Hostname: page-component-848d4c4894-p2v8j Total loading time: 0 Render date: 2024-05-09T04:09:01.927Z Has data issue: false hasContentIssue false

Landlubbers to leviathans: evolution of swimming in mosasaurine mosasaurs

Published online by Cambridge University Press:  08 April 2016

Johan Lindgren
Affiliation:
Department of Earth and Ecosystem Sciences, Lund University, Sölvegatan 12, SE-223 62 Lund, Sweden. E-mail: johan.lindgren@geol.lu.se
Michael J. Polcyn
Affiliation:
Department of Earth Sciences, Southern Methodist University, 3225 Daniel Avenue, Dallas, Texas 75275. E-mail: mpolcyn@smu.edu
Bruce A. Young
Affiliation:
Department of Physical Therapy, University of Massachusetts Lowell, 3 Solomont Way, Lowell, Massachusetts 01854. E-mail: bruce_young@uml.edu

Abstract

Incremental stages of major evolutionary transitions within a single animal lineage are rarely observed in the fossil record. However, the extraordinarily complete sequence of well preserved material spanning the 27-Myr existence of the marine squamate subfamily Mosasaurinae provides a unique exception. By comparison with extant and extinct analogs, the tail morphology of four mosasaurine genera is examined, revealing a pattern of evolution that begins with the generalized varanoid anatomy and culminates in a high-aspect-ratio fin, similar to that of sharks. However, unlike the epicercal caudal fluke of selachians in which the tail bends dorsocaudally, derived mosasaurs develop a hypocercal tail with a ventrocaudal bend. Progressive caudal regionalization, reduced intervertebral mobility, increased tail depth due to a marked downturn of the posterior caudal segment, and the development of finlike paired appendages reveal a pattern of adaptation toward an optimized marine existence. This change in morphology reflects a transition from anguilliform or sub-carangiform locomotion to carangiform locomotion, and indicates a progressive shift from nearshore dwellers to pelagic cruisers—a change in foraging habitat independently corroborated by paleobiogeographic, stable isotope, osteohistological, and paleopathological data. Evolutionary patterns similar to those observed in mosasaurine mosasaurs are seen in other secondarily aquatically adapted amniotes, notably metriorhynchid crocodyliforms, cetaceans, and ichthyosaurs, and may be explained by developmental modularity governing the observed phenotypic expression.

Type
Articles
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Ali, S. M. 1941. Studies on the comparative anatomy of the tail in Sauria and Rhynchocephalia. Part I. Sphenodon punctatus Gray. Proceedings of the Indian Academy of Sciences 13:171192.Google Scholar
Ali, S. M. 1949. Studies on the comparative anatomy of the tail in Sauria and Rhynchocephalia. Part III. Varanus monitor (Linné). Proceedings of the Indian Academy of Sciences 32:155167.Google Scholar
Bateman, P. W., and Fleming, P. A. 2009. To cut a long tail short: a review of lizard caudal autotomy studies carried out over the last 20 years. Journal of Zoology 277:114.Google Scholar
Bedford, G. S., and Christian, K. A. 1996. Tail morphology related to habitat of varanid lizards and some other reptiles. Amphibia-Reptilia 17:131140.Google Scholar
Bell, G. L. Jr. 1997. A phylogenetic revision of North American and Adriatic Mosasauroidea. Pp. 293332 in Callaway, J. M. and Nicholls, E. L., eds. Ancient marine reptiles. Academic Press, San Diego.Google Scholar
Bell, G. L. Jr., and Polcyn, M. J. 2005. Dallasaurus turneri, a new primitive mosasauroid from the Middle Turonian of Texas and comments on the phylogeny of Mosasauridae (Squamata). Netherlands Journal of Geosciences 84:177194.Google Scholar
