New publication: Triassic stem caecilian supports dissorophoid origin of living amphibians (Kligman et al., 2023; Nature)
Title: Triassic stem caecilian supports dissorophoid origin of living amphibians
Authors: B.T. Kligman, B.M. Gee, A.M. Marsh, S.J. Nesbitt, M.E. Smith, W.G. Parker, & M.R. Stocker
General summary: The origin of modern amphibians (frogs/toads, salamanders/newts, caecilians), which are more often termed 'lissamphibians' by scientists to differentiate from the more ambiguous 'amphibians,' has long been a vexing problem. The three modern groups are remarkably morphologically disparate, which makes it hard to both confidently identify and conceive of the ancestral lissamphibian. Lissamphibians today are also relatively small, a pattern thought to have characterized much of their evolutionary history and also an attribute that predisposes their remains to not have been fossilized. Exacerbating this is the extremely poor record of caecilians, which, even today, are a rather cryptic group found only in the equatorial regions and that typically burrow, making them rather hard to observe. Burrowing animals, especially those that not only burrow but that spend much of their lives underground, also have a poor fossil record, which compounds the problems for caecilians. The first caecilian fossils were not even reported until 1972 (previous reports were a misidentifed catfish spine and a misidentified cephalopid, respectively), and to date, there are less than a dozen distinct occurrences of fossil caecilians known globally over an 180 million year interval.
In this study, led by my colleague and current Virginia Tech PhD student Ben Kligman, we report nearly 100 new specimens of the earliest known caecilian in the fossil record from a single Late Triassic site in Petrified Forest National Park, Arizona. Although no complete skulls or skeletons are known, numerous fragments preserve unequivocally diagnostic features found only in caecilians, such as a jaw comprised of largely fused elements that remain separate in other tetrapods and two rows of small teeth with a distinctive feature called pedicelly – a dividing zone at the mid-height of the tooth that often leads the tips to be lost during preservation. This occurrences pre-dates the previous oldest occurrence of caecilians by at least 35 million years and provides new insights into the early stages of the group's evolution. In particular, the new fossils appear to capture the transition toward the modern caecilian condition in which there is extensive co-ossification of multiple elements to form a more consolidated skull (good for burrowing). Their occurrence in Arizona, which was positioned close to the equator in the Late Triassic, suggests that an origin within the equatorial belt also constrained their dispersal, therein offering an explanation as to why caecilians remain tied to these regions when frogs and salamanders have nearly a global distribution except at the poles (and Australia for salamanders).
Sleuthing the specialized
Elucidating the evolutionary origin of highly specialized organisms has been a persistent challenge for evolutionary biologists and paleontologists because the patchy fossil record often obscures the gradual transition from a generalized "ancestral" form to the observed specialized one. Fossils that fill in these gaps, often dubbed "transitional fossils," contribute substantive information by their mixture of features, but it is not as if one can simply declare, "today I will find this transitional fossil" and then actually do so. For this reason, the evolutionary origins of various groups of living tetrapods like turtles and snakes has remained contentious to even the present day; we simply lack enough transitional fossils or cannot be certain that a given fossil truly represents a transition, rather than a convergence on a similar body plan (e.g., a long body with greatly reduced or entirely absent limbs occurs across many different groups of animals, not just snakes). It's only within my parents' lifetime that the notion that birds descended from dinosaurs became the accepted consensus, which today's 5-year-olds know by heart.
One of the most vexing origin stories is that of modern amphibians, collectively termed "lissamphibians." There are three living groups of lissamphibians: the worm-like caecilians, which are poorly-known to scientists and the public alike; frogs (of which toads are a subset); and salamanders (of which newts are a subset). The simple explanation for the ongoing uncertainty is how different these three groups look – one has entirely lost its limbs, another has lost its tail and shortened its body; and the third looks like a prototypical tetrapod (salamanders are often confused for lizards because people don't think amphibians have tails). As a result, it is difficult to figure out what a transitional form to one or all three would look like – does the common ancestor of these three groups have a long or short body, a tail or no tail, etc.
