Global interrelationships of Plesiosauria (Reptilia, Sauropterygia) and the pivotal role of taxon sampling in determining the outcome of phylogenetic analyses

Previous attempts to resolve plesiosaurian phylogeny are reviewed and a new phylogenetic data set of 66 taxa (67% of ingroup taxa examined directly) and 178 characters (eight new) is presented. We recover two key novel results: a monophyletic Plesiosauridae comprising Plesiosaurus dolichodeirus, Hydrorion brachypterygius, Microcleidus homalospondylus, Occitanosaurus tournemirensis and Seeleyosaurus guilelmiimperatoris; and five plesiosaurian taxa recovered outside the split between Plesiosauroidea and Pliosauroidea. These taxa are Attenborosaurus conybeari, ‘Plesiosaurus’macrocephalus and a clade comprising Archaeonectrus rostratus, Macroplata tenuiceps and BMNH 49202. Based on this result, a new name, Neoplesiosauria, is erected for the clade comprising Plesiosauroidea and Pliosauroidea. Taxon subsamples of the new dataset are used to simulate previous investigations of global plesiosaurian relationships. Based on these simulations, most major differences between previous global phylogenetic hypotheses can be attributed to differences in taxon sampling. These include the position of Leptocleididae and Polycotylidae and the monophyly or paraphyly of Rhomaleosauridae. On this basis we favour the results recovered by our, larger analysis. Leptocleididae and Polycotylidae are sister taxa, forming a monophyletic clade within Plesiosauroidea, indicating that the large‐headed, short‐necked ‘pliosauromorph’ body plan evolved twice within Plesiosauria. Rhomaleosauridae forms the monophyletic sister taxon of Pliosauridae within Pliosauroidea. Problems are identified with previous phylogenetic definitions of plesiosaurian clades and new, stem‐based definitions are presented that should maintain their integrity over a range of phylogenetic hypotheses. New, rank‐free clade names Cryptoclidia and Leptocleidia are erected to replace the superfamilies Cryptoclidoidea and Leptocleidoidea. These were problematic as they were nested within the superfamily Plesiosauroidea. The incongruence length difference test indicates no significant difference in levels of homoplasy between cranial and postcranial characters.

[1]  F. O’Keefe,et al.  Morphologic and Ontogenetic Patterns in Elasmosaur Neck Length, with Comments on the Taxonomic Utility of Neck Length Variables , 2006 .

[2]  T. Rae,et al.  The Logical Basis for the use of Continuous Characters in Phylogenetic Systematics , 1998, Cladistics : the international journal of the Willi Hennig Society.

[3]  Michael S. Y. Lee,et al.  An archaic crested plesiosaur in opal from the Lower Cretaceous high-latitude deposits of Australia , 2006, Biology Letters.

[4]  P. Goloboff,et al.  Continuous characters analyzed as such , 2006, Cladistics : the international journal of the Willi Hennig Society.

[5]  F. O’Keefe,et al.  A Cladistic Analysis and Taxonomic Revision of the Plesiosauria (Reptilia: Sauropterygia) , 2001 .

[6]  F. Robin O'Keefe,et al.  The evolution of plesiosaur and pliosaur morphotypes in the Plesiosauria (Reptilia: Sauropterygia) , 2002, Paleobiology.

[7]  E. Frey,et al.  Osteology of Manemergus anguirostris n. gen. et sp., a new plesiosaur (Reptilia, Sauropterygia) from the Upper Cretaceous of Morocco , 2005, Palaeontographica Abteilung A.

[8]  William R. Wahl,et al.  Preliminary Report on the Osteology and Relationships of a New Aberrant Cryptocleidoid Plesiosaur from the Sundance Formation, Wyoming , 2003 .

[9]  S. Wroe,et al.  Bottom-Feeding Plesiosaurs , 2005, Science.

[10]  Richard A. Pimentcl,et al.  THE NATURE OF CLADISTIC DATA , 1987, Cladistics : the international journal of the Willi Hennig Society.

[11]  Tamaki Sato.  Description of plesiosaurs (reptillia: sauropterygia) from the Bearpaw Formation (campanian - maastrichtian) and a phylogenetic analysis of the elasmosauridae , 2002 .

[12]  H. Seeley.  Note on some of the Generic Modifications of the Plesiosaurian Pectoral Arch , 1874, Quarterly Journal of the Geological Society of London.

