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9 - A Review of the Skull Anatomy and Phylogenetic Affinities of Marine Pachyophiid Snakes

from Part II - Palaeontology and the Marine-Origin Hypothesis

Published online by Cambridge University Press:  30 July 2022

By
Hussam Zaher ,
Bruno G. Augusta ,
Rivka Rabinovich ,
Michael J. Polcyn  and
Paul Tafforeau
Edited by
David J. Gower  and
Hussam Zaher
David J. Gower
Affiliation:
Natural History Museum, London
Hussam Zaher
Affiliation:
Universidade de São Paulo
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Summary

Pachyophiidae fossils are among the most complete known for snakes, and include the earliest snakes with fully developed hindlimbs. Pachyophiids have been historically seen as suitable morphological intermediates between lizards and extant snakes, supporting the hypothesis that snakes originated in a marine setting from a macrophagous common ancestor with mosasaurian lizards. Pachyophiids have been subject to conflicting interpretations of their anatomy, fuelling renewed debate on snake origins and early diversification. We revisit pachyophiid cranial anatomy, providing additional evidence from new preparations, high resolution CT scans, and Synchrotron images. We address challenges posed by fossil (in)completeness to the study and interpretation of these specimens, and reassess phylogenetic affinities. We critically reassess morphological evidence supporting the Marine Hypothesis, concluding that (i) snakes are not especially closely related to mosasaurians, and (ii) pachyophiids are relatively deeply nested within the snake crown, so that they are of greater importance for understanding early crown-snake evolutionary history than they are for understanding snake origins.

Keywords

PachyophiidaefossilsmorphologysystematicsphylogenyevolutionmarineskullCretaceousAlethinophidia
Type
Chapter
Information
The Origin and Early Evolutionary History of Snakes , pp. 180 - 206
Publisher: Cambridge University Press
Print publication year: 2022

