follow tradition and misidentify the supratemporal as the squamosal and the squamosal as the quadratojugal in Proganochelys in particular and turtles in general. Click here for clarification.
  5. In the LRT various specimens of Youngina, Youngoides and Youngopsis are basal the Protorosauria and Archosauriformes — completely unrelated to turtles and lepidosaurs.
  6. Here’s how you know their cladogram is bunk: No one has ever produced a basal lepidosaur (Iguana) that would be close to basal archosauriforms (Proterosuchus). Please don’t raise the hopeful specter of a lost ghost lineage. The LRT does not need that and neither should any other cladogram on reptile interrelationships.

The stapes in Hupesuchia
Sobral et al. 2016 report, “little is known about their braincases or ear regions.” The LRT finds Hupehsuchians to be derived from shastasaurid ichthyosaurs.

The stapes in Ichthyosauria
Sobral et al. 2016 report, “The stapes of most ichthyosaurs consists of a dorsomedially broadened footplate (sometimes referred to as the occipital head) (e.g., Fischer et al. 2012) and a narrower ventrolateral shaft. In some cases, such as in the Jurassic Temnodontosaurus, thickness is more consistent throughout the shaft, resulting in overall stout stapedial morphology. The stapes structurally supports the braincase by articulating with the basioccipital and the basisphenoid medially and the quadrate laterally. A massive stapes does not necessarily imply lack of hearing, however, because it could still  transduce low-frequency sound waves via a bony connection directly to the fluids of the inner ear.”

“the lack of an otic notch together with the bony contact between the otic capsules and the suspensorium led to the proposition that a tympanic membrane was completely lost in ichthyosaurs and that they were not capable of acute, directional hearing.”

The stapes in thalattosauriformes
Sobral et al. 2016 report, “in Askeptosaurus [the] stapes is an elongated rod-like bone that medially thickens into a two-headed knob reminiscent of the stapedial shapes found in various stem diapsids. The lateral concave posterior emargination of the quadrate further argues for the presence of a tympanic membrane.”

The stapes in placodonts
Sobral et al. report, “Only one stapes is known to be preserved in one specimen of the basal placodont species Placodus gigas indicating that this structure may not have been fully ossified inderived placodonts.”

The stapes in pachypleurosaurs
Sobral et al. 2016 report, “the stapes has been reported in only one pachypleurosaur genus, Neusticosaurus, consisting of a short, slender, and cylindrical rod. The tympanic membrane would have been particularly large in pachypleurosaurs as they have the unique feature of a quadrate fossa posterior to the articular facet of the retroarticular process on the lower jaw, which contributed to form part of the middle ear chamber.”

The stapes in nothosaurs, pistosaurs and plesiosaurs
Sobral et al. 2016 report, “the tympanic membrane appears to have been completely lost, possibly due to these taxa being increasingly aquatic. Narrow stapes have been described for the nothosaur Ceresiosaurus and for the pistosaur Yunguisaurus, but it remains unclear whether they were used for hearing. Plesiosaurs from the Early Jurassic, such as Plesiosaurus and Stratesaurus are commonly reported to have had narrow stapes. However, from the Middle Jurassic until the clade died out at the end of the Cretaceous, no conclusive examples of plesiosaur stapes have been described.”

The stapes in turtles (Proganochelys)
Sobral et al. 2016 report, “in all post-Triassic turtles, in which the stapedial shaft articulates with the tympanic membrane via a cartilaginous extrastapes. In Proganochelys the medial footplate of the stout, rod-like stapes articulates with the FO, and the lateral aspect of the stapes fits into an articular pocket on the medial side of the quadrate.” In many turtles the quadrate produces a lateral tunnel that supports a tympanic membrane and encloses a tiny rod-like stapes and extrastapes.

Conclusions
Sobral et al. 2016 report, “it is clear that early reptilians did not possess tympanic hearing” and that there were multiple appearances of tympanic hearing. In early tetrapodomorphs and in stem amniotes, the stapes served an important bracing function. The paroccipital process gradually replaced the initial bracing function of the stapes. This replacement is characterized by eventual loss of the dorsal process and reduction in the size of the footplate and in the thickness of the shaft.”

