Ontogenetic bone growth in the caecilian skull

Back to an old subject…
Earlier we looked at the skull of Dermophis, an extant caecilian from Mexico (Fig. 1) based on Digimorph.org images. There were comments from anamniote experts criticizing my labeling of the bones, suggesting I had a ‘magic fusion detector.’ I was encouraged to check out Wake and Hanken 1982, which documents the growth of the Dermophis skull (Fig. 2).

Figure 1. Dermophis, the extant Mexican caecilian, with bones, even if fused to one another, identified. The quadratojugal and squamosal are absent. Black and white image from Digimorph.org. Coloring the bones makes them so much easier to read and understand.

Figure 1. Dermophis, the extant Mexican caecilian, with bones, even if fused to one another, identified. The quadratojugal and squamosal are absent. Coloring the bones makes them so much easier to read and understand. Skull from Digimorph.org and used with permission.

Wake and Hanken discuss
some of the earlier hypotheses regarding the origin of the skull bones in caecilians. “The belief of Marcus et al, (’35) that the well-developed skull of caecilians is a retained primitive feature has been challenged by many authors, however, all of whom interpret the stegokrotaphy of the caecilian skull as being secondarily derived from a reduced skull typical of other Recent amphibians.”

Unfortunately for Wake and Hanken,
the publication of Eocaecilia (Jenkins and Walsh 1993; Eaerly Jurassic, 190 mya) came eleven years later. That settled the issue.

Figure 1. Dermophis skull elements according to Wake and Hanken 1982.

Figure 2. Dermophis skull elements according to Wake and Hanken 1982. Two of the larger growth series specimens  are shown here,  Red = pterygoid/quadrate. Also shown are the source of the fused bones based on phylogenetic relationship to Acherontiscus. Note the green ellipse = supratemporal, as in Eocaecilia.

Eocaecilia retains
the supratemporal and postfrontal, two bones thought by Wake and Hanken to have been absent in recent amphibians including caecilians. However, the elliptical supratemporal and the strip-like postfrontal both become temporarily visible in the 6.85 cm immature skull and then become fused to what Wake and Hanken label the squamosal. Their squamosal encircles the tiny orbit. Squamosals usually do not do that on their own, as everyone familiar with tetrapods knows. It doesn’t even contact the squamosal in Eocaecilia.

Figure 1. Eocaecilia skull with original and new bone identifications based on comparisons to sister taxa listed here. Like Brachydectes, the jaw joint has moved forward, beneath the jugal now fused to the quadratojugal creating a long retroarticular process, otherwise rare in amphibians. Also rare is the fusion of the squamosal with the postorbital.

Figure 3. Eocaecilia skull with original and new bone identifications based on comparisons to sister taxa listed here. Like Brachydectes, the jaw joint has moved forward, beneath the jugal now fused to the quadratojugal creating a long retroarticular process, otherwise rare in amphibians. Also rare is the fusion of the squamosal with the postorbital.

Wake and Hanken reported:
“Our analysis of skull development in Dermophis has several implications for this controversy. First, as presented above, we did not observe several of the embryonic ossification centers whose supposed presence has been used to ally caecilians and early amphibians, particularly the microsaurs.” Again, they did not have the blueprint of Eocaecilia to work with, as we do now. They did not mention the microsaur, Acherontiscus (Carroll 1969; Namurian, Carboniferous; Fig. 4), in their paper. This taxon phylogenetically and chronologically precedes caecilians in the large reptile tree (LRT). Microbrachis is also related, but has a shorter torso and longer legs than Acherontiscus and Eocaecilia.

Figure 4. Acherotisicus has large cheek bones (squamosal, quadratojugal) that appear to fuse in Eocaecilia and Dermophis.

Figure 4. Acherotisicus has large cheek bones (squamosal, quadratojugal) that appear to fuse in Eocaecilia and Dermophis.

Earlier I used the term bone ‘buds’
to represent small ossification centers from which the adult skull bone would eventually develop. This term caught some flak, but as you can see (Fig. 2) the adult skull bones do indeed develop from smaller ‘buds’.