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References

Burbrink, F. T., Grazziotin, F. G., Pyron, R. A., et al., Interrogating genomic-scale data for Squamata (lizards, snakes, and amphisbaenians) shows no support for key traditional morphological relationships. Systematic Biology, 69 (2020), 502–520.Google Scholar
Dercourt, J., Zonenshain, L. P., Ricou, L.- E., et al., Geological evolution of the Tethys belt from the Atlantic to the Pamirs since the Lias. Tectonophys, 123 (1986), 241–315.CrossRefGoogle Scholar
Berra, F. and Angiolini, L., The evolution of the Tethys region throughout the Phanerozoic: A brief tectonic reconstruction. American Association of Petroleum Geologists, Memoirs, 106 (2014), 1–27.Google Scholar
Polcyn, M. J., Tchernov, E., and Jacobs, L. L., The Cretaceous biogeography of the eastern Mediterranean with a description of a new basal mosasauroid from ‘Ein Yabrud, Israel. In Tomida, Y., Rich, T. H., and Vickers-Rich, P., eds., Proceedings of the Second Gondwanan Dinosaur Symposium, National Science Museum Tokyo , Monographs (1999), pp. 259–290.Google Scholar
Caldwell, M. W. and Lee, M. S. Y., A snake with legs from the marine Cretaceous of the Middle East. Nature, 386 (1997), 705–709.Google Scholar
Rage, J.-C. and Escuillié, F., Un nouveau serpent bipède du Cénomanien (Crétacé). Implications phylétiques. Comptes Rendus de l’Academie des Sciences, Paris, Sciences de la Terre et des Planètes, 330 (2000), 513–520.Google Scholar
Tchernov, E., Rieppel, O., Zaher, H., Polcyn, M. J., and Jacobs, L. L., A fossil snake with limbs. Science, 287 (2000), 2010–2012.Google Scholar
Zaher, H., The phylogenetic position of Pachyrhachis within snakes (Squamata, Lepidosauria). Journal of Vertebrate Paleontology, 18 (1998), 1–3.CrossRefGoogle Scholar
Zaher, H. and Rieppel, O., Tooth implantation and replacement in squamates, with special reference to mosasaur lizards and snakes. American Museum Novitates, 3271 (1999), 1–19.Google Scholar
Rage, J.-C. and Escuillié, F., The Cenomanian: stage of hindlimbed snakes. Carnets de Geologie, 2003/01 (2003), 1–11.Google Scholar
Scanlon, J. D. and Lee, M. S. Y., The Pleistocene serpent Wonambi and the early evolution of snakes. Nature, 403 (2000), 416–420.Google Scholar
Scanlon, J. D., Skull of the large non-macrostomatan snake Yurlunggur from the Australian Oligo-Miocene. Nature, 439 (2006), 839–842.CrossRefGoogle ScholarPubMed
Vidal, N. and Hedges, S. B., Molecular evidence for a terrestrial origin of snakes. Proceedings of the Royal Society of London B, 271 (2004), S226–S229.CrossRefGoogle ScholarPubMed
Apesteguía, S. and Zaher, H., A Cretaceous terrestrial snake with robust hindlimbs and a sacrum. Nature, 440 (2006), 1037–1040.CrossRefGoogle ScholarPubMed
Bardet, N., Houssaye, A., Rage, J.-C., and Pereda Suberbiola, X., The Cenomanian-Turonian (late Cretaceous) radiation of marine squamates (Reptilia): the role of the Mediterranean Tethys. Bulletin de la Société Géologique de France, 179 (2008), 605–622.Google Scholar
Sauvage, H. E., Sur l’existence d’un reptile du type ophidien dans les couches à Ostrea columba des Charentes. Comptes Rendus de la Société de l’Academie des Sciences, Paris, 91 (1880), 671–672.Google Scholar
Nopcsa, F., Eidolosaurus und Pachyophis, zwei neue Neocom-Reptilien. Palaeontograpjica, 65 (1923), 99–154.Google Scholar
Nopcsa, F., Ergebnisse der Forschungsreisen Prof. E. Stromers in den Wüsten Ägyptens. II. Wirbeltier-Reste der Baharjie-Stufe (unterstes Cenoman). Abhandlungen der Bayerische Akademie der Wissenschaftern, Mathematische-naturwissenschaftliche Abteilung, 30 (1925), 5–27.Google Scholar
Bolkay, S. J., Mesophis nopcsai ngn sp. ein neues, schlangenähnliches reptil aus der unteren Kreide (Neocom) von Bilek-Selista (Ost-Hercegovina). Glasnik zemaljskog Muzeja u Bosni i Hercegovini, 37 (1925), 125–135.Google Scholar
Owen, R., Palaeontology, or a systematic summary of extinct animals and their geological relations (Edinburgh: Adam and Charlos Black, 1860).Google Scholar
Rochebrune, A.-T. d., Revision des ophidiens fossiles du Muséum d’Histoire naturelle. Nouvelles Archives du Muséum d’Histoire Naturelle, 2éme Série, 3 (1880), 271–296.Google Scholar
