Abstract
Amphisbaenia is a speciose clade of fossorial lizards characterized by a snake-like body and a strongly reinforced skull adapted for head-first burrowing1,2. The evolutionary origins of amphisbaenians are controversial, with molecular data uniting them with lacertids3,4, a clade of Old World terrestrial lizards, whereas morphology supports a grouping with snakes and other limbless squamates5,6,7,8,9. Reports of fossil stem amphisbaenians10 have been falsified11, and no fossils have previously tested these competing phylogenetic hypotheses or shed light on ancestral amphisbaenian ecology. Here we report the discovery of a new lacertid-like lizard from the Eocene Messel locality of Germany that provides the first morphological evidence for lacertidâamphisbaenian monophyly on the basis of a reinforced, akinetic skull roof and braincase, supporting the view that body elongation and limblessness in amphisbaenians and snakes evolved independently. Morphometric analysis of body shape and ecology in squamates indicates that the postcranial anatomy of the new taxon is most consistent with opportunistically burrowing habits, which in combination with cranial reinforcement indicates that head-first burrowing evolved before body elongation and may have been a crucial first step in the evolution of amphisbaenian fossoriality.
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References
Kearney, M. Systematics of the Amphisbaenia (Lepidosauria: Squamata) based on morphological evidence from recent and fossil forms. Herpet . Monog 17, 1â74 (2003)
Gans, C. & Montero, R. in Biology of the Reptilia, Vol. 21 (eds Gans, C., Gaunt, A. S. & Adler, K. ) 621â738 (Society for the Study of Amphibians and Reptiles, 2008)
Townsend, T. M., Larson, A., Louis, E. & Macey, J. R. Molecular phylogenetics of Squamata: the position of snakes, amphisbaenians, and dibamids, and the root of the squamate tree. Syst. Biol. 53, 735â757 (2004)
Vidal, N. & Hedges, S. B. The phylogeny of squamate reptiles (lizards, and amphisbaenians) inferred from nine protein-coding genes. C. R. Biol. 328, 1000â1008 (2005)
Estes, R., de Queiroz, K. & Gauthier, J. A. in Phylogenetic Relationships of the Lizard Families (eds Estes, R. & Pregill, G. K. ) 119â281 (Stanford Univ. Press, 1988)
Rieppel, O. A review of the origin of snakes. Evol. Biol. 22, 37â130 (1988)
Hallerman, J. Thee ethmoidal regionof Dibamus taylori (Squamata: Dibamidae), with a phylogenetic hypothesis on dibamid relationships within Squamata. Zool. J. Linn. Soc. 122, 385â426 (1998)
Evans, S. & Barbadillo, L. J. An unusual lizard from the Early Cretaceous of Las Hoyas, Spain. Zool. J. Linn. Soc. 124, 235â265 (1998)
Conrad, J. L. Phylogeny and systematics of Squamata (Reptilia) based on morphology. Bull. Am. Mus. Nat. Hist. 310, 1â182 (2008)
Wu, X.-C. et al. Oldest known amphisbaenian from the Upper Cretaceous of Chinese Inner Mongolia. Nature 366, 57â59 (1993)
Kearney, M. The phylogenetic position of Sineoamphisbaena hexatabularis reexamined. J. Vertebr. Paleontol. 23, 394â403 (2003)
Franzen, J. L., Weber, J. & Wuttke, M. Senckenberg-Grabungen in der Grube Messel bei Darmstadt. 3. Ergebnisse 1979â1981. Cour. Forsch.-Inst. Senckenberg 54, 12â15 (1982)
Berman, D. S. Spathorhynchus fossorium, a middle Eocene amphisbaenian (Reptilia) from Wyoming. Copeia 1973, 704â721 (1973)
Berman, D. S. Spathorhynchus natronicus, a new species of rhineurid amphisbaenian (Reptilia) from the Early Oligocene of Wyoming. J. Paleontol. 51, 986â991 (1977)
Kearney, M., Maisano, J. A. & Rowe, T. Cranial anatomy of the extinct amphisbaenian Rhineura hatcherii (Squamata, Amphisbaenia) based on high-resolution X-ray computed tomography. J. Morphol. 264, 1â33 (2005)
Lee, M. S. Y. Hidden support from unpromising data sets strongly unites snakes with anguimorph âlizardsâ. J. Evol. Biol. 22, 1308â1316 (2009)
