The morphology of the inner ear of squamate reptiles and its bearing on the origin of snakes

The inner ear morphology of 80 snake and lizard species, representative of a range of ecologies, is here analysed and compared to that of the fossil stem snake Dinilysia patagonica, using three-dimensional geometric morphometrics. Inner ear morphology is linked to phylogeny (we find here a strong phylogenetic signal in the data that can complicate ecological correlations), but also correlated with ecology, with Dinilysia resembling certain semi-fossorial forms (Xenopeltis and Cylindrophis), consistent with previous reports. We here also find striking resemblances between Dinilysia and some semi-aquatic snakes, such as Myron (Caenophidia, Homalopsidae). Therefore, the inner ear morphology of Dinilysia is consistent with semi-aquatic as well as semi-fossorial habits: the most similar forms are either semi-fossorial burrowers with a strong affinity to water (Xenopeltis and Cylindrophis) or amphibious, intertidal forms which shelter in burrows (Myron). Notably, Dinilysia does not cluster as closely with snakes with exclusively terrestrial or obligate burrowing habits (e.g. scolecophidians and uropeltids). Moreover, despite the above similarities, Dinilysia also occupies a totally unique morphospace, raising issues with linking it with any particular ecological category.Alessandro Palci, Mark N. Hutchinson, Michael W. Caldwell and Michael S.Y. Le

Shape and size variation in elapid snake fangs, and the effects of phylogeny and diet

Published online: 9 October 2023Recent studies have found correlations between the shape of snake teeth/fangs and diet. These studies were done at a very broad phylogenetic scale, making it desirable to test if correlations are still detectable at a narrower evolutionary scale, specifically within the family Elapidae. To this end, we studied fang shape in a dense selection of elapids representing most genera worldwide (74%). We used three-dimensional geometric morphometrics to analyse fang diversity and evaluate possible correlations between fang shape, fang size, and diet. We detected only weak phylogenetic signal in our dataset for both shape and size, and no significant evolutionary allometry when correcting for phylogeny. Overall, the distribution of elapid fangs in morphospace was found to be surprisingly conservative, with only a few outliers. The only two dietary categories that were found to have a significant effect on fang shape are fish and snakes, while mammals have a significant effect on absolute but not relative fang size. Our results show that there are disparate patterns in fang-diet relationships at different evolutionary scales. Across all venomous snakes, previous work found that fangs are strongly influenced by diet, but within elapids our study shows these same associations are weaker and often non-significant. This could result from limitations in these types of studies, or could reflect the fact that elapids are a relatively young clade, where recent extensive divergences in diet have yet to be mirrored in fang shape, suggesting a lag between changes in ecology and dental morphology.Alessandro Palci, Michael S. Y. Lee, Jenna M. Crowe, Riddell, Emma Sherrat

Palaeoecological inferences for the fossil Australian snakes yurlunggur and wonambi (Serpentes, madtsoiidae)

Madtsoiids are among the most basal snakes, with a fossil record dating back to the Upper Cretaceous (Cenomanian). Most representatives went extinct by the end of the Eocene, but some survived in Australia until the Late Cenozoic. Yurlunggur and Wonambi are two of these late forms, and also the best-known madtsoiids to date. A better understanding of the anatomy and palaeoecology of these taxa may shed light on the evolution and extinction of this poorly known group of snakes and on early snake evolution in general. A digital endocast of the inner ear of Yurlunggur was compared to those of 81 species of snakes and lizards with known ecological preferences using three-dimensional geometric morphometrics. The inner ear of Yurlunggur most closely resembles both that of certain semiaquatic snakes and that of some semifossorial snakes. Other cranial and postcranial features of this snake support the semifossorial interpretation. While the digital endocast of the inner ear of Wonambi is too incomplete to be included in a geometric morphometrics study, its preserved morphology is very different from that of Yurlunggur and suggests a more generalist ecology. Osteology, palaeoclimatic data and the palaeobiogeographic distribution of these two snakes are all consistent with these inferred ecological differences.Alessandro Palci, Mark N. Hutchinson, Michael W. Caldwell, John D. Scanlon, Michael S. Y. Le

Novel vascular plexus in the head of a sea snake (Elapidae, Hydrophiinae) revealed by high-resolution computed tomography and histology

