The phylogeny and evolution of Cretaceous–Palaeogene metatherians: cladistic analysis and description of new early Palaeocene specimens from the Nacimiento Formation, New Mexico

Metatherian mammals were the most diverse mammalian clade in North America through the Late Cretaceous, but they underwent a severe extinction at the Cretaceous–Palaeogene (K-Pg) boundary. In order to clarify the origin of Palaeogene metatherians and the pattern of metatherian survivorship across the K-Pg boundary we conducted an inclusive species-level phylogenetic analysis of Cretaceous and early Palaeogene metatherian taxa. This analysis includes information from new Palaeocene specimens from south-western North America. Both the phylogenetic topology and information from new specimens support the validity of the genus Thylacodon and justify the recognition of a new species, T. montanensis. Thylacodon is closely related to Swaindelphys and Herpetotheriidae, which must have diverged by the latest Cretaceous due to its close relationship with late Campanian Ectocentrocristus. Pediomyidae and ‘Peradectidae sensu lato’ together comprise a major metatherian clade. Maastrichtidelphys, from the Late Cretaceous of the Netherlands, is the oldest member of ‘Peradectidae sensu lato’, indicating a Cretaceous origination for this group. Therefore, the major groups Herpetotheriidae and ‘Peradectidae sensu lato’, represented almost completely by Palaeocene taxa, must have originated in the Late Cretaceous. The lineages leading to these clades include at least four lineages that must have crossed the K-Pg boundary and therefore confirm that the K-Pg boundary marked a profound extinction event for metatherians and suggests that Palaeogene taxa originated from only a few clades of Cretaceous species, all of which were relatively minor or very rare components of known Cretaceous mammalian faunas.

[1]  W. Clemens Were Immigrants a Significant Part of the Earliest Paleocene Mammalian Fauna of the North American Western Interior , 2010 .

[2]  J. Lillegraven Latest Cretaceous mammals of upper part of Edmonton Formation of Alberta, Canada, and review of marsupial-placental dichotomy in mammalian evolution , 1969 .

[3]  Nobuyuki Itoh,et al.  Regulation of Mammalian Tooth Cusp Patterning by Ectodin , 2005, Science.

[4]  P. Sereno The logical basis of phylogenetic taxonomy. , 2005, Systematic biology.

[5]  C. de Muizon,et al.  The oldest modern therian mammal from Europe and its bearing on stem marsupial paleobiogeography , 2009, Proceedings of the National Academy of Sciences.

[6]  A. Weil,et al.  Cimolestids (Mammalia) from the Early Paleocene (Puercan) of New Mexico , 2011 .

[7]  Zhe‐Xi Luo,et al.  In quest for a phylogeny of Mesozoic mammals , 2002 .

[8]  Van Valen,et al.  Deltatheridia, a new order of mammals. Bulletin of the AMNH ; v. 132, article 1 , 1966 .

[9]  G. Wilson Mammalian Faunal Dynamics During the Last 1.8 Million Years of the Cretaceous in Garfield County, Montana , 2005, Journal of Mammalian Evolution.

[10]  J. Eberle,et al.  A new important record of earliest Cenozoic mammalian history :geologic setting, Multituberculata, and Peradectia , 1998 .

[11]  T. Rowe Definition and Diagnosis in the Phylogenetic System , 1987 .

[12]  L. Taylor,et al.  New species of Peradectes and Swaindelphys (Mammalia: Metatheria) from the Early Paleocene (Torrejonian) Nacimiento Formation, San Juan Basin, New Mexico, USA , 2011 .

[13]  A. Sahni The vertebrate fauna of the Judith River Formation, Montana. Bulletin of the AMNH ; v. 147, article 6 , 1972 .

[14]  Brian M. Davis,et al.  A revision of "pediomyid" marsupials from the Late Cretaceous of North America , 2007 .

[15]  Kirk R. Johnson,et al.  The Hell Creek Formation and the Cretaceous-Tertiary boundary in the northern Great Plains : an integrated continental record of the end of the Cretaceous , 2002 .

[16]  R. C. Fox The Wounded Knee local fauna and mammalian evolution near the Cretaceous-Tertiary boundary, Saskatchewan, Canada , 1989 .

[17]  W. Clemens Early Paleocene (Puercan) peradectid marsupials from northeastern Montana, North American Western Interior , 2006, Palaeontographica Abteilung A.

[18]  C. Muizon,et al.  THE AFFINITIES OF ROBERTHOFFSTETTERIA NATIONALGEOGRAPHICA (MARSUPIALIA) AND THE ORIGIN OF THE POLYDOLOPINE MOLAR PATTERN , 2003 .

[19]  T. E. Macrini,et al.  Exceptionally preserved North American Paleogene metatherians: adaptations and discovery of a major gap in the opossum fossil record , 2007, Biology Letters.

[20]  G. Wilson,et al.  New Latest Cretaceous Mammals from Northeastern Colorado with Biochronologic and Biogeographic Implications , 2010 .

[21]  A. Weil,et al.  Metatherian Mammals from the Naashoibito Member, Kirtland Formation, San Juan Basin, New Mexico and Their Biochronologic and Paleobiogeographic Significance , 2008 .