Wake and Hanken concluded:
“We heartily concur with the idea of a long and separate evolutionary history for caecilians, independent of frogs and salamanders, as has been expressed by Carroll and Currie (’75). However, the resemblances between the cranial morphology of caecilians and that of their purported ancestors, the microsaurs, are only superficial, and many significant differences remain. Further, there are real differences in the postcranial elements, which were not within the purview of Carroll and Currie’s study. Based on our observations of skull development in Dermophis mexicanus, we believe that there is now little evidence for the hypothesis of primary derivation of the caecilian skull from any known early amphibian group.”

So Wake and Hanken gave up —
but this was before the advent of widespread computer-aided phylogenetic analysis, Now, like flak itself, you don’t have to actually hit a target. You can get really close and still knock it down. So ‘superficial’ resemblances, if nothing else in the gamut of included taxa comes closer, become homologies. That’s what happens in the LRT.

Based on what Wake and Hanken 1982 wrote,
skull buds are not apparent. Based on what Wake and Hanken 1982 traced, skull buds for all pertinent bones are indeed present.

And caecilians are cemented down
as living microsaurs close to Eocaecilia, Acherontiscus and Microbrachis based on morphology, phylogeny and ontogeny.

References
Jenkins FA, Walsh DM and Carroll RL 2007. Anatomy of Eocaecilia micropodia, a limbed caecilian of the Early Jurassic. Bulletin of the Museum of Comparative Zoology 158(6): 285-366.
Jenkins FA and Walsh M 1993. 
An Early Jurassic caecilian with limbs. Nature 365: 246–250.
Marcus H, Stimmelmayr E and Porsch G 1935. Beitrage zur Kenntnis der Gymnophionen. XXV. Die Ossifikation des Hypogeophisschddels. Morphol. Jahrb. 76;375-420.
Wake MH and Hanken J 1982. Development of the Skull of Dermophis mexicanus (Amphibia: Gymnophiona), With Comments on Skull Kinesis and Amphibian Relationships. Journal of Morphology 173:203-222.

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4 thoughts on “Ontogenetic bone growth in the caecilian skull

  1. Some other caecilians do have a separate postfrontal or “circumorbital” that encircles the orbit or most of it. No trace of a supratemporal anywhere, though, neither in adults nor in embryos.

    Also shown are the source of the fused bones based on phylogenetic relationship to Acherontiscus.

    Thank you for admitting that part of your interpretation of Dermophis is not based on evidence from Dermophis in the first place.

    Earlier I used the term bone ‘buds’

    The criticism here is that “bud” already means something else in development biology. It involves outgrowths from the body surface. Dermal bones form flat, in the flat dermis. Calling an ossification center a “bud” is really strange.

    BTW, no way is Acherontiscus a microsaur, whether or not there’s a clade that deserves that name in the first place.

  2. Determining the homology of skull elements is difficult, particularly when we’re comparing Paleozoic taxa with large numbers of dermal bones to post-Paleozoic taxa with reduced complements of bone.

    However, homology interpretation is a complex process and one which requires substantial self-doubt and independent justifications for one’s interpretations. How one interprets homologies has direct implications for phylogeny, so it pays to have very solid bases for homology assignments. One cannot draw homology assignments ad hoc through comparisons with animals you want to be their relatives, as that will bias subsequent analyses in favor of those interpretations.

    The way we typically have to do this in paleontology is to find specific osteological correlates of soft tissue landmarks that are always associated with an element. In practice, this is very difficult to do because many dermal bone elements are not actually associated with specific structures. So, we can do this more confidently with the braincase and palate, but when it comes to the dermal skull homology statements are often guesswork. A good example of this is the single bone of the temporal series in many ‘microsaurs’, which may be a tabular or may be a supratemporal….we have no way of distinguishing these at all.

    But when we have modern taxa, we have some extra tools. Development is one of those tools; certain bones come from certain tissues, so we can trace that and use it to make decent educated guesses of how the original tissue got there. In the case of membrane bones, it is still sometimes difficult to identify what bone primordia represent (there are no “buds”….”bud” has a very specific meaning in development that has been used for almost 200 years. You cannot just redefine it offhand). However, we can use a number of high-tech and low-tech methods to trace where cells come from and how they get to the site of eventual ossification, and that can help us discern between certain bones.