[13]  Gareth Nelson,et al.  Systematics and Biogeography: Cladistics and Vicariance , 1981 .

[14]  J. Wiffen,et al.  Late Cretaceous reptiles (Families Elasmosauridae and Pliosauridae) from the Mangahouanga Stream, North Island, New Zealand , 1986 .

[15]  Z. Gasparini,et al.  Marine reptiles from the Late Cretaceous of northern Patagonia , 2001 .

[16]  G. Storrs.  Morphological and Taxonomic Clarification of the Genus Plesiosaurus , 1997 .

[17]  I. Kitching.  Cladistics: The Theory and Practice of Parsimony Analysis , 1998 .

[18]  F. O’Keefe,et al.  Osteology of the Cryptocleidoid Plesiosaur Tatenectes laramiensis, with Comments on the Taxonomic Status of the Cimoliasauridae , 2009 .

[19]  H. Cappetta,et al.  The marine vertebrate faunas from the Late Cretaceous phosphates of Syria , 2000, Geological Magazine.

[20]  Z. Gasparini,et al.  A new cryptoclidid Plesiosaur from the Oxfordian (Late Jurassic) of Cuba , 2002 .

[21]  F. Nopcsa.  Palaeontological notes on reptiles , 1928 .

[22]  F. Robin O'Keefe,et al.  Correlated trends in the evolution of the plesiosaur locomotor system , 2005, Paleobiology.

[23]  J. Wiens.  Character analysis in morphological phylogenetics: problems and solutions. , 2001, Systematic biology.

[24]  J. GRAHAM KERR,et al.  The Osteology of the Reptiles , 1926, Nature.

[25]  A. Cruickshank.  A juvenile plesiosaur (Plesiosauria: Reptilia) from the Lower Lias (Hettangian: Lower Jurassic) of Lyme Regis, England: a pliosauroid-plesiosauroid intermediate? , 1994 .

[26]  G. Dyke,et al.  The skull of the giant predatory pliosaur Rhomaleosaurus cramptoni: implications for plesiosaur phylogenetics , 2008, Naturwissenschaften.

[27]  N. Bardet.  Evolution et extinction des reptiles marins au cours du mesozoique , 1992 .

[28]  K. Müller,et al.  PRAP-computation of Bremer support for large data sets. , 2004, Molecular phylogenetics and evolution.

[29]  K. Thiele.  THE HOLY GRAIL OF THE PERFECT CHARACTER: THE CLADISTIC TREATMENT OF MORPHOMETRIC DATA , 1993, Cladistics : the international journal of the Willi Hennig Society.

[30]  Carol J. Bult,et al.  Constructing a Significance Test for Incongruence , 1995 .

[31]  B. Small,et al.  New plesiosaurs from the Upper Cretaceous of Antarctica , 1989, Geological Society, London, Special Publications.

[32]  P. Upchurch,et al.  Systematics and phylogeny of Stegosauria (Dinosauria: Ornithischia) , 2008 .

[33]  K. Nixon,et al.  The Parsimony Ratchet, a New Method for Rapid Parsimony Analysis , 1999, Cladistics : the international journal of the Willi Hennig Society.

[34]  J. A. Massare.  Tooth morphology and prey preference of Mesozoic marine reptiles , 1987 .

[35]  G. Storrs,et al.  Cranial anatomy of a new plesiosaur genus from the lowermost Lias (Rhaetian/Hettangian) of Street, Somerset, England , 1996 .

[36]  D. Rosen,et al.  CENTERS OF ORIGIN AND RELATED CONCEPTS , 1974 .

[37]  Franziska Grossmann.  THE TAXONOMIC AND PHYLOGENETIC POSITION OF THE PLESIOSAUROIDEA FROM THE LOWER JURASSIC POSIDONIA SHALE OF SOUTH‐WEST GERMANY , 2007 .

[38]  K. Angielczyk.  NEW SPECIMENS OF THE TANZANIAN DICYNODONT “CRYPTOCYNODON PARRINGTONI” VON HUENE, 1942 (THERAPSIDA, ANOMODONTIA), WITH AN EXPANDED ANALYSIS OF PERMIAN DICYNODONT PHYLOGENY , 2007 .

[39]  F. O’Keefe,et al.  PRELIMINARY DESCRIPTION AND PHYLOGENETIC POSITION OF A NEW PLESIOSAUR (REPTILIA: SAUROPTERYGIA) FROM THE TOARCIAN OF HOLZMADEN, GERMANY , 2004 .