Cope, E. D., On the reptilian orders, Pythonomorpha and Streptosauria. Proceedings of the Boston Society of Natural History, 12 (1869), 250–266.Google Scholar
Camp, C. L., Classification of the lizards. Bulletin of the American Museum of Natural History, 48 (1923), 289–481.Google Scholar
Russell, D. A., Systematics and morphololgy of American mosasaurs (Reptilia, Sauria). Peabody Museum of Natural History Bulletin, 23 (1967), 1–241.Google Scholar
Seeley, H. G., On remains of a small lizard from the Neocomian rocks of Comén, near Trieste, preserved in the Geological Museum of the University of Vienna. Quarterly Journal of the Geological Society of London, 37 (1881), 52–56.Google Scholar
Kornhuber, A., Über einen neuen fossilen Saurier aus Lesina. Abhandlungen der kaiserlich-königlichen geologischen Reichsanstalt, 5 (1873), 75–90.Google Scholar
Kornhuber, A., Carsosaurus Marchesettii, ein neuer fossiler Lacertilier aus den Kreideschichten des Karstes bei Komen. Abhandlungen der kaiserlich-königlichen geologischen Reichsanstalt, 17 (1893), 1–15.Google Scholar
Kornhuber, A., Opetiosaurus Bucchichi, eine neue fossile Eidechse aus der unteren Kreide von Lesina in Dalmatien. Abhandlungen der kaiserlich-königlichen geologischen Reichsanstalt, 17 (1901), 1–24.Google Scholar
Gorjanović-Kramberger, K., Aigialosaurus, eine neue Eidechse aus den Kreideschiefern der Insel Lesina, mit Rücksicht auf die bereits beschriebenen Lacertiden von Comen und Lesina. Glasnik hrvatskoga naravoslovnoga drustva u Zagrebu, 7 (1892), 74–106.Google Scholar
Nopcsa, F., Über die varanusartigen lacerten Istriens. Beiträge zur Paläontologie und Geologie Österreich-Ungarns und des Orients, 15 (1903), 31–42.Google Scholar
Boulenger, G. A., Notes on the Osteology of Heloderma horridum and H. suspectum, with Remarks on the Systematic Position of the Helodermatidæ and on the Vertebræ of the Lacertilia. Proceedings of the zoological Society of London, 59 (1891), 109–118.Google Scholar
Dollo, L., Les ancêtres des mosasauriens. Bulletin Scientifique de la France et de la Belgique, 38 (1903), 137–139.Google Scholar
McDowell, S. B. and Bogert, C. M., The systematic position of Lanthanotus and the affinities of the anguinomorphan lizards. Bulletin of the American Museum of Natural History, 105 (1954), 1–142.Google Scholar
Lee, M. S. Y., The phylogeny of varanoid lizards and the affinities of snakes. Philosophical Transactions of the Royal Society of London B, 352 (1997), 53–91.Google Scholar
Rieppel, O., Zaher, H., Tchernov, E., and Polcyn, M. J., The anatomy and relationships of Haasiophis terrasanctus, a fossil snake with well-developed hind limbs from the Mid-Cretaceous of the Middle East. Journal of Paleontology, 77 (2003), 536–558.Google Scholar
Palci, A. and Caldwell, M. W., Redescription of Acteosaurus tommasinii von Meyer, 1860, and a discussion of evolutionary trends within the clade Ophidiomorpha. Journal of Vertebrate Paleontology, 30 (2010), 94–108.CrossRefGoogle Scholar
Garberoglio, F. F., Apesteguia, S., Simoes, T., et al., New skulls and skeletons of the Cretaceous legged snake Najash, and the evolution of the modern snake body plan. Science Advances, 5 (2019), eaax5833.Google Scholar
Garberoglio, F. F., Gómez, R. O., Simões, T. R., Caldwell, M. W., and Apesteguía, S., The evolution of the axial skeleton intercentrum system in snakes revealed by new data from the Cretaceous snakes Dinilysia and Najash . Scientific Reports, 9 (2019), 1–10.Google Scholar
Caldwell, M. W., The Origin of Snakes: Morphology and the Fossil Record (Boca Raton: CRC Press, 2020).Google Scholar
Conrad, J. L., Phylogeny and systematics of Squamata (Reptilia) based on morphology. Bulletin of the American Museum of Natural History, 310 (2008), 1–182.CrossRefGoogle Scholar
Evans, S. E., A new anguimorph lizard from the Jurassic and Lower Cretaceous of England. Palaeontology, 37 (1994), 33–49.Google Scholar
Reeder, T. W., Townsend, T. M., Mulcahy, D. G., et al., Integrated analyses resolve conflicts over squamate reptile phylogeny and reveal unexpected placements for fossil taxa. PLoS ONE, 10 (2015), e0118199.Google Scholar