Bemis, W. E., and Grande, L. 1999. Development of the median fins of the North American paddlefish (Polyodon spathula), and a reevaluation of the lateral fin-fold hypothesis. Pp. 4168 in Arratia, G. and Schultze, H.-P., eds. Mesozoic fishes II: systematics and fossil record. Dr. Friedrich Pfeil, Munich.Google Scholar
Blake, R. W. 2004. Fish functional design and swimming performance. Journal of Fish Biology 65:11931222.Google Scholar
Borazjani, I., and Sotiropoulos, F. 2010. On the role of form and kinematics on the hydrodynamics of self-propelled body/caudal fin swimming. Journal of Experimental Biology 213:89107.Google Scholar
Braun, J., and Reif, W.-E. 1985. A survey of aquatic locomotion in fishes and tetrapods. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 169:307332.Google Scholar
Breder, C. M. 1926. The locomotion of fishes. Zoologica 4:159297.Google Scholar
Buchholtz, E. A. 1998. Implications of vertebral morphology for locomotor evolution in early Cetacea. Pp. 325351 in Thewissen, J. G. M., ed. The emergence of whales: evolutionary patterns in the origin of Cetacea. Plenum, New York.CrossRefGoogle Scholar
Buchholtz, E. A. 2001a. Swimming styles in Jurassic ichthyosaurs. Journal of Vertebrate Paleontology 21:6173.Google Scholar
Buchholtz, E. A. 2001b. Vertebral osteology and swimming style in living and fossil whales (Order: Cetacea). Journal of Zoology, London 253:175190.Google Scholar
Buchholtz, E. A. 2007. Modular evolution of the cetacean vertebral column. Evolution and Development 9:278289.Google Scholar
Buchholtz, E. A., and Schur, S. A. 2004. Vertebral osteology in Delphinidae (Cetacea). Zoological Journal of the Linnean Society 140:383401.Google Scholar
Caldwell, M. W. 1996. Ontogeny and phylogeny of the mesopodial skeleton in mosasauroid reptiles. Zoological Journal of the Linnean Society 116:407436.CrossRefGoogle Scholar
Caldwell, M. W. 2002. From fins to limbs to fins: limb evolution in fossil marine reptiles. American Journal of Medical Genetics 112:236249.Google Scholar
Caldwell, M. W. 2006. A new species of Pontosaurus (Squamata, Pythonomorpha) from the Upper Cretaceous of Lebanon and a phylogenetic analysis of Pythonomorpha. Memoire della Società Italiana di Scienze Naturali e del Museo Civico di Storia Narurale di Milano 34:142.Google Scholar
Caldwell, M. W., and Diedrich, C. G. 2005. Remains of Clidastes Cope, 1868, an unexpected mosasaur in the upper Campanian of NW Germany. Netherlands Journal of Geosciences 84:213220.Google Scholar
Caldwell, M. W., Carroll, R. L., and Kaisar, H. 1995. The pectoral girdle and forelimb of Carsosaurus marchesetti (Aigialosauridae), with a preliminary phylogenetic analysis of mosasauroids and varanoids. Journal of Vertebrate Paleontology 15:516531.CrossRefGoogle Scholar
Camp, C. L. 1942. California mosasaurs. Memoirs of the University of California 13:168.Google Scholar
Carroll, R. L. 1997. Mesozoic marine reptiles as models of long-term, large-scale evolutionary phenomena. Pp. 467489 in Callaway, J. M. and Nicholls, E. L., eds. Ancient marine reptiles. Academic Press, San Diego.CrossRefGoogle Scholar
Carroll, R. L., and deBraga, M. 1992. Aigialosaurs: mid-Cretaceous varanoid lizards. Journal of Vertebrate Paleontology 12:6686.Google Scholar
Clementz, M. T., and Koch, P. L. 2001. Differentiating aquatic mammal habitat and foraging ecology with stable isotopes in tooth enamel. Oecologia 129:461472.Google Scholar
Compagno, L. J. V. 1999. Systematics and body form. Pp. 142 in Hamlett, W. C., ed. Sharks, skates, and rays. Johns Hopkins University Press, Baltimore.Google Scholar
Conrad, J. L. 2008. Phylogeny and systematics of Squamata (Reptilia) based on morphology. Bulletin of the American Museum of Natural History 310:1183.Google Scholar