The Sobral et al. observations and summaries of the literature with regard to reptile hearing are important contributions to paleontology. Unfortunately their cladograms of interrelationships are a train wreck… and there’s no reason for that in 2016, six years after the new tree topology was first presented and expanded every since. Given a little time this weekend, I will attempt to separate support stapes from auditory stapes in the LRT.

References
Joyce WG 2015. The origin of turtles: A paleontological perspective. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 324B(3), 181–193. doi:10.110. 1002/jez.b.22609
Sobral G, Reisz R, Neenan JM, Müller J and Scheyer TM 2016. Chapter 8. Basal reptilians, marine diapsids, and turtles: The flowering of reptile diversity, pp.  207–243 in Evolution of the vertebrate ear, Evidence from the fossil record, Volume 59 of the series Springer Handbook of Auditory Research. Eds. Clack JA, Fay RR and Popper AN.

 

Reptile stapes evolution, part 1: terrestrial taxa

I saw this recent publication (Sobral et al. 2016) at
ResearchGate.net. It’s all about the stapes, tympanic membrane and cranial bones that make up the hearing apparatus in reptiles. Unfortunately the cladograms used are, once again antiquated, the product of taxon exclusion and not matched by the large reptile tree (LRT) which produces a completely different tree topology based on magnitudes more taxa, none of which are suprageneric.

From the Sobral et al. abstract
“In this chapter we revise the otic anatomy of early reptilians, including some aquatic groups and turtles. Basal members possessed a stout stapes that still retained its ancestral bracing function, and they lacked a tympanic membrane. The acquisition of tympanic hearing did not happen until later in the evolution of the clade and occurred independently in both parareptiles and diapsids.”

  1. The authors do not include synapsids (including mammals) within the clade Reptilia. They define Repitlia as: “the most inclusive clade containing Lacerta agilis Linnaeus 1758 and Crocodylus niloticus Laurenti 1768, but not Homo sapiens Linnaeus 1758.” Since Lacerta (a lepidosauromorph) and Crocodylus (an archosauromorph) do not have a last common ancestor more recent than Gephyrostegus bohemicus in the LRT, that clade thus includes Homo and the definition is invalid.
  2. The authors retain the clade “Parareptilia” members of which are paraphyletic in the LRT.
  3. The authors confess, “Because of the uncertainty in their relationships, it is difficult to understand their patterns of otic evolution.” There is no uncertainty of relationships within the LRT, online for all to see since 2010.
  4. The authors also report, “Unfortunately, there is as yet no recent, detailed analysis tackling early reptilian phylogenetic relationships.” That detailed analysis is within the LRT, online for all to see since 2010.
  5. The authors agree with Joyce 2015 that turtles are diapsid reptiles, which is not supported in the LRT. Joyce posits Eunotosaurus as a diapsid (it is not) turtle ancestor. Only by massive taxon exclusion is Eunotosaurus a turtle ancestor and only by deriving Eunotosaurus from Archosauria + Lepidosauria (not sister clades) does Eunotosaurus become, in Joyce’s vision, a diapsid.
  6. The authors report “the phylogenetic position of mesosaurs is uncertain.” The LRT has nested them firmly between basal pachypleurosaurs and thalattosaurs + ichthyosaurs for the last 6 years.
  7. The authors report correctly that millerettids are basal to procolophonids and pareiasaurs, but fail to note they are also basal to diadectids and turtles.
  8. The authors lament, “The phylogeny of millerettids is poorly understood.” In the LRT the phylogeny of millerettids is well understood.
  9. The authors do not realize the interrelationship of bolosaurs and procolophonids with diadectids and so ignore the latter or consider them a stem reptile.
  10. The authors ally Delorhynchus and Bolosaurus. The LRT separates them in distinct clades with many intervening taxa.
  11. The authors include Owenetta as a procolophonid, but it is not closely related in the LRT.
  12. The authors note, “The phylogenetic relationships of basal diapsid clades are still controversial, and their early evolutionary history remains poorly understood.” In the LRT their is no controversy and relationships are well understood. Part of their confusion stems from the fact that the authors do not yet realize the Diapsida is diphyletic, with lepidosauromorph diapsids unrelated to archosauromorph diapsids in the LRT.
  13. The authors note the exact phylogenetic position of the genus Youngina is uncertain. In the LRT several specimens are employed and every position is certain.

Figure 1. Antiquated cladogram (Sobral et al. 2016) of basal reptile relationships.