Novel phenotypes are often linked to major ecological transitions during evolution. Here, we describe for the first time an unusual network of large blood vessels in the head of the sea snake Hydrophis cyanocinctus. MicroCT imaging and histology reveal an intricate modified cephalic vascular network (MCVN) that underlies a broad area of skin between the snout and the roof of the head. It is mostly composed of large veins and sinuses and converges posterodorsally into a large vein (sometimes paired) that penetrates the skull through the parietal bone. Endocranially, this blood vessel leads into the dorsal cerebral sinus, and from there, a pair of large veins depart ventrally to enter the brain. We compare the condition observed in H. cyanocinctus with that of other elapids and discuss the possible functions of this unusual vascular network. Sea snakes have low oxygen partial pressure in their arterial blood that facilitates cutaneous respiration, potentially limiting the availability of oxygen to the brain. We conclude that this novel vascular structure draining directly to the brain is a further elaboration of the sea snakes' cutaneous respiratory anatomy, the most likely function of which is to provide the brain with an additional supply of oxygen.Alessandro Palci, Roger S. Seymour, Cao Van Nguyen, Mark N. Hutchinson, Michael S. Y. Lee and Kate L. Sander

Cretaceous Blind Snake from Brazil Fills Major Gap in Snake Evolution

Blind snakes (Scolecophidia) are minute cryptic snakes that diverged at the base of the evolutionary radiation of modern snakes. They have a scant fossil record, which dates back to the Upper Paleocene-Lower Eocene ( 56 Ma); this late appearance conflicts with molecular evidence, which suggests a much older origin for the group (during the Mesozoic: 160–125 Ma). Here we report a typhlopoid blind snake from the Late Cretaceous of Brazil, Boipeba tayasuensis gen. et sp. nov, which extends the scolecophidian fossil record into the Mesozoic and reduces the fossil gap predicted by molecular data. The new species is estimated to have been over 1 m long, much larger than typical modern scolecophidians (<30 cm). This finding sheds light on the early evolution of blind snakes, supports the hypothesis of a Gondwanan origin for the Typhlopoidea, and indicates that early scolecophidians had large body size, and only later underwent miniaturization.Thiago Schineider Fachini, Silvio Onary, Alessandro Palci, Michael S.Y. Lee, Mario Bronzati, and Annie Schmaltz Hsio

Reacquisition of the lower temporal bar in sexually dimorphic fossil lizards provides a rare case of convergent evolution

Temporal fenestration has long been considered a key character to understand relationships amongst reptiles. In particular, the absence of the lower temporal bar (LTB) is considered one of the defining features of squamates (lizards and snakes). In a re-assessment of the borioteiioid lizard Polyglyphanodon sternbergi (Cretaceous, North America), we detected a heretofore unrecognized ontogenetic series, sexual dimorphism (a rare instance for Mesozoic reptiles), and a complete LTB, a feature only recently recognized for another borioteiioid, Tianyusaurus zhengi (Cretaceous, China). A new phylogenetic analysis (with updates on a quarter of the scorings for P. sternbergi) indicates not only that the LTB was reacquired in squamates, but it happened independently at least twice. An analysis of the functional significance of the LTB using proxies indicates that, unlike for T. zhengi, this structure had no apparent functional advantage in P. sternbergi, and it is better explained as the result of structural constraint release. The observed canalization against a LTB in squamates was broken at some point in the evolution of borioteiioids, whereas never re-occuring in other squamate lineages. This case of convergent evolution involves a mix of both adaptationist and structuralist causes, which is unusual for both living and extinct vertebrates

Geometric morphometrics, homology and cladistics: review and recommendations

Geometric morphometric (GM) data has a long and contentious history in phylogenetic analyses. Often associated with phenetics, GM has been considered by many to be unable to provide meaningful information on phylogenetic relationships. However, the concepts of primary and secondary homology as developed for discrete characters can be readily extended to GM data: raw similarity in aligned landmark positions represents primary homology, and similarity ascribable to common ancestry represents secondary homology. We review fundamental concepts from the literature and provide a series of practical guidelines for the use of GM data in phylogenetics: (i) alignments that minimize linear distances between landmarks (or their approximation) perform better in highlighting apomorphic traits; (ii) Type I, Type II and linear semi-landmarks are preferable to Type III and surface semi-landmarks; (iii) excluding bilateral landmarks after, rather than before, alignment will prevent artefactual mediolateral displacement of midsagittal landmarks; (iv) phylogenetic analyses should employ linear rather than squared-change parsimony analysis of landmark displacements; (v) optimization of shape changes across a tree can be improved with methods that re-align the landmark configurations based on the results of the phylogenetic analysis; and (vi) GM data are no substitute for traditional morphological characters, but rather a complementary descriptor of shape diversity.Alessandro Palcia, b, and Michael S. Y. Le