deBraga, M., and Carroll, R. L. 1993. The origin of mosasaurs as a model of macroevolutionary patterns and processes. Evolutionary Biology 27:245322.Google Scholar
Dortangs, R. W., Schulp, A. S., Mulder, E. W. A., Jagt, J. W. M., Peeters, H. H. G., and De Graaf, D. Th. 2002. A large new mosasaur from the Upper Cretaceous of The Netherlands. Netherlands Journal of Geosciences 81:18.Google Scholar
Dutchak, A. R., and Caldwell, M. W. 2006. Redescription of Aigialosaurus dalmaticus Kramberger, 1892, a Cenomanian mosasauroid lizard from Hvar Island, Croatia. Canadian Journal of Earth Sciences 43:18211834.Google Scholar
Everhart, M. J. 2005. Oceans of Kansas: a natural history of the Western Interior Sea. Indiana University, Bloomington.Google Scholar
Everhart, M. J., ed. 2008. Proceedings of the second mosasaur meeting. Fort Hays Studies Special Issue 3. Fort Hays State University, Hays, Kansas.Google Scholar
Ferry, L. A., and Lauder, G. V. 1996. Heterocercal tail function in leopard sharks: a three-dimensional kinematic analysis of two models. Journal of Experimental Biology 199:22532268.Google Scholar
Graham, J. B., Lowell, W. R., Rubinoff, I., and Motta, J. 1987. Surface and subsurface swimming of the sea snake Pelamis platurus . Journal of Experimental Biology 127:2744.Google Scholar
Hildebrand, M. 1995. Analysis of vertebrate structure. Wiley, New York.Google Scholar
Jacobs, L. L., Polcyn, M. J., Taylor, L. H., and Ferguson, K. 2005. Sea-surface temperatures and palaeoenvironments of dolichosaurs and early mosasaurs. Netherlands Journal of Geosciences 84:269281.CrossRefGoogle Scholar
Jacobs, L. L., Mateus, O., Polcyn, M. J., Schulp, A. S., Antunes, M. T., Morais, M. L., and da Silva Tavares, T. 2006. The occurrence and geological setting of Cretaceous dinosaurs, mosasaurs, plesiosaurs, and turtles from Angola. Journal of the Paleontological Society of Korea 22:91110.Google Scholar
Jacobs, L. L., Mateus, O., Polcyn, M. J., Schulp, A. S., Scotese, C. R., Goswami, A., Ferguson, K. M., Robbins, J. A., Vineyard, D. P., and Neto, A. Buto 2009. Cretaceous paleogeography, paleoclimatology, and amniote biogeography of the low and mid-latitude South Atlantic Ocean. Bulletin de la Société Géologique de France 180:333341.Google Scholar
Kuratani, S. 2009. Modularity, comparative embryology and evodevo: developmental dissection of evolving body plans. Developmental Biology 332:6169.Google Scholar
Lindgren, J. 2007. First record of Halisaurus (Squamata: Mosasauridae) from the Pacific coast of North America. PaleoBios 27:4047.Google Scholar
Lindgren, J., and Siverson, M. 2004. The first record of the mosasaur Clidastes from Europe and its palaeogeographical implications. Acta Palaeontologica Polonica 49:219234.Google Scholar
Lindgren, J., Jagt, J. W. M., and Caldwell, M. W. 2007. A fishy mosasaur: the axial skeleton of Plotosaurus (Reptilia, Squamata) reassessed. Lethaia 40:153160.Google Scholar
Lindgren, J., Caldwell, M. W., and Jagt, J. W. M. 2008. New data on the postcranial anatomy of the California mosasaur Plotosaurus bennisoni (Camp, 1942) (Upper Cretaceous: Maastrichtian), and the taxonomic status of P. tuckeri (Camp, 1942). Journal of Vertebrate Paleontology 28:10431054.CrossRefGoogle Scholar
Lindgren, J., Alwmark, C., Caldwell, M. W., and Fiorillo, A. R. 2009. Skin of the Cretaceous mosasaur Plotosaurus: implications for aquatic adaptations in giant marine reptiles. Biology Letters 5:528531.Google Scholar
Lindgren, J., Caldwell, M. W., Konishi, T., and Chiappe, L. M. 2010. Convergent evolution in aquatic tetrapods: insights from an exceptional fossil mosasaur. PLoS ONE 5(8):e11998. doi: 10.1371/journal.pone.0011998.Google Scholar