Figure 1. Antiquated cladogram (Sobral et al. 2016) of basal reptile relationships. If you’re familiar with the taxa at ReptileEvolution.com you’ll see the morphological mismatches, the nesting of derived taxa at basal nodes, the use of suprageneric taxa and worst of all, a large swath of taxon exclusion.

The stapes in Captorhinus
After describing the stapes of Captorhinus as “massive and complex with a much expanded footplate” the authors note that in more basal unnamed captorhinids, “the shafte of the stapes is long and narrow.”

The stapes in Parareptilia
The authors consider Erpetonyx “the oldest parareptile” which they date from the latest Carboniferous. The LRT nests Erpetonyx with Broomia and Milleropsis as stem diapsids. The authors claim that “Parareptilia includes groups that were among the first reptilians to evolve herbivory and associated modified feeding mechanisms,” but then they include Mesosaurs as basal parareptiles and excluded the herbivorous captorhinids. The nonsense continues unabated. The authors report, “This group shows many evolutionary novelties that parallel and predate those seen in other amniote groups. Among those novelties are the independent acquisition of tympanic hearing and impedance-matching hearing.”

The stapes in mesosaurs
The authors report, “their otic region is poorly known.”

The stapes in millerettids
The authors report, the braincase of Milleretta is very similar to that of Captorhinus. In the LRT basal captorhinids and Milleretta are separated by only a few intervening taxa. “The stapes is very different. It is stout and bears a rather narrow footplate and a very short shaft. The shaft expands significantly distally to become wider than the footplate. The stapes does not contact the quadrate.”

The stapes in bolosaurids, pareiasauromorphs and procolophonids
The authors report, “they otic morphology is not well understood. In Delorhynchus” (actually closer to Eunotosaurus and Acleistorhinus) “the stapes resembles closely that of Captorhinus.” In the LRT they are somewhat related, not close, not far. In Procolophon, “the stapes is very short, but the distance of the distal end from the deep, well-developed otic notch may indicate that it was much longer.”

The authors report, “pareiasauromorphs have very prominent otic notches indicating the undoubted presence of a large tympanic membrane.” Pareiasaurs have a notch hidden from lateral view by the quadratojugal flange. Closely related Macroleter and Emeroleter have a prominent notch, but it is framed by the supratemporal, postorbital, squamosal and quadratojugal. The authors only mention the latter two. In Macroleter, the authors report, “The stapes bears a small footplate. Although the shaft is long, it would have had no close contact with the lateral side of the skull. The shaft is also very slender.” 

In Pareiasuchus, a very well-preserved pareiasaur skull, a stapes was not preserved. In another pareiasaur, Deltavjatia, “The preserved part of the stapes is very short, and the footplate is formed by two articular surfaces separated by a sulcus.”

The stapes of basal diapsida
The authors report, “There is no evidence of a tympanic ear in these early diapsids” (Petrolacosaurus and Araeoscelis).They lack an otic notch and have a laterally or ventrally oriented stapes with a dorsal process. In fact, the stapes seems to have functioned more as a support for the jaw joint, directly or indirectly.”

In Youngina (but which one??), “The stapes is very long and robust. There is no sign of an osseous dorsal process and the shaft is perforated by a large foramen for the stapedial artery. The footplate is separated from the shaft by a poorly defined neck. It is not much larger than the shaft itself. The shaft is long and slender and appears to extend laterally toward a slight emargination of the squamosal-quadrate complex. An imperforate, ossified extrastapes has also been identified.”

The stapes in marine diapsid reptiles
we’ll look at those tomorrow.

The stapes in the basal amniotes, Gephyrostegus and Silvanerpeton
have not been identified in the literature. This is very strange if the stapes in these two is supposed to be a robust jaw-supporting bone.

References
Joyce WG 2015. The origin of turtles: A paleontological perspective. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 324B(3), 181–193. doi:10.110. 1002/jez.b.22609
Sobral G, Reisz R, Neenan JM, Müller J and Scheyer TM 2016. Chapter 8. Basal reptilians, marine diapsids, and turtles: The flowering of reptile diversity, pp.  207–243 in Evolution of the vertebrate ear, Evidence from the fossil record, Volume 59 of the series Springer Handbook of Auditory Research. Eds. Clack JA, Fay RR and Popper AN.