Wiens, J. J. et al. Combining phylogenomics and fossils in higher level squamate reptile phylogeny: molecular data change the placement of fossil taxa. Syst. Biol. 59, 675â688 (2010)
Lee, M. S. Y. Convergent evolution and character correlation in burrowing reptiles: towards a resolution of squamate relationships. Biol. J. Linn. Soc. 65, 369â453 (1998)
Wiens, J. J., Brandley, M. C. & Reeder, T. W. Why does a trait evolve multiple times within a clade? Repeated evolution of snakelike body form in squamate reptiles. Evolution 60, 123â141 (2006)
Brandley, M. C., Huelsenbeck, J. P. & Wiens, J. J. Rates and patterns in the evolution of snake-like body form in squamate reptiles: evidence for repeated re-evolution of lost digits and long-term persistence of intermediate body forms. Evolution 62, 2042â2064 (2008)
Gans, C. Tetrapod limblessness: evolution and functional corrollaries. Am. Zool. 15, 455â467 (1975)
Greer, A. E. Limb reduction in squamates: identification of the lineages and discussion of the trends. J. Herpetol. 25, 166â173 (1991)
Wiens, J. J. & Slingluff, J. L. How lizards turn into snakes: a phylogenetic analysis of body-form evolution in anguid lizards. Evolution 55, 2303â2318 (2001)
Hipsley, C. A., Himmelmann, L., Metzler, D. & Müller, J. Integration of Bayesian molecular clock methods and fossil-based soft bounds reveals early Cenozoic colonization of African lacertid lizards. BMC Evol. Biol. 9, 151 (2009)
Estes, R. Handbuch der Paläoherpetologie Pt 10 (Gustav Fischer, 1983)
Müller, J. Osteology and relationships of Eolacerta robusta, a lizard from the middle Eocene of Germany (Reptilia, Squamata). J. Vertebr. Paleontol. 21, 261â278 (2001)
Rieppel, O., Conrad, J. L. & Maisano, J. A. New morphological data for Eosaniwa koehni Haubold 1977, and a revised phylogenetic analysis. J. Paleontol. 81, 760â769 (2007)
Weber, S. Ornatocephalus metzleri gen. et spec. nov. (Lacertilia, Scincoida) â taxonomy and paleobiology of a basal scincoid lizard from the Messel formation (middle Eocene: basal Lutetian, Geiseltalium), Germany. Abh. Senckenb. Naturf. Gesellsch. 561, 1â159 (2004)
Popov, S. V. et al. Lithological-Paleogeographic maps of the Paretethys. 10 maps Late Eocene to Pliocene. Cour. Forsch.-Inst. Senckenberg 250, 1â46 (2004)
The Deep Scaly Project. Rhineura floridana, Florida worm lizard. ãhttp://digimorph.org/specimens/Rhineura_floridana/ã (Digimorph, 2008)
Acknowledgements
We thank S. Schaal for making the specimen available for study, J. J. Wiens for providing his morphometric data set of extant squamates, J. L. Conrad for providing his morphological data set of fossil and extant squamates, I. Manke for technical and administrative support, H. Mewis, H. Stöhr and A. Paulke for technical support, C. Bell and D. Evans for discussion, and P. Holroyd, M. Kroniger, M. Cunningham, M.-O. Rödel, K. Seymour, H.-D. Sues and F. Tillack for access to specimens. J.J.H. was funded by Natural Sciences and Engineering Research Council of Canada Discovery and Research Tools and Instruments grants, R.R.R. was funded by a Natural Sciences and Engineering Research Council of Canada Discovery grant and the Alexander von Humboldt-Stiftung.
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J.M., C.A.H., J.J.H. and R.R.R. contributed to project planning and anatomical analysis. J.M., C.A.H., N.K. and A.H. contributed to micro-CT scanning. J.M. contributed to phylogenetic analysis. J.J.H. contributed to ecomorphological analysis. M.W. contributed to project initiation. All authors contributed to manuscript and figure preparation.
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Müller, J., Hipsley, C., Head, J. et al. Eocene lizard from Germany reveals amphisbaenian origins. Nature 473, 364â367 (2011). https://doi.org/10.1038/nature09919
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DOI: https://doi.org/10.1038/nature09919
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