Cladistic ontogeny of Jiufotang tapejarids

As you probably already know, Sinopterus is a genus of tapejarid pterosaur from the Jiufotang Formation of China. The holotype of Sinopterus dongi was first named by Wang and Zhou (2003). Since then, a bunch of other species of tapejarid from the Jiufotang Formation have been named (incl. Li et al. 2003, Lü et al. 2016). Some of these (Lü and Yuan 2005, Lü et al. 2006a, 2007) have been referred to the genus Huaxiapterus, which was coined because the type species H. jii was larger than S. dongi, and appeared to show a transitional morphology between the cranial morphology of Sinopterus and that of later tapejarids such as Tapejara (i.e. intermediate crest size and rostral downturn). In total, the following species have been named: Sinopterus dongi, S. gui, S. lingyuanensis, Huaxiapterus jii, H. corollatus, H. benxiensis, H. atavismus, and Nemicolopterus crypticus, which was originally described as an aberrant pterodactyloid (Wang et al. 2008) but has been more recently recognized as a young tapejarid (e.g. Witton 2013, Andres et al. 2014).

The status of each of these species has been questioned, with a growing consensus that Jiufotang tapejarids are taxonomically oversplit (e.g. Witton 2013, Zhang et al. 2019, Naish et al. 2021). It’s been suggested, with decently high acceptance, that S. gui and H. jii are likely growth stages of S. dongi (e.g. Zhang et al. 2019) and that Nemicolopterus is likely a young flapling of one of the other tapejarids (Naish et al. 2021). Since H. jii is the type species of Huaxiapterus, this has led to benxiensis and corollatus being called “Huaxiapterus” (in quotes). Some researchers have supported combining all Jiufotang tapejarids into the genus Sinopterus, considering the differences between the two genera (i.e. crest shape/size and rostrum shape) too minor for genus-level separation (e.g. Zhang et al. 2019).

Some have taken this a step further, suggesting that most if not all Jiufotang tapejarids belong to one species, S. dongi., with the differences between species being attributable to ontogeny, sexual dimorphism, or individual variation (e.g. Witton 2013). Naish et al. (2021) concluded that Jiufotang tapejarids are by and large referable to S. dongi, with the potential exception of “Huaxiapterus” corollatus based on limb proportions. It has been pointed out that most Jiufotang tapejarid specimens are skeletally immature (Zhang et al. 2019), with only one (D2525; Lü et al. 2006b) showing the postcranial fusion in elements such as the dorsal vertebrae, carpals, and scapulocoracoid that indicate maturity in pterosaurs (e.g. Bennett 1993). Several characters used in species-level diagnoses of Jiufotang tapejarids, such as crest shape and limb bone ratios, have been shown to be variable with sex or age in other pterosaurs (e.g. Bennett 1993, Manzig et al. 2014, Wang et al. 2014), and thus may not be reliable for species-level diagnosis.

Regardless of the specifics of Jiufotang tapejarid alpha taxonomy, I was intrigued by how different specimens appear to represent different ontogenetic stages. Different specimens display different degrees of body size, crest size, rostral downturn, and postcranial bone fusion; these characters are thought to change with maturity in tapejarids and pterosaurs in general (Bennett 1993, Manzig et al. 2014). I decided to mess around with ontogenetic cladistics. Cladistic analysis of ontogeny can reconstruct growth sequences in a taxon, allowing the ability to track changes in morphological characters along a taxon’s growth series in a similar manner to how phylogenetic analyses do so for evolutionary relationships (Zietlow 2020). This has previously been applied to, among others, Centrosaurus apertus (Frederickson and Tumarin-Deratzian 2014), Tyrannosaurus rex (Carr 2020) and Tylosaurus spp.(Zietlow 2020).

I put together a dataset of all currently published Jiufotang tapejarid specimens, as well as two hypothetical OTUs. The holotypes of every tapejarid species mentioned above are included, as well as D2525 (referred to Sinopterus dongi; Lü et al. 2006b), IVPP V 23388 (referred to “Huaxiapterus” atavismus; Zhang et al. 2019), and PMOL-AP00030 (indeterminate tapejarid, but previously recovered close to “H.” benxiensis and “H.” corollatus; Liu et al. 2014). Following the methodology of Carr (2020) and Zietlow (2020), the outgroup taxon for analysis was a hypothetical embryo OTU coded to be the most immature in the dataset, and a hypothetical adult OTU was added to identify the most mature specimen (it should return as its sister taxon). The hypothetical embryo and hypothetical adult OTUs were coded under the assumption that postcranial bones are completely unfused at birth, and completely fused at skeletal maturity, as appears to be the case for pterosaurs. I also assumed that embryos were crestless (based on Nemicolopterus) and adults had large crests (based on the size of the crests in H. benxiensis). All other characters were coded unknown for the hypothetical OTUs. The entire sample of Jiufotang tapejarids is included even if they do not all represent the same species, because if they aren’t, they’re still probably very closely related (e.g. Longrich et al. 2018, Kellner et al. 2019, Thomas 2019) so ontogenetic trends are likely to be similar between species. Besides, ontogenetic cladistics can test for this; if a bifurcation appears among specimens, this may support the existence of two species in the sample (e.g. Zietlow 2020). The dataset contains 111 characters; 34 are discrete characters (not all of which are necessarily variable in the sample), and 77 are continuous (all but one are ratios between skeletal elements). All data was compiled from the literature; observing specimens firsthand isn’t an option thanks to the global pandemic.

