Belongs within: Unidentata.
Contains: Serpentes, Iguania, Anguiformes.
A toxic debate
Published 2 December 2024
There is no question that the advent of molecular phylogenetic analyses represented a major event in our understanding of evolutionary history. The early years of molecular analyses were a wild time, as the first tentative studies threw up a whole range of surprising results that seemed to fly in the face of morphological orthodoxy. As our understanding of evolutionary processes and analytical methods (both molecular and morphological) improved, these novel hypotheses were put to the test. In some cases, new morphological data were assembled that gave credence to the molecular results (yes, hippos really are the closest living relatives of whales). In other cases, unexpected molecular results proved to be the result of analytical errors (no, the marine worm-like animal Xenoturbella is not a shell-less bivalve). But there are some cases where the conflict seemingly remains unresolved, no matter how much new data is thrown against it. Consider the question of Toxicofera.
With over 10,000 known species, lizards (including snakes, which are really just fancy lizards) are one of the most significant radiations of terrestrial vertebrates in the modern fauna. There are nearly twice as many species of lizard as there are mammals, and about the same number of lizards as there are birds. Nevertheless, lizards do not receive anywhere near the amount of attention either mammals or birds do. This includes studies on their evolutionary relationships. Recent analyses, both molecular and morphological, have largely agreed on the division of lizards between seven major subgroups. For this post, I’ll refer to these as the Iguania (iguanas and dragons), Gekkota (geckoes), Scincoidea (skinks), Lacertoidea (wall lizards), Anguimorpha (monitors and glass lizards), Serpentes (snakes) and Dibamidae. The Dibamidae are a small family of legless lizards found mostly in south-east Asia; they’ll be largely ignored for the remainder of this post. The other lineages are all more diverse in both appearance and species number.
Since the late 1980s, most morphological studies of lizard phylogeny have agreed in placing the Iguania as the sister lineage to all other lizards (Koch & Gauthier 2018). Among the characters supporting this placement, particular attention has been paid to the structure of the tongue. Iguanians possess a fleshy, muscular tongue that is actively used in the capture and manipulation of food, similar to that of the closest living relative of lizards, the tuatara Sphenodon punctatus. In other lizards, the tongue is flattened and keratinised, functioning as a sensory organ (think the flicking tongue of a snake) while food is handled directly by the jaws only. The perceived significance of this change is such that the clade excluding iguanians was dubbed the Scleroglossa, ‘hard tongues’.
It therefore came as a surprise when molecular analyses, beginning in the late 1990s, proposed a different scenario (Burbrink et al. 2020). Iguanians were not placed as the outlier to all other lizards but instead formed a clade with the anguimorphs and snakes. This proposed clade was dubbed the Toxicofera, ‘venom bearers’. Both the snakes and anguimorphs had previously been known to include venomous species, and supposed toxin proteins were also identified in the oral tissues of iguanians and other species previously thought non-venomous. The suggestion was floated that, rather than evolving independently in multiple lineages, venom had evolved once at the base of the Toxicofera clade and its apparent absence in some species was the result of secondary losses.
Subsequent analyses only reinforced the divide with neither molecular nor morphological studies shifting their stance. If the Toxicofera hypothesis was correct, then a remarkable degree of convergence had occurred with either the scleroglossan tongue evolving on multiple occasions or the iguanians somehow reverting to a more primordial morphology. If the Scleroglossa hypothesis was correct, then it remained to be established how its opponent could be so consistently supported by multiple analysed genes. Though subsequent studies challenged the idea of a basal origin for venom within Toxicofera, indicating that the so-called ‘venom genes’ may have been misidentified (Hargreaves et al. 2014), the question of whether all toxicoferans were originally ‘venom bearers’ is a distinct question from whether the clade exists that happens to have been labelled ‘Toxicofera’.
What makes this particularly interesting is that the conflict is largely specific to Iguania. Koch & Gauthier (2018) compared the results of morphological and molecular analyses; other than Iguania, their trees from both sources are largely congruent in an arrangement of (Gekkota (Scincoidea, Lacertoidea (Anguimorpha + Serpentes))). Molecular and morphological analyses differed whether Lacertoidea was closer to Scincoidea or Anguimorpha + Serpentes but, as that boils down to different resolutions within a single trichotomy, it seems less fundamental a conflict than that affecting Iguania. Koch & Gauthier (2018) suggested that the ‘Toxicofera’ arrangement might be an artefact resulting from similar raised rates of evolution and bias towards A+T gene composition in Iguania and Serpentes. However, Simões & Pyron (2021) accused Koch & Gauthier’s argument of boiling down to, “If you discount the evidence supporting Toxicofera, the support for Toxicofera disappears”.
