Aquatic adaptations in the four limbs of the snake-like reptile Tetrapodophis from the Lower Cretaceous of Brazil

doi:10.1016/j.cretres.2016.06.004

Cretaceous Research

Volume 66, November 2016, Pages 194-199

https://doi.org/10.1016/j.cretres.2016.06.004 Get rights and content

Abstract

The exquisite transitional fossil Tetrapodophis – described as a stem-snake with four small legs from the Lower Cretaceous of Brazil – has been widely considered a burrowing animal, consistent with recent studies arguing that snakes had fossorial ancestors. We reevaluate the ecomorphology of this important taxon using a multivariate morphometric analysis and a reexamination of the limb anatomy. Our analysis shows that the body proportions are unusual and similar to both burrowing and surface-active squamates. We also show that it exhibits striking and compelling features of limb anatomy, including enlarged first metapodials and reduced tarsal/carpal ossification – that conversely are highly suggestive of aquatic habits, and are found in marine squamates. The morphology and inferred ecology of Tetrapodophis therefore does not clearly favour fossorial over aquatic origins of snakes.

Section snippets

Materials and methods

We expanded a multivariate morphometric analysis of lepidosaurs (lizards, snakes, tuataras) of known ecology (Wiens et al., 2006, Müller et al., 2011) by adding Tetrapodophis and fossil marine squamates (pleurosaurs, dolichosaurs, mosasauroids). The original habitat divisions were reduced by combining three overlapping categories (cryptic, saxicolous, terrestrial) into one category (terrestrial); a new category (fully aquatic) was added to accommodate the additional taxa included, leading to 5

Results and discussion

The PCA analysis (data scaled to SEL; Fig. 1, File 1) revealed that most (82%) of the variance was captured by the first 2 principal components, with loadings suggesting that PC1 represents shape change associated with body elongation, and PC2 relative tail length. The bivariate plot of the first 2 PCs confirms that Tetrapodophis falls near fossorial forms, close to long-bodied but tetrapodal skinks that burrow through loose sediments and leaf litter, such as Sepsina angolensis and Chalcides (

Conclusions

The results of our multivariate morphometric analyses (PCA, LDA) intriguingly suggest that Tetrapodophis has a body shape similar to that of modern burrowers as well as surface-active but cryptozoic lizards (e.g. the diploglossid Celestus). The burrowers most similar to Tetrapodophis are relatively generalised forms that move through loose soil or leaf litter, so if Tetrapodophis is accepted as a stem snake, it would suggest that snake ancestors were not heavily specialised fossors. An

Acknowledgements

MC and RR thank Martin Röper (Museum Solnhofen) for access to Tetrapodophis during late 2015. MJ thanks Oliver Rauhut (LMU Munich) for access to specimens of Pleurosaurus. AP and MC thank Giorgio Teruzzi and Cristiano dal Sasso (Museo Civico di Storia Naturale di Milano) for access to a specimen of Pontosaurus. AP thanks Alan Resetar and Kathleen Kelly (Field Museum of Natural History) for access to specimens of Chalcides. We thank Johannes Müller, Christy Hipsley, for discussion, and Michel

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Tetrapodophis amplus exhibits features of fossorial snakes and lizards such as a short rostrum and elongation of the postorbital skull, a long trunk and short tail, short neural spines, and considerably reduced limbs (Martill et al., 2015). These morphological characteristics indicated that the first snake had a burrowing habit (Martill et al., 2015); however, a redescription of Tetrapodophis suggested an anguilliform locomotion habit in water or land (Lee et al., 2016). Araripemys arturi and A. barretoi are the only known turtle species of the CKL, including juvenile specimens (Fielding et al., 2005; Naish, 2007; Oliveira and Kellner, 2017).
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The regression of these traits can also contribute to a vigorous debate concerning the origins of snakes (Bellairs and Underwood, 1951). The ecological context for serpent origins has been attributed to early marine (Cope, 1869; Nopcsa, 1923; Caldwell and Lee, 1997; Lee et al., 1999; Caprette et al., 2004; Lee, 2005; Lee et al., 2016), fossorial (Mahendra, 1938; Walls, 1942; Bellairs and Underwood, 1951; Apesteguía and Zaher, 2006; Longrich et al., 2012; Yi and Norell, 2015; Martill et al., 2015), and/or nocturnal adaptations (Underwood, 1967, 1977; Hsiang et al., 2015). These models are variably consistent with the loss of limbs, taste buds, and photopic photoreception, and the timing and distribution of gene loss may have some bearing on these hypotheses.
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Short communicationAquatic adaptations in the four limbs of the snake-like reptile Tetrapodophis from the Lower Cretaceous of Brazil

Abstract

Section snippets

Materials and methods

Results and discussion

Conclusions

Acknowledgements

Marine Mammals: Evolutionary Biology

From fins to limbs to fins: limb evolution in fossil marine reptiles

American Journal of Medical Genetics

A snake with legs from the marine Cretaceous of the Middle East

Nature

A new species of marine ophidiomorph lizard, Adriosaurus skrbinensis, from the Upper Cretaceous of Slovenia

Journal of Vertebrate Paleontology

Marine members of Sphenodontia

Les rhynchocephales et les sauriens de calcaires lithographiques (Jurassique supérieur) d'Europe occidentale

Nouvelles Archives du Muséum d'Histoire Naturelle de Lyon

Aphanizocnemus libanensis n. gen. n. sp., a new dolichosaur (Reptilia, Varanoidea) from the Upper Cretaceous of Lebanon

Paleontologia Lombarda

The R commander: a basic statistics graphical user interface to R

Journal of Statistical Software

Assembling the squamate tree of life: Perspectives from the phenotype and the fossil record

Bulletin of the Peabody Museum of Natural History

Factors affecting habitat selection in a specialist fossorial skink

Biological Journal of the Linnean Society

PAST: Paleontological statistics software package for education and data analysis

Palaeontologia Electronica

The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record

BMC Evolutionary Biology

Molecular evidence and marine snake origins

Biology Letters

Hidden support from unpromising data sets strongly unites snakes with anguimorph ‘lizards’

Journal of Evolutionary Biology

The relationship between limb reduction, body elongation and geographical range in lizards (Lerista, Scincidae)

Journal of Biogeography

A transitional snake from the Late Cretaceous period of North America

Nature

Short communication
Aquatic adaptations in the four limbs of the snake-like reptile Tetrapodophis from the Lower Cretaceous of Brazil