New Publication: Computed tomographic analysis of the cranium of the early Permian recumbirostran 'microsaur' Euryodus dalyae reveals new information of the braincase and mandible (Gee, Bevitt, & Reisz; Papers in Palaeontology)

Title: Computed tomographic analysis of the cranium of the early Permian recumbirostran 'microsaur' Euryodus dalyae reveals new information of the braincase and mandible.
​Authors: B.M. Gee, J.J. Bevitt, R.R. Reisz
Journal: Papers in Palaeontology
DOI to paper: 10.1002/spp2.1304

Holotype of Euryodus dalyae in dorsal and lateral views (fig. 1 from the paper).

​General summary: Yes, this is a long title. No, this is not a temnospondyl. I thought I was done with 'microsaurs' with Llistrofus. That has not panned out. So here we are...
   Here is more CT of another 'microsaur,' this time the gymnarthrid Euryodus dalyae (with bonus friends from Richards Spur)! This continues what is now a longstanding trend of zapping 'microsaurs' - to date, descriptions via CT data have been made for Quasicaecilia (Pardo et al., 2015), Carrolla (Maddin et al., 2011), Rhynchonkos, Aletrimyti, and Dvellecanus (Szostakiwskyj et al., 2015), Huskerpeton (Huttenlocker et al., 2011), Brachydectes (Pardo & Anderson, 2016), and Llistrofus (Gee et al., 2019), which is way more sampling than anybody's done for a particular temnospondyl clade... Here we scanned the holotype of Euryodus dalyae, a 'microsaur' from the early Permian of Oklahoma (but not Richards Spur) and a specimen from Richards Spur that was identified as E. dalyae. This provides the first published data on gymnarthrid 'microsaurs' and revealed a number of intriguing features, such as extensive ossification of the braincase, as seen in many recumbirostrans, and a second tooth row on the lower jaw, a feature that's never been reported in 'microsaurs.' 

Gymnarthrids 101

First off, if you want a little more about 'microsaurs,' pop over to my summary of my PeerJ paper on Llistrofus from last year. We're back with more 'microsaur' magic, this time on the gymnarthrid Euryodus. In the longstanding debate over whether 'microsaurs' are in fact crown amniotes, not stem amniotes or stem lissamphibians, gymnarthrids are of great interest because they're among the most similar to eureptiles among the recumbirostrans (derived 'microsaurs' with recumbent snouts for digging). Specifically with respect to Richards Spur, material of Euryodus was long thought to be fairly common based on distinctive bulbous teeth until those teeth were found attached to the jaw of a captorhinid eureptile, Opisthodontosaurus (Reisz et al., 2015). Recumbirostrans are a weird batch, so gymnarthrids are sort of the "normal ones" - they don't have giant holes in their head like hapsidopareiids or lysorophians or extensively co-ossified braincases like brachystelechids or deeply vaulted skulls like ostodolepids. They're just sort of flat and uh...triangular. What gymnarthrids do have is that they're fairly common. A lot of other recumbirostrans are only known from one or two specimens, but there's a fair bit of Euryodus and its occasional doppelgänger, Cardiocephalus, floating around the early Permian of Texas and Oklahoma. We don't know too much about ontogeny in recumbirostrans, but the gymnarthrids are some of the few taxa where we have at least some info (Anderson & Reisz, 2011). 

Skull of a referred specimen of Euryodus sp. from Richards Spur in...all of the views (figs. 7-8 from the paper).

The many flavours of Euryodus

The Euryodus of this paper, Euryodus dalyae, isn't the OG Euryodus; that honour belongs to Euryodus primus from the early Permian of Texas, named in 1939 by American paleontologist Everett Olson. Another species of Euryodus, E. bonneri, was described from Kansas in 1981, but it was recently (well not too recently I suppose) demonstrated to be a different taxon, Proxilodon (Huttenlocker et al., 2013). Euryodus dalyae comes from Oklahoma, but not originally from Richards Spur; instead, it comes from the fairly notable South Grandfield locality. It was first described as Cardiocephalus cf. C. peabodyi, which speaks to the similarities between these genera (Daly, 1973), but it was subsequently named as a species of Euryodus after (Eleanor) Daly in 1978 by Bob Carroll and Eleanor Gaskill in 1978. Euryodus dalyae was reported from Richards Spur by MacDougall et al. (2017), which was apparently based on my advisor seeing the above specimen labeled as such in collections; there is no other published record. 

