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

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