[22]  L. Krishtalka,et al.  Revision of the Wind River faunas, early Eocene of central Wyoming. Part 3. Marsupialia , 1983, Annals of the Carnegie Museum.

[23]  Kirk R. Johnson,et al.  Correlated terrestrial and marine evidence for global climate changes before mass extinction at the Cretaceous–Paleogene boundary , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[24]  J. Alroy,et al.  Mammalian Dispersal at the Paleocene/Eocene Boundary , 2002, Science.

[25]  John J. Wiens,et al.  Missing data and the design of phylogenetic analyses , 2006, J. Biomed. Informatics.

[26]  C. de Muizon,et al.  A NEW BASAL “DIDELPHOID” (MARSUPIALIA, MAMMALIA) FROM THE EARLY PALEOCENE OF TIUPAMPA (BOLIVIA) , 2001 .

[27]  R. C. Fox,et al.  Paleocene and Late Cretaceous Mammals from Saskatchewan, Canada , 1984 .

[28]  C. C. Paleocene Faunas of the San Juan Basin, New Mexico , 1937, Nature.

[29]  L. Marshall,et al.  The down of the age of mammals in South America , 1984 .

[30]  Cynthia L. Gordon A First Look at Estimating Body Size in Dentally Conservative Marsupials , 2003, Journal of Mammalian Evolution.

[31]  G. Wilson,et al.  New Specimen Reveals Delta Theroidan Affinities of the North American Late Cretaceous Mammal Nanocuris , 2010 .

[32]  J. Bloch,et al.  Cranial Anatomy of the Earliest Marsupials and the Origin of Opossums , 2009, PloS one.

[33]  Donald L. Lofgren The Bug Creek Problem and the Cretaceous-Tertiary Transition at McGuire Creek, Montana , 1995 .

[34]  F. Szalay Mixodectidae, Microsyopidae, and the insectivore-primate transition , 1969 .

[35]  M. Novacek,et al.  Implications of Deltatheridium specimens for early marsupial history , 1998, Nature.

[36]  J. Wiens,et al.  INCOMPLETE TAXA, INCOMPLETE CHARACTERS, AND PHYLOGENETIC ACCURACY: IS THERE A MISSING DATA PROBLEM? , 2003 .

[37]  D. Wolberg,et al.  The Therian mammalian fauna (Campanian) of Quarry 1, Fossil Forest study area, San Juan Basin, New Mexico , 1987 .

[38]  Barbara S. Grandstaff,et al.  Alphadon (Marsupialia) and Multituberculata (Allotheria) in the Cretaceous of eastern North America , 1992 .

[39]  J. Archibald,et al.  Placental nature of the alleged marsupial from the Cretaceous of Madagascar , 2003 .

[40]  W. Korth Evolution of Tertiary Mammals of North America: Marsupialia , 2008 .

[41]  W. Matthew,et al.  New genera of Paleocene mammals. American Museum novitates ; no. 13 , 1921 .

[42]  J. Archibald,et al.  Differential Cretaceous/Tertiary extinctions of nonmarine vertebrates; Evidence from northeastern Montana , 1990 .

[43]  R. Cifelli Chapter 5: Marsupial Mammals from the Albian–Cenomanian (Early–Late Cretaceous) Boundary, Utah , 2004 .

[44]  J. Archibald Dinosaur extinction and the end of an era : what the fossils say , 1996 .

[45]  D. Krause Fossil molar from a Madagascan marsupial , 2001, Nature.

[46]  L. Marshall,et al.  Evolution of the Borhyaenidae, extinct South American predaceous marsupials , 1978 .

[47]  I. Thesleff,et al.  Nonindependence of mammalian dental characters , 2004, Nature.

[48]  Michael Archer,et al.  A Bizarre New Family of Marsupialia (Incertae sedis) from the Early Pliocene of Northeastern Australia: Implications for the Phylogeny of Bunodont Marsupials , 2008, Journal of Paleontology.

[49]  T. E. Macrini,et al.  The anatomy of Herpetotherium cf. fugax COPE, 1873, a metatherian from the Oligocene of North America. , 2008 .

[50]  J. Crochet Diversité systématique des Didelphidae (Marsupialia) européens tertiaires , 1979 .

[51]  M. Norell,et al.  An aberrant island-dwelling theropod dinosaur from the Late Cretaceous of Romania , 2010, Proceedings of the National Academy of Sciences.

[52]  Timothy B. Rowe,et al.  Definition, diagnosis, and origin of Mammalia , 1988 .

[53]  P. Gingerich,et al.  3. Paleocene Biochronology: The Puercan Through Clarkforkian Land Mammal Ages , 2004 .

[54]  J. Storer The mammals of the Gryde Local Fauna, Frenchman Formation (Maastrichtian: Lancian), Saskatchewan , 1991 .

[55]  O. C. Marsh Discovery of Cretaceous Mammalia , 1889, American Journal of Science.

[56]  J. Archibald,et al.  Mammals from the mid-Cretaceous Khodzhakul Formation, Kyzylkum Desert, Uzbekistan , 2005 .