But this there actually Euryodus dalyae from Richards Spur? One of the major differences that we noted between the holotype from South Grandfield and the purported specimen from Richards Spur was in the braincase. The specimens aren't too differently sized, but the holotype (LEFT above) has a bunch of braincase ossifications found in other recumbirostrans but not in the RS specimen (RIGHT above). The two to note are most visible in part A of each (the dorsal view); the holotype has a presphenoid (prs) and an ossification of the subiculum infundibulum (si; try saying that five times fast). There's a few other differences that could be suggested to be ontogenetically influenced, but we just don't have enough information to say at present, and because the specimens are pretty similar in size, some of these transformations would seem to be very abrupt. Based on this, we elected to just refer the Richards Spur material (which includes a less complete skull that lives at the Field Museum) to Euryodus sp. Like the other Richards Spur 'microsaurs,' we don't get very many that fell into the fissures

Recumbirostran phylogeny

With additional CT data, the 'microsaur' tree continues to be flushed out, and they're probably the best-sampled Paleozoic clade with respect to CT analyses (there might be some therapsid out there that has them beat). The whole goal of zapping all these little burrowing bastards was to improve what we knew about their braincases with an eye towards phylogenetics. Add Euryodus dalyae to a long laundry list of zapped taxa that already includes the brachystelechids Carrolla and Quasicaecilia, the lysorophian Brachydectes, the whole lot of rhynchonkids, Huskerpeton, and Llistrofus. Not too many big surprises when we added in our new gymnarthrid data (+ some non-CT codings from the literature), although Llistrofus bizarrely ends up next to the ostodolepids. That taxon's been hopping around in every subsequent study that incorporates it, so clearly there's a lot to do with respect to where hapsidopareiids go. The Richards Spur Euryodus is closely related to E. dalyae​, but it's not possible to distinguish them as closely related congenerics vs. conspecifics at this point. 

Majority-rule consensus tree (% nodal occurrence above line, bootstrap below line) from this analysis in the matrix of Pardo et al. (2017).

Mandible of the captorhinid Captorhinikos valensis (figure from Modesto et al., 2014).

Multiple tooth rows and the captorhinid controversy

Most animals only have one row of marginal teeth that line the mouth; you probably cannot think of any that have more than that. The same is true of most extinct tetrapods too. One notable Paleozoic exceptions are many members of Captorhinidae, a group of early diverging eureptiles, which will go on to become all modern reptiles. The photographs to the right are of Captorhinikos valensis​, and as you can see, it has several discrete tooth rows on the lower jaw. The formation of a simple dental battery accompanied the acquisition of more omnivorous habits in captorhinids, who lived amongst largely carnivorous tetrapods, and probably accounts for their taxonomic longevity as some of the first taxa to start nomming on plants. 

Lower jaws of the Richards Spur Euryodus.

'Microsaurs' have also been suggested to be early reptiles, an idea most recently revived by my friend Jason Pardo and colleagues (Pardo et al., 2017) who recovered recumbirostran 'microsaurs' as the sister group to captorhinids. This is based on a growing body of work identifying increased similarities between these clades, but the idea of 'microsaur'-captorhinid closeness is not new and has been debated for decades. I am a particular fan of Peter Vaughn's 1962 paper, cheekily titled "The Paleozoic microsaurs as close relatives of reptiles, again." There is of course, the alternative and similarly longstanding hypothesis that 'microsaurs' are actually closely related to modern amphibians, a stark contrast to their possible reptile affinities. One can identify homologous features (or analogous depending on your take) across the skeleton of 'microsaurs' and captorhinids, but one area that hadn't turned up anything yet was tooth rows...until now! As you can see below (parts E and F), this 'microsaur' had a partial second tooth row on the main element of the mandible, the dentary ('d'). One could argue that the teeth situated more internal on the coronoids ('c1,' 'c2,' and 'c3') add yet more mores to form a continuous toothy surface. We'd known about the extensive palatal dentition of some 'microsaurs,' but nobody's ever identified a second marginal tooth row until now. This row is extremely hard to ID when the jaws are articulated with the skull, and we could only clearly parse it out in the digital data. In captorhinids, multiple tooth rows aren't the product of absurd tooth growth, but the retention of several generations of teeth due to disproportionate jaw remodeling. 