As yet, the conflict appears unresolved. Perhaps the majority of recent authors favour recognition of Toxicofera, but that may simply reflect a bias towards favouring molecular analyses. Simões et al. (2018) did find results consistent with Toxicofera in a morphology-only analysis (as presented in their supplementary data), but did not explicitly discuss what characters supported this result. We are still yet to confidently establish how the lizard got its tongue, or the viper its bite.
Systematics of Toxicofera
Toxicofera [Anguimorpha, Anguinomorpha, Anguoidea, Varanoidea]BG20
| i. s.: CarolinidaeB93
| |--Carusia intermedia (Borsuk-Bialynicka 1985)B93
| `--Shinisauroides latipalatum Borsuk-Bialynicka 1985B93
| Dorsetisaurus [Dorsetisauridae]B93
| |--D. hebetidens Hoffstetter 1967B93
| `--D. purbeckensis Hoffstetter 1967 [incl. Introrsisaurus pollicidens Seiffert 1973]B93
|--OphidiaLBG12b
| | i. s.: Rottophis atavus (von Meyer 1860)S05
| | CheilophisLBG12b
| | SanjuanophisLBG12b
| |--+--SerpentesBG20
| | `--Najash Apesteguía & Zaher 2006LBG12a, AZ06
| | `--*N. rionegrina Apesteguía & Zaher 2006AZ06
| `--Coniophis Marsh 1892 [Coniophidae]LBG12a
| |--C. carinatus McGrew et al. 1959LBG12a
| |--C. cosgriffi Armstrong-Ziegler 1978LBG12a
| |--C. dabiebus Rage & Werner 1999LBG12a
| |--C. platycarinatus McGrew et al. 1959LBG12a
| `--C. precedens Marsh 1892LBG12a
`--+--+--IguaniaBG20
| `--Lamiasaurus Longrich, Bhullar & Gauthier 2012LBG12b
| `--*L. ferox Longrich, Bhullar & Gauthier 2012LBG12b
`--AnguiformesBG20
*Type species of generic name indicated
References
[AZ06] Apesteguía, S. & H. Zaher. 2006. A Cretaceous terrestrial snake with robust hindlimbs and a sacrum. Nature 440: 1037–1040.
[B93] Benton, M. J. 1993. Reptilia. In: Benton, M. J. (ed.) The Fossil Record 2 pp. 681–715. Chapman & Hall: London.
[BG20] Burbrink, F. T., F. G. Grazziotin, R. A. Pyron, D. Cundall, S. Donnellan, F. Irish, J. S. Keogh, F. Kraus, R. W. Murphy, B. Noonan, C. J. Raxworthy, S. Ruane, A. R. Lemmon, E. M. Lemmon & H. Zaher. 2020. Interrogating genomic-scale data for Squamata (lizards, snakes, and amphisbaenians) shows no support for key traditional morphological relationships. Systematic Biology 69 (3): 502–520.
Koch, N. M., & J. A. Gauthier. 2018. Noise and biases in genomic data may underlie radically different hypotheses for the position of Iguania within Squamata. PLoS One 13 (8): e0202729.
[LBG12a] Longrich, N. R., B.-A. S. Bhullar & J. A. Gauthier. 2012a. A transitional snake from the Late Cretaceous period of North America. Nature 488: 205–208.
[LBG12b] Longrich, N. R., B.-A. S. Bhullar & J. A. Gauthier. 2012b. Mass extinction of lizards and snakes at the Cretaceous–Paleogene boundary. Proceedings of the National Academy of Sciences of the USA 109 (52): 21396–21401.
[S05] Scanlon, J. D. 2005. Cranial morphology of the Plio-Pleistocene giant madtsoiid snake Wonambi naracoortensis. Acta Palaeontologica Polonica 50: 139–180.
Simões, T. R., M. W. Caldwell, M. Talanda, M. Bernardi, A. Palci, O. Vernygora, F. Bernardini, L. Mancini & R. L. Nydam. 2018. The origin of squamates revealed by a Middle Triassic lizard from the Italian Alps. Nature 557: 706–709.
Simões, T. R., & R. A. Pyron. 2021. The squamate tree of life. Bulletin of the Museum of Comparative Zoology 163 (2): 47–95.