    With caecilians, a lot of that work has been done. While not all of it has (there’s still a lot of unsettled questions) we have to address these problems using the more accurate and precise developmental techniques and not simply guessing.

    Pretending that your tracings can usurp the very careful and very high quality work that Wake and Hanken have done is arrogant and incorrect. The findings of Wake & Hanken (and other comparative embryologists) do not conflict with the interpretations of Eocaecilia by Jenkins et al. 2007 or subsequent studies. Moreover, we have independent developmental data for modern caecilians, but do not have that for Eocaecilia, so if anything we should be using modern caecilians to interpret the Jurassic ones. Which is precisely what all workers to date have done.

    As for the open/closed skull issue, that has been addressed in a number of recent papers by Hillary Maddin and Thomas Kleinteich. The conclusion really is that it’s impossible to figure out what the basal condition is for caecilians (modern early-diverging caecilians are zygokrotaphic i.e. have an open skull, Eocaecilia does not, and the common ancestor of Eocaecilia and modern caecilians cannot be easily inferred. Open and closed skulls are both credible hypotheses, in contrast to the ideas of some workers in the 70s and 80s (e.g. Nussbaum 1983, who argued that caecilians must have come from a lysorophian-like ancestor because he could not see a way for them to evolve from an ancestor without an open cheek). This is an unresolved issue, in large part because we do not have a good credible sister group to Eocaecilia+Caecilians.

    I’m glad you’re interested in Acherontiscus. It’s an intriguing little animal. However, it is very small, not exceptionally preserved, and difficult to interpret. I believe it is currently under study, but if not, it definitely will be soon. The illustrations are not necessarily reliable and devising a large-scale hypothesis of tetrapod evolution on the basis of this very tenuous specimen will likely mislead you, especially if you’re using tenuous interpretations of Acherontiscus to guide homology interpretations elsewhere. Using an extremely poorly understood fossil animal (Acherontiscus) to reinterpret a very well-preserved fossil animal (Eocaecilia), and the using those to inform homology statements concerning a modern animal that can be raised and bred in the bad (Dermophis) is absolutely the wrong direction to be drawing these inferences.

    I have no problem with heterodox hypotheses of vertebrate evolution. I have no problem with heterodox homology statements. But you absolutely need to do your due diligence and make 100% certain that you are taking your inferences in the right direction. Additionally, it is absolutely critical that you do not use an ad hoc preferred phylogeny to reinterpret homology and thus “confirm” your own phylogenetic preferences. Which is unfortunately exactly what you’re doing here.

    This is likely to be my final response, as this is a distraction from work that I need to be doing and my efforts are mostly falling on deaf ears. I realize that you have personal reasons for not liking some of the dinosaur and bird community, and that this has shaped some of your skepticism of prior work, but please recognize that most of us work very hard, do due diligence to ensure that our interpretations are as correct as possible, and try not to overinterpret ambiguous features. Please take the time to understand why people have made the interpretations they have, rather than glancing at a drawing and assuming that the rest of us are simply incompetent. Thank you.

  3. The Wake & Hanken paper is here. The text describes the ontogenetic origin of the skull bones. Fig. 1c is where you found a “supratemporal”; it’s simply the lateral margin of the palatoquadrate cartilage.

    That’s right: it’s a two-dimensional drawing. (Amazingly few scientists are any good at shading or think it’s worth the effort.) You can still see that the palatoquadrate lies ventral to the eye and to the otic capsule on both sides of the head.

  4. Thank you, Jason and David.
    I understand that the skull of caecilians is likely the most derived of all tetrapod skulls. I am not UP on all the literature, but I do rely on phylogenetic analysis to eliminate improbabilities and shed light on possibilities. These I present.

    I don’t have personal reasons for not liking some of the dinosaur and bird community. I simply have a healthy skepticism for everything presented in Science — which is what you have and how it should be.

    David, not sure why you said the palatoquadrate is ventral to the eye in the dorsal view drawings of D. mexicanus. The labels in the paper say otherwise, but, to your point, I do realize the quadrate and palatal bones are fused and some of them extend far forward of the quadrate.

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