Both fossil and modern amphibians are on the smaller side of the tetrapod scale; consider that the recent capture of the new recordholder for the largest living toad (who was promptly euthanized due to being an invasive species in Australia) was for a cane toad weighing just under 6 lbs, or roughly equivalent to a large chihuahua (the healthy ones, not those severely obese ones you see in kitschy Route 66 hotels sometimes). Their skeleton is rather fragile, and in early stages of life (e.g., the tadpole stage of frogs), has not even solidifed into bone. This makes them poor candidates for fossilization, which is why the fossil record of caecilians and frogs is atrocious; salamanders benefit only from apparently taking up residence in the lakes that lended themselves to lagerstätte like in the Jurassic of China. However, whereas salamanders and frogs become increasingly well-documented towards the present-day, caecilians remain nearly invisible in the fossil record.
Needle in a haystack
It is no exaggeration to say that among the various groups of living tetrapods, caecilians have one of the worst fossil records. There are fewer than a dozen definitive occurrences of fossil caecilians between the Early Jurassic and the present day, fewer than 10 of which have been published in full. Until 1972, there were no published records of fossil caecilians from even recent history. The below summary figure showing the temporal distribution of published fossil caecilian records. Six of the nine records shown here are just vertebrae, and only Eocaecilia micropodia, known from several dozen specimens on the Navajo Nation of Arizona, is represented by any appreciable number of specimens.
The fossil record of caecilians likely owes to a combination of a lot paleobiological attributes that are all disadvantageous for their preservation. As discussed above, the small size of lissamphibians reduces their odds of being preserved. Where caecilians differ from most other lissamphibians is that they are fossorial, meaning they live underground (e.g., within leaf litter or soil) by burrowing with their heads (they have no limbs to speak of). If their extinct relatives had similar ecologies, which seems likely given the many skeletal adaptations for this ecology, they would not be inhabitating areas that are frequent sites of preservation of skeletal remains, like rivers or lakes. It is no coincidence that freshwater aquatic animals like various temnospondyls and crocodilians have a pretty good fossil record. Lastly, modern caecilians are predominantly found in the tropics. These regions, while home to some of the greatest biodiversity in terrestrial environments, are also not very conducive to fossilization because humid/moist environments promote rapid decomposition of remains. Add these up and you have a recipe for a depauperate fossil record.
The funky worm
With nearly a hundred specimens attributed to Funcusvermis (and many more that were subsequently picked out of the sediment after we had begun finalizing this paper), we've nearly doubled the entire fossil record of caecilians based on specimen number, all from just a single remarkable site in the middle of the Arizona desert. The below figures show the relative abundance of specimens and individuals of Funcusvermis to the rest of the caecilian fossil record.
This isn't a case of many elements of a few individuals as well. The site's (published) MNI is established at a whopping 76 individuals based on lower right jaw elements (pseudodentaries), increasing the number of distinct caecilian individuals represented in the fossil record by an even greater magnitude. For some reason, nearly all of the elements are from the right side of the body, a skew that wouldn't be expected using a thorough process like screenwashing in which there's careful sorting of both fragmentary and complete elements of all taxa (this is the one time that people don't throw the temnospondyls out). We're still figuring that part out...
So...what about Chinlestegophis?
Perhaps the best place to start with "where does Chinlestegophis stand now" is to discuss where Chinlestegophis stood before this. Acceptance of the hypothesis of lissamphibian origins has been tepid at best and practically non-existent at worse. Per Google Scholar, Pardo et al. (2017) has been cited 62 times. When you cut out unidentified duplicate entries, theses/dissertations, preprints, and conference abstracts, the number comes down to 50 (there are a few that it misses that ResearchGate catches). Somehow, I think I am the most frequent citer of this paper actually – 13 first-authored papers that do so. Nearly all of these citations, mine included and particularly those from paleontologists, are "neutral" – they profess no personal stance on the hypothesis of Pardo et al. and do not attempt to directly tackle the question. Some examples:
All of this is to say that, like Anderson et al.'s (2008) polphyly hypothesis, the diphyly/new polyphyly (depending on how you want to cut it) hypothesis is not exactly causing anyone to rewrite any textbooks, and it has not gained really even marginal acceptance among workers not affiliated with the study.