Hsiang, A. Y., Field, D. J., Webster, T. H., et al., The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evolutionary Biology, 15 (2015), 87.CrossRefGoogle ScholarPubMed
Caldwell, M. W., Snake phylogeny, origins, and evolution: the role, impact, and importance of fossils (1869–2006). In Anderson, J. S. and Sues, H.-D., ed., Evolutionary Transitions and Origins of Major Groups of Vertebrates (Bloomington, Indiana: Indiana University Press, 2007), pp. 253–302.Google Scholar
Paparella, I., Palci, A., Nicosia, U., and Caldwell, M. W., A new fossil marine lizard with soft tissues from the Late Cretaceous of southern Italy. Royal Society Open Science, 5 (2018), 172411.Google Scholar
Rieppel, O. and Head, J. J., New specimens of the fossil snake genus Eupodophis Rage & Escuillié, from Cenomanian (Late Cretaceous) of Lebanon. Memorie Soc Italiana Sci Nat, 32 (2004), 1–26.Google Scholar
Rage, J.-C. and Néraudeau, D., A new pachyostotic squamate reptile from the Cenomanian of France. Palaeontology, 47 (2004), 1195–1210.Google Scholar
Houssaye, A., ‘Pachyostosis’ in aquatic amniotes: a review. Integrative Zoology, 4 (2009), 325–340.Google Scholar
Polcyn, M. J., Jacobs, L. L., Araújo, R., Schulp, A. S., and Mateus, O., Physical drivers of mosasaur evolution. Palaeogeography, Palaeoclimatology, Palaeoecology, 400 (2014), 17–27.CrossRefGoogle Scholar
Gauthier, J., Kearney, M., Maisano, J. A., Rieppel, O., and Behlke, A. D. B., Assembling the squamate tree of life: Perspectives from the phenotype and the fossil record. Bulletin of the Peabody Museum of Natural History, 53 (2012), 3–308.Google Scholar
Zaher, H. and Smith, K. T., Pythons in the Eocene of Europe reveal a much older divergence of the group in sympatry with boas. Biology Letters, 16 (2020), 20200735.Google Scholar
Albino, A., Carrillo-Briceño, J. D., and Neenan, J. M., An enigmatic aquatic snake from the Cenomanian of Northern South America. PeerJ, 4 (2016), e2027.Google Scholar
Rage, J. C., Vullo, R., and Néraudeau, D., The mid-Cretaceous snake Simoliophis rochebrunei Sauvage, 1880 (Squamata: Ophidia) from its type area (Charentes, southwestern France): Redescription, distribution, and palaeoecology. Cretaceous Research, 58 (2016), 234–253.Google Scholar
Nessov, L. A., Zhegallo, V. I., and Averianov, A. O., A new locality of Late Cretaceous snakes, mammals and other vertebrates in Africa (western Libya). Annales de Paléontologie, 84 (1998), 265–274.CrossRefGoogle Scholar
Haas, G., On a new snakelike reptile from the lower Cenomanian of ‘Ein Yabrud, near Jerusalem. Bulletin du Museum National d’Histoire Naturelle, Paris, Série 4, 1 (1979), 51–64.Google Scholar
Haas, G., Pachyrhachis problematicus Haas, snakelike Reptile from the lower Cenomanian: ventral view of the skull. Bulletin du Museum National d’Histoire Naturelle, Paris, Série 2 (1980), 87–104.Google Scholar
Haas, G., Remarks on a new ophiomorph reptile from the Lower Cenomanian of Ein Jabrud, Israel. In Jacobs, L. L., ed., Aspects of Vertebrate History, in Honor of E H Colbert (Flagstaff, Arizona: Museum of Northern Arizona Press, 1980), pp. 177–92.Google Scholar
Lee, M. S. Y., Caldwell, M. W., and Scanlon, J. D., A second primitive marine snake: Pachyophis woodwardi from the Cretaceous of Bosnia-Herzegovina. Journal of Zoology, 248 (1999), 509–520.Google Scholar
Houssaye, A., Rediscovery and description of the second specimen of the hind-limbed snake Pachyophis woodwardi Nopcsa, 1923 (Squamata, Ophidia) from the Cenomanian of Bosnia Herzegovina . Journal of Vertebrate Paleontology, 30 (2011), 276–279.Google Scholar
Đurić, D., Radosavljević, D., Petrović, D., Radonjić , M., and Vojnović , P., A new evidence for pachyostotic snake from Turonian of Bosnia-Herzegovina. Geoloski anali Balkanskoga poluostrva, (2017), 17–21.Google Scholar
Lee, M. S. Y. and Caldwell, M. W., Anatomy and relationships of Pachyrhachis problematicus, a primitive snake with hindlimbs. Philosophical Transactions of the Royal Society of London B, 353 (1998), 1521–1552.Google Scholar
