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

Leave a Reply

Fill in your details below or click an icon to log in:

WordPress.com Logo

You are commenting using your WordPress.com account. Log Out /  Change )

Google photo

You are commenting using your Google account. Log Out /  Change )

Twitter picture

You are commenting using your Twitter account. Log Out /  Change )

Facebook photo

You are commenting using your Facebook account. Log Out /  Change )

Connecting to %s

This site uses Akismet to reduce spam. Learn how your comment data is processed.