With that being said, I would summarize my opinion of Chinlestegophis, which hasn't really changed over the years, as an "interesting and plausible idea that fills some notable conceptual / data gaps but that is not well-supported quantitatively or phenetically." I won't beat the proverbial horse again on the phylogenetic bits, which are re-summarized briefly in our supplemental data, but I will spend some time going through the qualitative comparisons and arguments (but read the supplement, I wrote a lot more in there).
A comparison of the distribution and anatomy of a lateral exposure of the palatine (LEP, rare in temnospondyls) and the loss of a distinct lacrimal. b, The dvinosaur Thabanchuia oomie. c, The amphibamid Doleserpeton annectens. d, The ‘dendrerpetid’ Dendrerpeton helogenes. e, The trematosaur Wantzosaurus elongatus. f, The dvinosaur Acroplous vorax. g, the rhytidosteid Laidleria gracilis. h, Chinlestegophis jenkinsi. i, Acroplous vorax in lateral view. j, Rileymillerus cosgriffi in lateral view. k, Chinlestegophis jenkinsi in lateral view
Most of my reservations have more to do with how Chinlestegophis is compared to other temnospondyls and caecilians, rather than the anatomical interpretation of Chinlestegophis (at least Schoch et al., 2020, dispute their identification of a lateral exposure of the palatine). I find many of the favorable comparisons made by Pardo et al. to either be oversimplifications or mischaracterizations. Let's take two examples of co-ossification that are proposed to be shared between Chinlestegophis and some other tetrapods:
Trapped in the middle
Today, caecilians occur within a narrow latitudinal belt (27° N and 34° S), and their fossil occurrences are bracketed between what would have been around 16° N and 27° S. This constrasts sharply with both the fossil and extant distribution of frogs and salamanders, the former of which make it nearly to the poles. Understanding the present distributions of different groups of tetrapods necessarily requires a look into the deep past to understand how the continents were arranged and how different organisms could or could not get around.
Figure 2 from the paper, showing: a, Biogeographic history of Gymnophionomorpha and Triassic batrachians; yellow indicates living caecilian distribution. b, Time-calibrated topology of lissamphibian relationships showing major divergences (topology derived from refs. 6,23,38). Estimated molecular divergence dates for major divergences are shown as blue circles (Gymnophionomopha–Batrachia divergence without Gerobatrachus calibration; Supplementary Table 4), pink circles (Gymnophionomopha–Batrachia divergence with Gerobatrachus calibration; Supplementary Table 5), yellow circles (Salientia–Caudata divergence; Supplementary Table 6) and green circles (Rhinatrematidae–Stegokrotaphia divergence; Supplementary Table 7); coloured vertical bars show the average for each set of divergence estimates. Numbered white and orange circles correspond to occurrences in Supplementary Tables 2 and 3, respectively. Crosses indicate extinct taxa.
All lissamphibians are susceptible to drying out because of their wet skin and their use of it to breath (cutaneous respiration), but caecilians are particularly susceptible to dry environments, which is one reason they spend a lot of their time below ground where it's more humid/damp. Even though caecilians were already established at a time when the continents were largely still connected, allowing the dispersal of all sorts of different organisms around the world, that their fossil occurrences remain tied to this narrow equatorial belt indicates that early caecilians were also more climatically sensitive than other lissamphibians, and thus, that caecilians' present distribution has been strongly constrained by the presence or absence of humid environments. It's a strong reminder of the ways in which the past directly shapes what we observe in the present and underscores the importance of studying the deep time record of the planet and its inhabitants in order to really understand how we ended up with today's ecosystems.
About the blog
A blog on all things temnospondyl written by someone who spends too much time thinking about them. Covers all aspects of temnospondyl paleobiology and ongoing research (not just mine).