Sunday, December 15, 2019

What Good is Less Than Half a Beak?

One of the many distinctive features of modern birds is their complete lack of teeth, their jaws instead being sheathed in a keratinous beak. Modern birds are not the only beaked dinosaurs though; beaks have also been found in ornithischians, therizinosaurs, ornithomimids, caenagnathoid oviraptorosaurs, and confuciusornithiforms, just to name a few major groups. However, all of these examples appear to have acquired beaks independently; their beaks were not directly related to those of modern birds.

The beaks that did give rise to those of modern birds appear to have arisen relatively late, corresponding to the origin of the clade Euornithes*, which includes neornitheans (modern birds) and everything more closely related to them than to the enantiornitheans or "opposite birds". Contrary to a lot of paleoart, however, the beak in most non-neornithean euornitheans did not take up most of the jaw like it does in modern birds. Instead, both their upper and lower jaws generally had a short toothless section at the jaw tips; it is likely that the euornithean beak was originally restricted only to this small region.

*In recent literature, the most popular name for this group is Ornithuromorpha, which was originally named in 1999 and defined in 2002 as the clade uniting Patagopteryx and modern birds. Under the results of most phylogenetic studies, this would actually refer to a slightly smaller group within Euornithes instead of being equivalent to Euornithes itself. Furthermore, given that Euornithes was both named (in 1889) and explicitly defined as the "closer to modern birds than enantiornitheans" clade (in 1998) earlier than Ornithuromorpha was, I favor its use here.

The toothless portion of the lower jaw in non-neornithean euornitheans was particularly curious. In most vertebrates, the frontmost bones in the lower jaw are the dentaries. The toothless tip of the lower jaw in non-neornithean euornitheans, however, was composed of a small separate bone that lay in front of the dentaries, appropriately called the predentary.

The predentaries of various euornitheans, from Bailleul et al. (2019). The middle and right columns show the front end of each skull under microcomputed tomography (microCT) scanning. (And look, there's cranial material of Gansus!)

Not many vertebrates have a predentary. Some types of fish (such as marlins) have one, as did ornithischian dinosaurs. As many dinosaur geeks are eager to point out, even though ornithischians are known as "bird-hipped dinosaurs", birds are not ornithischians. The similarities between the hips of birds and ornithischians evolved convergently, and so too did the predentary.

Given that modern birds lack a separate predentary, and similar structures have only been found in fairly distantly related groups, analogues for the anatomy and function of the euornithean predentary are limited. In a recent study, Alida Bailleul and colleagues took the predentary from a specimen of the Cretaceous euornithean Yanornis and examined it in detail. They scanned the bone at extremely high resolution, took sections of it to view it in cross section under a microscope, and treated it with chemicals that react to specific tissue components.

The jaw tips of Yanornis, with special focus on the predentary (labeled "pd"), from Bailleul et al. (2019).

These methods allowed Bailleul et al. to identify traces of cartilage on both the predentary and dentaries of Yanornis where these bones would have attached to one another. The specific type of cartilage that forms on the dentaries is secondary cartilage, which generally forms at mobile joints that experience compressive forces. This, along with the shape of the bones themselves, led the authors to conclude that the euornithean predentary could move independently of the rest of the jaw, which has been previously suggested by other researchers. (Interestingly, this would provide another parallel with many ornithischians, in which the predentary allowed each half of the lower jaw to rotate along their long axes. In ornithischians, however, this movement probably occurred during chewing, which we have no evidence that any euornithean ever did.)

Unfortunately, we don't currently have enough information to reconstruct exactly what type of motion the euornithean predentary would have been capable of. However, this does imply that the predentary could have played a role in manipulating and processing food. Furthermore, Bailleul et al. identified canals for blood vessels and nerves that would have entered the predentary from the dentary, suggesting that the predentary could have also had a sensory function.

3D reconstruction of the dentary tips and predentary of Yanornis, from Bailleul et al. (2019). Blue represents patches of cartilage on the dentaries, whereas purple represents a patch of cartilage on the predentary.

Yanornis is known to have eaten fish, and it's not hard to see how a sensitive jaw tip might have helped it detect its prey. The authors point out that a piscivorous diet was probably not typical of all non-neornithean euornitheans though, so the mobile and sensory properties of the predentary were likely advantageous for euornitheans adopting a wide variety of ecologies. They could have even come in handy during behaviors other than feeding, such as preening and nest building.

Bailleul et al. note that the predentary in euornitheans is almost always paired with a corresponding toothless tip of the upper jaw. This may indicate that these two features were functionally linked. However, just a few weeks before the publication of Bailleul et al.'s study, a new Cretaceous euornithean, Mengciusornis, was described. Mengciusornis deviated from the usual euornithean pattern by having teeth at the tip of its upper jaw (in fact, it only had teeth at the tip of its upper jaw), and yet it still had a predentary. Perhaps, though, this is actually a point in favor of the idea that the predentary could be beneficial for many disparate feeding strategies.

Some euornitheans that don't appear to have much use for the predentary are the ones that lost teeth entirely. In addition to modern birds, a number of other euornitheans had independently evolved toothlessness, including Archaeorhynchus, Schizooura, Eogranivora, and Xinghaiornis, and it seems that none of these had a predentary. (The purportedly toothless Dingavis may preserve a surface at the tips of the dentaries where a predentary could have been present, but its describers also mention that they can't reject the possibility that it had small teeth.)

So what happens to the predentary in such taxa? Does it simply fail to form entirely? Does it fuse with the rest of the lower jaw? It would be interesting to find out whether any trace of the predentary can be detected in the developing embryos of modern birds. Bailleul et al.'s paper is by far the most detailed study on the euornithean predentary to date, but it's evident that there's much we still don't know about this interesting piece of avian evolution. I look forward to future research that aims to shed light on this enigmatic bone.

Reference: Bailleul, A.M., Z. Li, J. O'Connor, and Z. Zhou. 2019. Origin of the avian predentary and evidence of a unique form of cranial kinesis in Cretaceous ornithuromorphs. PNAS 116: 24696-24706. doi: 10.1073/pnas.1911820116