[57]  L. Prendini,et al.  Species or supraspecific taxa as terminals in cladistic analysis? Groundplans versus exemplars revisited. , 2001, Systematic biology.

[58]  R. Cifelli Cretaceous mammals of southern Utah. I. Marsupials from the Kaiparowits Formation (Judithian) , 1990 .

[59]  Kevin de Queiroz,et al.  Phylogeny as a Central Principle in Taxonomy: Phylogenetic Definitions of Taxon Names , 1990 .

[60]  Zhe‐Xi Luo,et al.  The earliest known eutherian mammal , 2002, Nature.

[61]  L. Marshall,et al.  Age and stratigraphic reassessment of the fossil-bearing Laguna Umayo red mudstone unit, SE Peru, from regional stratigraphy, fossil record, and paleomagnetism , 2004 .

[62]  Jeffrey G. Eaton Therian mammals from the Cenomanian (Upper Cretaceous) Dakota Formation, southwestern Utah , 1993 .

[63]  B. Haq,et al.  Chronology of Fluctuating Sea Levels Since the Triassic , 1987, Science.

[64]  M. Sánchez-Villagra,et al.  A morphological analysis of marsupial mammal higher-level phylogenetic relationships , 2003 .

[65]  Ian J. Corfe MAMMALS FROM THE AGE OF DINOSAURS—ORIGINS, EVOLUTION, AND STRUCTURE , 2007 .

[66]  M. Woodburne,et al.  “South American” Marsupials from the Late Cretaceous of North America and the Origin of Marsupial Cohorts , 2005, Journal of Mammalian Evolution.

[67]  G. Simpson THE BEGINNING OF THE AGE OF MAMMALS , 1937 .

[68]  Zhe‐Xi Luo,et al.  An Early Cretaceous Tribosphenic Mammal and Metatherian Evolution , 2003, Science.

[69]  J. Archibald,et al.  New material of the Late Cretaceous deltatheroidan mammal Sulestes from Uzbekistan and phylogenetic reassessment of the metatherian-eutherian dichotomy , 2010 .

[70]  W. Korth Middle Tertiary marsupials (Mammalia) from North America , 1994, Journal of Paleontology.

[71]  R. C. Fox,et al.  Stagodontid marsupials from the Late Cretaceous of Canada and their systematic and functional implications , 2006 .

[72]  Gregory M. Erickson,et al.  A Basal Dromaeosaurid and Size Evolution Preceding Avian Flight , 2007, Science.

[73]  Z. Johanson New marsupial from the Fort Union Formation, Swain Quarry, Wyoming , 1996, Journal of Paleontology.

[74]  W. Clemens Evolution of the mammalian fauna across the Cretaceous-Tertiary boundary in northeastern Montana and other areas of the Western Interior , 2002 .

[75]  A. Schulp,et al.  A New European Marsupial Indicates a Late Cretaceous High-Latitude Transatlantic Dispersal Route , 2005, Journal of Mammalian Evolution.

[76]  C. de Muizon,et al.  Marsupial mammal from the Upper Cretaceous North Horn Formation, Central Utah , 1998, Journal of Paleontology.

[77]  Elisabetta Pierazzo,et al.  The Chicxulub Asteroid Impact and Mass Extinction at the Cretaceous-Paleogene Boundary , 2010, Science.

[78]  Kevin dd Queiroz,et al.  PHYLOGENETIC TAXONOMY * , 2009 .

[79]  S. Brusatte Edinburgh Research Explorer Representing supraspecific taxa in higher-level phylogenetic analyses , 2013 .

[80]  Richard L. Cifelli,et al.  Earliest Evidence of Deltatheroida (Mammalia: Metatheria) from the Early Cretaceous of North America , 2008 .

[81]  L. Russell Tertiary mammals of Saskatchewan. , 1980 .

[82]  C. A. Young Observations on Encke's Comet at the Darmouth College Observatory , 1872, American Journal of Science and Arts.

[83]  Pablo A. Goloboff,et al.  TNT, a free program for phylogenetic analysis , 2008 .

[84]  J. Wiens Can incomplete taxa rescue phylogenetic analyses from long-branch attraction? , 2005, Systematic biology.

[85]  J. Archibald A Study of Mammalia and Geology Across the Cretaceous-Tertiary Boundary in Garfield County, Montana , 1982 .

[86]  J. Wiens,et al.  The accuracy of methods for coding and sampling higher-level taxa for phylogenetic analysis: a simulation study. , 1998, Systematic biology.

[87]  W. Matthew Paleocene Faunas of the San Juan Basin, New Mexico , 1937 .

[88]  R. Cifelli,et al.  Marsupial Origins , 2003, Science.

[89]  M. Novacek,et al.  NEW SPECIMEN OF DELTATHEROIDES CRETACICUS (METATHERIA, DELTATHEROIDA) FROM THE LATE CRETACEOUS OF MONGOLIA , 2004 .

[90]  M. Novacek,et al.  Epipubic bones in eutherian mammals from the Late Cretaceous of Mongolia , 1997, Nature.

[91]  R. Savage Cenozoic Mammals in North America , 1960, Nature.