[40]  Derrick J. Zwickl,et al.  Increased taxon sampling greatly reduces phylogenetic error. , 2002, Systematic biology.

[41]  A. R. Templeton,et al.  PHYLOGENETIC INFERENCE FROM RESTRICTION ENDONUCLEASE CLEAVAGE SITE MAPS WITH PARTICULAR REFERENCE TO THE EVOLUTION OF HUMANS AND THE APES , 1983, Evolution; international journal of organic evolution.

[42]  Fred R. McMorris,et al.  Consensusn-trees , 1981 .

[43]  G. Storrs.  Anatomy and relationships of Corosaurus alcovensis (Diapsida: Sauropterygia) and the Triassic Alcova Limestone of Wyoming , 1991 .

[44]  J. Hawkins,et al.  Primary Homology Assessment, Characters and Character States , 1997, Cladistics : the international journal of the Willi Hennig Society.

[45]  N. Jalil,et al.  A new polycotylid plesiosaur from the Late Cretaceous (Turonian) of Morocco , 2003 .

[46]  D. Swofford.  PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[47]  H. James.  The osteology and phylogeny of the Hawaiian finch radiation (Fringillidae: Drepanidini), including extinct taxa , 2004 .

[48]  Michaela A. Taylor,et al.  A plesiosaur from the Linksfield erratic (Rhaetian, Upper Triassic) near Elgin, Morayshire , 1993, Scottish Journal of Geology.

[49]  A. Graybeal,et al.  Is it better to add taxa or characters to a difficult phylogenetic problem? , 1998, Systematic biology.

[50]  F. O’Keefe,et al.  Neoteny and the Plesiomorphic Condition of the Plesiosaur Basicranium , 2006 .

[51]  P. Godefroit,et al.  a new elasmosaurid plesiosaur from the Lower Jurassic of southern France , 1999 .

[52]  K. Carpenter.  Comparative Cranial Anatomy of Two North American Cretaceous Plesiosaurs , 1997 .

[53]  B. Kear.  Marine reptiles from the Lower Cretaceous of South Australia: elements of a high‐latitude cold‐water assemblage , 2006 .

[54]  Z. Gasparini,et al.  THE ELASMOSAURID PLESIOSAUR ARISTONECTES CABRERA FROM THE LATEST CRETACEOUS OF SOUTH AMERICA AND ANTARCTICA , 2003 .

[55]  A. Titus,et al.  PLESIOSAURS FROM THE UPPER CRETACEOUS (CENOMANIAN–TURONIAN) TROPIC SHALE OF SOUTHERN UTAH, PART 2:POLYCOTYLIDAE , 2007 .

[56]  F. O’Keefe,et al.  Cranial Anatomy and Taxonomy of Dolichorhynchops Bonneri New Combination, a Polycotylid (Sauropterygia: Plesiosauria) from the Pierre Shale of Wyoming and South Dakota , 2008 .

[57]  G. Storrs.  Function and phylogeny in sauropterygian (Diapsida) evolution , 1993 .

[58]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[59]  N. Bardet.  Extinction events among Mesozoic marine reptiles , 1994 .

[60]  K. Tanabe,et al.  Cretaceous plesiosaurs ate ammonites , 1998, Nature.

[61]  Franziska Grossmann.  Taxonomy, phylogeny and palaeoecology of the plesiosauroids (Sauropterygia, Reptilia) from the Posidonia shale (Toarcian, Lower Jurassic) of Holzmaden, south west Germany , 2006 .

[62]  M. Taylor.  Plesiosaurs — rigging and ballasting , 1981, Nature.

[63]  K. Carpenter.  A review of short-necked plesiosaurs from the Cretaceous of the western interior, North America , 1996 .

[64]  Derrick J. Zwickl,et al.  Increased taxon sampling is advantageous for phylogenetic inference. , 2002, Systematic biology.

[65]  Miriam Leah Zelditch,et al.  MORPHOMETRICS, HOMOLOGY, AND PHYLOGENETICS: QUANTIFIED CHARACTERS AS SYNAPOMORPHIES , 1995 .

[66]  P. Upchurch,et al.  An analysis of dinosaurian biogeography: evidence for the existence of vicariance and dispersal patterns caused by geological events , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  J. Sepkoski,et al.  Estimating paleodiversities: a test of the taxic and phylogenetic methods , 2005, Paleobiology.