Zaher, H. and Rieppel, O., The phylogenetic relationships of Pachyrhachis problematicus, and the evolution of limblessness in snakes (Lepidosauria, Squamata). Comptes Rendus de Séances de l’Académie des Sciences (Série IIA), Earth and Planetary Science, 329 (1999), 831–837.Google Scholar
Zaher, H. and Rieppel, O., On the phylogenetic relationships of the Cretaceous snakes with legs, with special reference to Pachyrhachis problematicus (Squamata, Serpentes). Journal of Vertebrate Paleontology, 22 (2002), 104–109.Google Scholar
Rieppel, O. and Zaher, H., The intramandibular joint in squamates, and the phylogenetic relationships of the fossil snake Pachyrhachis problematicus Haas. Fieldiana Geology, 43 (2000), 1–69.Google Scholar
Polcyn, M. J., Jacobs, L. L., and Haber, A., A morphological model and CT assessment of the skull of Pachyrhachis problematicus (Squamata, Serpentes), a 98 million year old snake with legs from the Middle East. Palaeontologica Electronica, 8 (2005), 1–24.Google Scholar
Palci, A., Caldwell, M. W., and Nydam, R. L., Reevaluation of the anatomy of the Cenomanian (Upper Cretaceous) hind-limbed marine fossil snakes Pachyrhachis, Haasiophis, and Eupodophis . Journal of Vertebrate Paleontology, 33 (2013), 1328–1342.Google Scholar
Cundall, D. and Irish, F. J., The snake skull. In Gans, C., Gaunt, A. S. and Adler, K., eds., Biology of the Reptilia, Vol. 20, Morphology H, The Skull of Lepidosauria (Ithaca, New York: Society for the Study of Amphibians and Reptiles, 2008), pp. 349–692.Google Scholar
Zaher, H. and Scanferla, C. A., The skull of the Upper Cretaceous snake Dinilysia patagonica Smith-Woodward, 1901, and its phylogenetic position revisited. Zoological Journal of the Linnean Society, 164 (2012), 194–238.Google Scholar
Zaher, H., Apesteguía, S., and Scanferla, C. A., The anatomy of the Upper Cretaceous snake Najash rionegrina Apesteguía & Zaher, 2006, and the evolution of limblessness in snakes. Zoological Journal of the Linnean Society, 156 (2009), 801–826.Google Scholar
McDowell, S. B., The skull of Serpentes. In Gans, C., Gaunt, A. S., and Adler, K., eds., Biology of the Reptilia, Vol. 21, Morphology I, The Skull and Appendicular Locomotor Apparatus of Lepidosauria (Ithaca, New York: Society for the Study of Amphibians and Reptiles, 2008), pp. 467–620.Google Scholar
Lessmann, M. H., Zur labialen Pleurodontie an Lacertilier-Gebissen. Anatomischer Anzeiger, 99 (1952), 35–67.Google Scholar
Kochva, E., The origin of snakes and evolution of the venom apparatus. Toxicon, 25 (1987), 65–106.Google Scholar
deBraga, M. and Carroll, R. L., The origin of mosasaurs as a model of macroevolutionary patterns and processes. Evolutionary Biology, 27 (1993), 245–322.Google Scholar
Apesteguia, S. and Zaher, H., A Cretaceous terrestrial snake with robust hindlimbs and a sacrum. Nature, 440 (2006), 1037–1040.Google Scholar
Harrington, S. M. and Reeder, T. W., Phylogenetic inference and divergence dating of snakes using molecules, morphology and fossils: new insights into convergent evolution of feeding morphology and limb reduction. Biological Journal of the Linnean Society, 121 (2017), 379–394.Google Scholar
Martill, D. M., Tischlinger, H., and Longrich, N. R., A four-legged snake from the Early Cretaceous of Gondwana. Nature, 349 (2015), 416–419.Google Scholar
Kley, N. J., Prey transport mechanisms in blindsnakes and the evolution of unilateral feeding systems in snakes. American Zoologist, 41 (2001), 1321–1337.Google Scholar
Northcutt, R. G.. Forebrain and midbrain organization in lizards and its phylogenetic significance. In Greenberg, N. and Maclean, P. D., eds., Behavior and Neurology of Lizards (Rockville: National Institute of Mental Health, 1978), pp. 11–64.Google Scholar
Longrich, N. R., Bhullar, B.-A. S., and Gauthier, J. A., A transitional snake from the Late Cretaceous Period of North America. Nature, 488 (2012), 205–208.Google Scholar
Lee, M. S. Y., Bell, G. L., and Caldwell, M. W., The origin of snake feeding. Nature, 400 (1999), 655–659.Google Scholar

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