Lindsey, C. C. 1978. Form, function and locomotory habits in fish. Pp. 1100 in Hoar, W. S. and Randall, D. J., eds. Fish physiology. Locomotion 7. Academic Press, London.Google Scholar
Lingham-Soliar, T. 2000. The mosasaur Mosasaurus lemonnieri (Lepidosauromorpha, Squamata) from the Upper Cretaceous of Belgium and The Netherlands. Paleontological Journal 34(Suppl. 2):S225S237.Google Scholar
Lingham-Soliar, T. 2005. Caudal fin in the white shark, Carcharodon carcharias (Lamnidae): a dynamic propeller for fast, efficient swimming. Journal of Morphology 264:233252.Google Scholar
Lingham-Soliar, T., and Nolf, D. 1990. The mosasaur Prognathodon (Reptilia, Mosasauridae) from the Upper Cretaceous of Belgium. Bulletin de l'Institut Royal des Sciences Naturelles de Belgique, Sciences de la Terre 59:137190.Google Scholar
Little, C. D., and Bemis, W. E. 2004. Observations on the skeleton of the heterocercal tail of sharks (Chondrichthyes: Elasmobranchii). Pp. 563573 in Arratia, G., Wilson, M. V. H., and Cloutier, R., eds. Recent advances in the origin and early radiation of vertebrates. Dr. Friedrich Pfeil, Munich.Google Scholar
Martin, J. E. 2007. A new species of the durophagous mosasaur Globidens (Squamata: Mosasauridae) from the Late Cretaceous Pierre Shale Group of central South Dakota, USA. Geological Society of America Special Paper 427:177198.Google Scholar
Martin, J. E., and Bell, G. L. Jr. 1995. Abnormal caudal vertebrae of Mosasauridae from Late Cretaceous marine deposits of South Dakota. Proceedings of the South Dakota Academy of Sciences 74:2327.Google Scholar
Martin, L. D., and Rothschild, B. M. 1989. Paleopathology and diving mosasaurs. American Scientist 77:460467.Google Scholar
Martin, B. L., Peyrot, S. M., and Harland, R. M. 2007. Hedgehog signaling regulates the amount of hypaxial muscle development during Xenopus myogenesis. Developmental Biology 304:722734.Google Scholar
Massare, J. A. 1987. Tooth morphology and prey preference of Mesozoic marine reptiles. Journal of Vertebrate Paleontology 7:121137.Google Scholar
Massare, J. A. 1988. Swimming capabilities of Mesozoic marine reptiles: implications for method of predation. Paleobiology 14:187205.Google Scholar
McGlinn, E., and Tabin, C. J. 2006. Mechanistic insight into how Shh patterns the vertebrate limb. Current Opinions in Genetics & Development 16:426432.Google Scholar
McGowan, C. 1989. The ichthyosaurian tailbend: a verification problem facilitated by computed tomography. Paleobiology 15:429436.CrossRefGoogle Scholar
McMillen, T., and Holmes, P. 2006. An elastic rod model for anguilliform swimming. Journal of Mathematical Biology 53:843886.Google Scholar
Motani, R. 2002. Swimming speed estimation of extinct marine reptiles: energetic approach revisited. Paleobiology 28:251262.Google Scholar
Motani, R., You, H., and McGowan, C. 1996. Eel-like swimming in the earliest ichthyosaurs. Nature 382:347348.CrossRefGoogle Scholar
Mulder, E. W. A. 2001. Co-ossified vertebrae of mosasaurs and cetaceans: implications for the mode of locomotion of extinct marine reptiles. Paleobiology 27:724734.Google Scholar
Müller, U. K., and van Leeuwen, J. L. 2006. Undulatory fish swimming: from muscles to flow. Fish and Fisheries 7:84103.Google Scholar
Polcyn, M. J., Tchernov, E., and Jacobs, L. L. 1999. 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 15:259290.Google Scholar
Polcyn, M. J., Bell, G. L. Jr., Shimada, K., and Everhart, M. J. 2008. The oldest North American mosasaurs (Squamata: Mosasauridae) from the Turonian (Upper Cretaceous) of Kansas and Texas with comments on the radiation of major mosasaur clades. Pp. 137155 in Everhart, 2008.Google Scholar