Morphological phylogenetics in the genomic age

ReviewEvolutionary trees underpin virtually all of biology, and the wealth of new genomic data has enabled us to reconstruct them with increasing detail and confidence. While phenotypic (typically morphological) traits are becoming less important in reconstructing evolutionary trees, they still serve vital and unique roles in phylogenetics, even for living taxa for which vast amounts of genetic information are available. Morphology remains a powerful independent source of evidence for testing molecular clades, and - through fossil phenotypes - the primary means for time-scaling phylogenies. Morphological phylogenetics is therefore vital for transforming undated molecular topologies into dated evolutionary trees. However, if morphology is to be employed to its full potential, biologists need to start scrutinising phenotypes in a more objective fashion, models of phenotypic evolution need to be improved, and approaches for analysing phenotypic traits and fossils together with genomic data need to be refined.Michael S.Y. Lee, Alessandro Palc

Patterns of postnatal ontogeny of the skull and lower jaw of snakes as revealed by micro-CT scan data and three-dimensional geometric morphometrics

We compared the head skeleton (skull and lower jaw) of juvenile and adult specimens of five snake species [Anilios (=Ramphotyphlops) bicolor, Cylindrophis ruffus, Aspidites melanocephalus, Acrochordus arafurae, and Notechis scutatus] and two lizard outgroups (Ctenophorus decresii, Varanus gilleni). All major ontogenetic changes observed were documented both qualitatively and quantitatively. Qualitative comparisons were based on high-resolution micro-CT scanning of the specimens, and detailed quantitative analyses were performed using three-dimensional geometric morphometrics. Two sets of landmarks were used, one for accurate representation of the intraspecific transformations of each skull and jaw configuration, and the other for comparison between taxa. Our results document the ontogenetic elaboration of crests and processes for muscle attachment (especially for cervical and adductor muscles); negative allometry in the braincase of all taxa; approximately isometric growth of the snout of all taxa except Varanus and Anilios (positively allometric); and positive allometry in the quadrates of the macrostomatan snakes Aspidites, Acrochordus and Notechis, but also, surprisingly, in the iguanian lizard Ctenophorus. Ontogenetic trajectories from principal component analysis provide evidence for paedomorphosis in Anilios and peramorphosis in Acrochordus. Some primitive (lizard-like) features are described for the first time in the juvenile Cylindrophis. Two distinct developmental trajectories for the achievement of the macrostomatan (large-gaped) condition in adult snakes are documented, driven either by positive allometry of supratemporal and quadrate (in pythons), or of quadrate alone (in sampled caenophidians); this is consistent with hypothesised homoplasy in this adaptive complex. Certain traits (e.g. shape of coronoid process, marginal tooth counts) are more stable throughout postnatal ontogeny than others (e.g. basisphenoid keel), with implications for their reliability as phylogenetic characters.Alessandro Palci, Michael S. Y. Lee and Mark N. Hutchinso

Emended diagnosis and phylogenetic relationships of the Upper Cretaceous fossil snake Najash rionegrina Apesteguia and Zaher, 2006

The fossil snake Najash rionegrina, from the Cenomanian–Turonian (Upper Cretaceous) of Argentina, is reinterpreted after examination of the type and referred material. The current diagnosis is emended in the light of important considerations that cast doubt on the attribution of type and referred specimens (a braincase, a quadrate, and two dentary/lower jaw fragments) used to systematize this taxon. Alternative interpretations of the anatomy of the sacrum and hind limbs are proposed. Following the reevaluation of the anatomy of the type specimen and the removal from this taxon of the above-mentioned referred material, the phylogenetic position of N. rionegrina was tested in a series of maximum parsimony analyses that included all groups of extant snakes, all best-known fossil snakes (i.e., Pachyrhachis, Haasiophis, Eupodophis, Madtsoiidae, and Dinilysia), and alternative outgroups. Regardless of the outgroup used to polarize the character-state transformations, our phylogenetic analyses found no support for the hypothesis that Najash rionegrina occupies a position as the most basal snake. Depending on the outgroup, Najash is placed (1) in a position basal to all living snakes, but more derived than other fossil forms (most notably Pachyrhachis, Eupodophis, and Haasiophis); or (2) as the most basal representative of a clade of fossil snakes that is the sister group of living snakes; or (3) as the most basal representative of a clade of fossil snakes that is located between the Scolecophidia and the Alethinophidia.Alessandro Palci, Michael W. Caldwell, and Adriana M. Albin