[68]  M. Wilkinson.  MISSING ENTRIES AND MULTIPLE TREES: INSTABILITY, RELATIONSHIPS, AND SUPPORT IN PARSIMONY ANALYSIS , 2003 .

[69]  P. Wagner.  Exhaustion of morphologic character states among fossil taxa. , 2000, Evolution; international journal of organic evolution.

[70]  D. Brown.  THE ENGLISH UPPER JURASSIC PLESIOSAUROIDEA (REPTILIA) AND A REVIEW OF THE PHYLOGENY AND CLASSIFICATION OF THE PLESIOSAURIA , 1981 .

[71]  D. Watson,et al.  The Elasmosaurid Shoulder-girdle and Fore-limb. , 2009 .

[72]  B. Kear.  A NEW ELASMOSAURID PLESIOSAUR FROM THE LOWER CRETACEOUS OF QUEENSLAND, AUSTRALIA , 2005 .

[73]  P. Wagner,et al.  Systematics and the Fossil Record , 1994 .

[74]  Chun Li,et al.  FIRST COMPLETE PISTOSAUROID FROM THE TRIASSIC OF CHINA , 2006 .

[75]  S. Welles.  Elasmosaurid plesiosaurs with description of new material from California and Colorado , 1943 .

[76]  Ellen E. Strong,et al.  Character Coding and Inapplicable Data , 1999 .

[77]  M. Novacek,et al.  FOSSILS, PHYLOGENY, AND TAXONOMIC RATES OF EVOLUTION , 1982 .

[78]  Mário C. C. Pinna.  CONCEPTS AND TESTS OF HOMOLOGY IN THE CLADISTIC PARADIGM , 1991 .

[79]  S. Sachs,et al.  Redescription of Elasmosaurus platyurus Cope 1868 (Plesiosauria: Elasmosauridae) from the Upper Cretaceous (lower Campanian) of Kansas, USA , 2005 .

[80]  Sudhir Kumar,et al.  Incomplete taxon sampling is not a problem for phylogenetic inference , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[81]  O. Rieppel.  Osteology of Simosaurus gaillardoti and the relationships of stem-group Sauropterygia / Olivier Rieppel --. , 1994 .

[82]  G. Storrs.  An examination of Plesiosauria (Diapsida: Sauropterygia) from the Niobrara Formation (Upper Cretaceous) of central North America , 1999 .

[83]  K. Müller.  The efficiency of different search strategies in estimating parsimony jackknife, bootstrap, and Bremer support , 2005, BMC Evolutionary Biology.

[84]  Owen.  Monograph of the Fossil Reptilia of the Liassic Formations. Part First. Sauropterygia , 1865 .

[85]  T. E. White.  Holotype of Plesiosaurus longirostris Blake and classification of the Plesiosaurs , 1940 .

[86]  D. Swofford,et al.  Taxon sampling revisited , 1999, Nature.

[87]  R. Fordyce,et al.  A New Marine Reptile (Sauropterygia) from New Zealand: Further Evidence for A Late Cretaceous Austral Radiation of Cryptoclidid Plesiosaurs , 2002 .

[88]  J. A. Massare.  Mechanics and Physiology of Animal Swimming: Swimming capabilities of Mesozoic marine reptiles: a review , 1994 .

[89]  M. Taylor.  Sea-saurians for sceptics , 1989, Nature.

[90]  C. Humphries,et al.  CLADISTICS AND COMPUTERS: A CHIRONOMID CONUNDRUM? , 1988 .

[91]  J. Gray.  A Synopsis of the genera of Reptiles and Amphibia, with a description of some new species. , 1825 .

[92]  G. Storrs.  Fossil vertebrate faunas of the British Rhaetian (latest Triassic) , 1994 .

[93]  M. Källersjö,et al.  Taxon sampling and seed plant phylogeny , 2002, Cladistics : the international journal of the Willi Hennig Society.

[94]  M. Wilkinson.  Common Cladistic Information and its Consensus Representation: Reduced Adams and Reduced Cladistic Consensus Trees and Profiles , 1994 .

[95]  S. Williston.  The skull of Brachauchenius , with observations on the relationships of the plesiosaurs , 1907 .

[96]  R. Owen.  A Monograph of the Fossil Reptilia of the Liassic Formations , 2010 .

[97]  A. Russell,et al.  A phylogeny of Plesiosauria (Sauropterygia) and its bearing on the systematic status of Leptocleidus Andrews, 1922 , 2008 .