The one MPT of the analysis. Skulls redrawn from Zhang et al. 2019 and Wang et al. 2008. Scale bar 50 mm.

The results pretty much line up with what had previously been published on Jiufotang tapejarid ontogeny (e.g. Witton 2013, Naish et al. 2021). By and large, the individuals show a linear progression from the youngest individual (IVPP V 14377, holotype of Nemicolopterus crypticus) to the oldest (D2525, referred to Sinopterus dongi). This lines up with body size and crest size pretty neatly. The trends in morphological change are similar to those present in the ontogeny of Caiuajara (Manzing et al. 2014), the only other tapejarid that preserves material from across the ontogenetic sequence. As Jiufotang tapejarids grew older, the degree of snout downturn becomes more prominent, the cranial crests become larger, the dorsal convexities of the mandible become more prominent and move anteriorly, and the postcrania fuses to a greater degree.

This analysis recovers no evidence for sexual dimorphism among Jiufotang tapejarids; if it did, we might expect the ontogram to bifurcate instead of showing a linear young-to-old gradient (Zietlow 2020). It does show a small bifurcation with the most mature individuals; however, the characters that cause this are all limb proportions, so I think it’s fair to say that this is unlikely to represent sexual dimorphism, at least in the way we would expect. Lack of sexual dimorphism would line up with Manzig et al.’s (2014) interpretation of the Caiuajara sample. This also means the analysis recovers no evidence for multiple species. Does this necessarily mean anything? I’d say no. The sample size is pretty small (if, say, H. corollatus was a separate species, maybe we just haven’t found other specimens of it), preservation quality isn’t always great, some specimens’ descriptions could be better, PMOL-AP00030 and D2525 lack skulls, and I wouldn’t read too much into species or sex differences from cladistics alone anyways. And I know there are multiple unpublished Jiufotang tapejarid specimens out there.

Gonna cap this off with the disclaimer that this is ultimately an exercise of my own curiosity. I haven’t observed any of the specimens in person, and so it wouldn’t be appropriate for me to take this any further. The dataset can be downloaded here in Nexus and TNT format, if you want.

References

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Bennett, S.C. (1993). “The Ontogeny of Pteranodon and Other Pterosaurs”. Paleobiology 19(1): 92-106.
Carr, T.D. (2020). “A high-resolution growth series of Tyrannosaurus rex obtained from multiple lines of evidence”. PeerJ 8: e9192.
Frederickson, J.A.; Tumarkin-Deratzian, A.R. (2014). “Craniofacial ontogeny in Centrosaurus apertus“. PeerJ 2: e252.
Kellner, A.W.A.; Weinschutz, L.C.; Holgado, B.; Bantim, R.A.M.; Sayao, J.M. (2019). “A new toothless pterosaur (Pterodactyloidea) from Southern Brazil with insights into the paleoecology of a Cretaceous desert”. Anais da Academia Brasileira de Ciencias 91 supl. 2.
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Naish, D.; Witton, M.P.; Martin-Silverstone, E. (2021). “Powered flight in hatchling pterosaurs: evidence from wing form and bone strength”. Scientific Reports 11: 13130.
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Wang, X.; Kellner, A.W.A.; Zhou, Z.; Campos, D. A. (2008). “Discovery of a rare arboreal forest-dwelling flying reptile (Pterosauria, Pterodactyloidea) from China”. Proceedings of the National Academy of Sciences 105(6): 1983-7.
Wang, X.; Zhou, Z. (2003). “A new pterosaur (Pterodactyloidea, Tapejaridae) from the Early Cretaceous Jiufotang Formation of western Liaoning, China and its implications for biostratigraphy”. Chinese Science Bulletin 48: 16-23.
Witton, M.P. (2013). Pterosaurs: Natural History, Evolution, Anatomy. Princeton University Press.
Zhang, X.; Jiang, S.; Cheng, X.; Wang, X. (2019). “New Material of Sinopterus (Pterosauria, Tapejaridae) from the Early Cretaceous Jehol Biota of China”. Anais da Academia Brasileira de Ciencias 91 supl.2.
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