Rieppel, O., Conrad, J. L., and Maisano, J. A. 2007. New morphological data for Eosaniwa koehni Haubold, 1977 and a revised phylogenetic analysis. Journal of Paleontology 81:760769.Google Scholar
Robbins, J. A., Ferguson, K. M., Polcyn, M. J., and Jacobs, L. L. 2008. Application of stable carbon isotope analysis to mosasaur ecology. Pp. 123130 in Everhart, 2008.Google Scholar
Rothschild, B. M., and Martin, L. R. 2006. Skeletal impact of disease. New Mexico Museum of Natural History and Science Bulletin 33:1226.Google Scholar
Rothschild, B. M., Martin, L. D., and Schulp, A. S. 2005. Sharks eating mosasaurs, dead or alive? Netherlands Journal of Geosciences 84:335340.Google Scholar
Russell, D. A. 1967. Systematics and morphology of American mosasaurs (Reptilia, Sauria). Peabody Museum of Natural History, Yale University, Bulletin 23:1241.Google Scholar
Schumacher, B. A., and Varner, D. W. 1996. Mosasaur caudal anatomy. Journal of Vertebrate Paleontology 16(Suppl. to No. 3):63A.Google Scholar
Schumacher, B. A. 2007. Morphology and function of tailbends in mosasaurs. Pp. 4142 in Everhart, M. J., ed. Second mosasaur meeting, abstract booklet and field guide. Sternberg Museum of Natural History, Fort Hays State University, Hays, Kansas.Google Scholar
Sheldon, A. 1997. Ecological implications of mosasaur bone microstructure. Pp. 333354 in Callaway, J. M. and Nicholls, E. L., eds. Ancient marine reptiles. Academic Press, San Diego.Google Scholar
Sheldon, A., and Bell, G. L. Jr. 1999. Paedomorphosis in Mosasauroidea (Squamata): evidence from fossil bone microstructure. Paludicola 2:190205.Google Scholar
Shubin, N., Tabin, C., and Carroll, S. 1997. Fossils, genes and the evolution of animal limbs. Nature 388:639648.Google Scholar
Shubin, N. 2009. Deep homology and the origins of evolutionary novelty. Nature 457:818823.Google Scholar
Smith, K., and Buchy, M.-C. 2008. A new aigialosaur (Squamata: Anguimorpha) with soft tissue remains from the Upper Cretaceous of Nuevo León, Mexico. Journal of Vertebrate Paleontology 28:8594.Google Scholar
Taylor, M. A. 1994. Stone, bone or blubber? Buoyancy control strategies in aquatic tetrapods. Pp. 151161 in Maddock, L., Bone, Q., and Rayner, J. M. V., eds. Mechanics and physiology of animal swimming. Cambridge University Press, New York.Google Scholar
Taylor, W. R., and van Dyke, G. C. 1985. Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium 9:107119.Google Scholar
Thomson, K. S. 1976. On the heterocercal tail in sharks. Paleobiology 2:1938.Google Scholar
Videler, J. J. 1993. Fish swimming. Chapman and Hall, London.Google Scholar
Webb, P. W., and Smith, G. 1980. Function of the caudal fin in early fishes. Copeia 3:559562.Google Scholar
Wilga, C. A. D., and Lauder, G. V. 2004a. Hydrodynamic function of the shark's tail. Nature 430:850.CrossRefGoogle ScholarPubMed
Wilga, C. A. D. 2004b. Biomechanics of locomotion in sharks, rays, and chimeras. Pp. 139164 in Carrier, J. C., Music, J. A., and Heithaus, M. R., eds. Biology of sharks and their relatives. CRC Press, London.CrossRefGoogle Scholar
Williston, S. W. 1897. Restoration of Kansas mosasaurs. Kansas University Quarterly 6:107110.Google Scholar
Williston, S. W. 1898. Mosasaurs. University Geological Survey of Kansas 4:83221.Google Scholar
Wiman, C. 1920. Some reptiles from the Niobrara Group in Kansas. Bulletin of the Geological Institute of Upsala 18:918.Google Scholar
Witmer, L. M. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. Pp. 1933 in Thomason, J., ed. Functional morphology in vertebrate paleontology. Cambridge University, New York.Google Scholar
Young, B. A., Boetig, M., Fahey, A., and Lawrence, A. 2008. The diversity of aquatic locomotion in extant varanoid lizards. Pp. 159167 in Everhart, 2008.Google Scholar