Lower jaws of the holotype of Euryodus dalyae.

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Refs

• Anderson J, Reisz R. 2011. Growth series of the recumbirostran (Lepospondyli; Gymnarthridae) Cardiocephalus peabodyi from Richards Spur, Oklahoma; new anatomical information and implication for the evolution of 'microsaurs.' Journal of Vertebrate Paleontology 31: 62.
  
• ​Gee BM, Bevitt JJ, Garbe U, Reisz RR. 2019. New material of the ‘microsaur’ Llistrofus from the cave deposits of Richards Spur, Oklahoma and the paleoecology of the Hapsidopareiidae. PeerJ 7: 6327. doi: 10.7717/peerj.6327
  
• Huttenlocker AK, Pardo JD, Small BJ, Anderson JS. 2013. Cranial morphology of recumbirostrans (Lepospondyli) from the Permian of Kansas and Nebraska, and early morphological evolution inferred by micro-computed tomography. Journal of Vertebrate Paleontology, 33(3): 540-552. doi: 10.1080/02724634.2013.728998
• MacDougall MJ, Tabor NJ, Woodhead J, Daoust AR, Reisz RR. 2017. The unique preservational environment of the Early Permian (Cisuralian) fossiliferous cave deposits of the Richards Spur locality, Oklahoma. Palaeogeography, Palaeoclimatology, Palaeoecology, 475: 1-11. 10.1016/j.palaeo.2017.02.019
  
• Maddin HC, Olori JC, Anderson JS. 2011. A redescription of Carrolla craddocki (Lepospondyli: Brachystelechidae) based on high‐resolution CT, and the impacts of miniaturization and fossoriality on morphology. Journal of Morphology, 272(6): 722-743. doi: 10.1002/jmor.10946
  
• Modesto SP, Lamb AJ, Reisz RR. 2014. The captorhinid reptile Captorhinikos valensis from the lower Permian Vale Formation of Texas, and the evolution of herbivory in eureptiles. Journal of Vertebrate Paleontology, 34(2): 291-302. doi: 10.1080/02724634.2013.809358
• Pardo JD, Anderson JS. 2016. Cranial morphology of the Carboniferous-Permian tetrapod Brachydectes newberryi (Lepospondyli, Lysorophia): new data from µCT. PloS one, 11(8): e0161823. doi: 10.1371/journal.pone.0161823
  
• Pardo JD, Szostakiwskyj M, Anderson JS. 2015. Cranial morphology of the brachystelechid ‘microsaur’ Quasicaecilia texana Carroll provides new insights into the diversity and evolution of braincase morphology in recumbirostran ‘microsaurs’. PloS one, 10(6): e0130359. doi: 10.1371/journal.pone.0130359
• Pardo JD, Szostakiwskyj M, Ahlberg PE, Anderson JS. 2017. Hidden morphological diversity among early tetrapods. Nature, 546(7660): 642-645. doi: 10.1038/nature22966
  
• Reisz RR, LeBlanc AR, Sidor CA, Scott D, May W. 2015. A new captorhinid reptile from the Lower Permian of Oklahoma showing remarkable dental and mandibular convergence with microsaurian tetrapods. The Science of Nature, 102(9-10): 50. doi: 10.1007/s00114-015-1299-y
  
• Szostakiwskyj M, Pardo JD, Anderson JS. 2015. Micro-CT study of Rhynchonkos stovalli (Lepospondyli, Recumbirostra), with description of two new genera. PLoS One, 10(6): e0127307. doi: 10.1371/journal.pone.0127307