Early penguin fossils, plus mitochondrial genomes, calibrate avian evolution.

Testing models of macroevolution, and especially the sufficiency of microevolutionary processes, requires good collaboration between molecular biologists and paleontologists. We report such a test for events around the Late Cretaceous by describing the earliest penguin fossils, analyzing complete mitochondrial genomes from an albatross, a petrel, and a loon, and describe the gradual decline of pterosaurs at the same time modern birds radiate. The penguin fossils comprise four naturally associated skeletons from the New Zealand Waipara Greensand, a Paleocene (early Tertiary) formation just above a well-known Cretaceous/Tertiary boundary site. The fossils, in a new genus (Waimanu), provide a lower estimate of 61-62 Ma for the divergence between penguins and other birds and thus establish a reliable calibration point for avian evolution. Combining fossil calibration points, DNA sequences, maximum likelihood, and Bayesian analysis, the penguin calibrations imply a radiation of modern (crown group) birds in the Late Cretaceous. This includes a conservative estimate that modern sea and shorebird lineages diverged at least by the Late Cretaceous about 74 +/- 3 Ma (Campanian). It is clear that modern birds from at least the latest Cretaceous lived at the same time as archaic birds including Hesperornis, Ichthyornis, and the diverse Enantiornithiformes. Pterosaurs, which also coexisted with early crown birds, show notable changes through the Late Cretaceous. There was a decrease in taxonomic diversity, and small- to medium-sized species disappeared well before the end of the Cretaceous. A simple reading of the fossil record might suggest competitive interactions with birds, but much more needs to be understood about pterosaur life histories. Additional fossils and molecular data are still required to help understand the role of biotic interactions in the evolution of Late Cretaceous birds and thus to test that the mechanisms of microevolution are sufficient to explain macroevolution.

[1]  A. Averianov.  Evolution and Palaeobiology of Pterosaurs, ed. by E. Buffetaut and J.-M. Mazin. Geol. Soc. Spec. Publ., no. 217, 1–347 (2003) , 2006 .

[2]  Gradstein,et al.  The New Zealand Geological Timescale , 2006 .

[3]  A. Baker,et al.  Multiple gene evidence for expansion of extant penguins out of Antarctica due to global cooling , 2006, Proceedings of the Royal Society B: Biological Sciences.

[4]  Zhonghe Zhou,et al.  Pterosaur diversity and faunal turnover in Cretaceous terrestrial ecosystems in China , 2005, Nature.

[5]  S. Peters.  Geologic constraints on the macroevolutionary history of marine animals. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Kate E. Jones,et al.  Multiple Causes of High Extinction Risk in Large Mammal Species , 2005, Science.

[7]  R. Nudds,et al.  The quality of the fossil record of Mesozoic birds , 2005, Proceedings of the Royal Society B: Biological Sciences.

[8]  D. Erwin,et al.  Abrupt and Gradual Extinction Among Late Permian Land Vertebrates in the Karoo Basin, South Africa , 2005, Science.

[9]  R. Ketcham,et al.  Definitive fossil evidence for the extant avian radiation in the Cretaceous , 2005, Nature.

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

[11]  D. Penny,et al.  The rise of birds and mammals: are microevolutionary processes sufficient for macroevolution? , 2004, Trends in ecology & evolution.

[12]  Zhonghe Zhou.  The origin and early evolution of birds: discoveries, disputes, and perspectives from fossil evidence , 2004, Naturwissenschaften.

[13]  G. Dyke,et al.  The evolutionary radiation of modern birds (Neornithes): reconciling molecules, morphology and the fossil record , 2004 .

[14]  D. Penny,et al.  Four new avian mitochondrial genomes help get to basic evolutionary questions in the late cretaceous. , 2004, Molecular biology and evolution.

[15]  D. Robertson,et al.  Survival in the first hours of the Cenozoic , 2004 .

[16]  J. Clarke,et al.  MORPHOLOGY, PHYLOGENETIC TAXONOMY, AND SYSTEMATICS OF ICHTHYORNIS AND APATORNIS (AVIALAE: ORNITHURAE) , 2004 .

[17]  G. Mayr,et al.  The deep divergences of neornithine birds: a phylogenetic analysis of morphological characters , 2003, Cladistics : the international journal of the Willi Hennig Society.

[18]  D. Steadman.  Mesozoic Birds: Above the Heads of Dinosaurs , 2003 .

[19]  D. Penny,et al.  Comment on "Hexapod Origins: Monophyletic or Paraphyletic?" , 2003, Science.

[20]  D. Penny,et al.  The root of the mammalian tree inferred from whole mitochondrial genomes. , 2003, Molecular phylogenetics and evolution.

[21]  H. Chang,et al.  Age of the pterosaur and web‐footed bird tracks associated with dinosaur footprints from South Korea , 2003 .

[22]  S. W. Wise,et al.  Paleocene–Eocene Nannofossil Biostratigraphy of ODP Leg 183, Kerguelen Plateau , 2003 .

[23]  C. Hollis,et al.  Biostratigraphic review of the Cretaceous/Tertiary boundary transition, mid‐Waipara River section, North Canterbury, New Zealand , 2003 .

[24]  A. Feduccia.  ‘Big bang’ for tertiary birds? , 2003 .

[25]  J. Boore,et al.  Hexapod Origins: Monophyletic or Paraphyletic? , 2003, Science.

[26]  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.

[27]  D. Penny,et al.  Two new avian mitochondrial genomes (penguin and goose) and a summary of bird and reptile mitogenomic features. , 2003, Gene.

[28]  J. Clarke,et al.  Description of the Earliest Fossil Penguin from South America and First Paleogene Vertebrate Locality of Tierra Del Fuego, Argentina , 2003 .

[29]  Chang Meemann.  The Jehol Biota: the emergence of feathered dinosaurs, beaked birds and flowering plants , 2003 .

[30]  E. Buffetaut,et al.  Evolution and palaeobiology of pterosaurs , 2003, Geological Society, London, Special Publications.

[31]  D. Unwin.  On the phylogeny and evolutionary history of pterosaurs , 2003, Geological Society, London, Special Publications.

[32]  G. Dyke,et al.  A New Presbyornithid Bird (Aves, Anseriformes) from the Late Cretaceous of Southern Mongolia , 2002 .

[33]  M. Norell,et al.  The Morphology and Phylogenetic Position of Apsaravis ukhaana from the Late Cretaceous of Mongolia , 2002 .

[34]  David Penny,et al.  Four new mitochondrial genomes and the increased stability of evolutionary trees of mammals from improved taxon sampling. , 2002, Molecular biology and evolution.

[35]  C. Johnson,et al.  Determinants of loss of mammal species during the Late Quaternary ‘megafauna’ extinctions: life history and ecology, but not body size , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[36]  S. Olson.  New Perspectives on the Origin and Early Evolution of Birds. Proceedings of the International Symposium in Honor of John H. Ostrom , 2002 .

[37]  Hirohisa Kishino,et al.  Divergence time and evolutionary rate estimation with multilocus data. , 2002, Systematic biology.

[38]  Andrew M. Simons,et al.  The continuity of microevolution and macroevolution , 2002 .

[39]  G. Dyke,et al.  Europe's last Mesozoic bird , 2002, Naturwissenschaften.

[40]  G. Dyke,et al.  THE MESOZOIC RADIATION OF BIRDS , 2002 .

[41]  T. Paton,et al.  Complete mitochondrial DNA genome sequences show that modern birds are not descended from transitional shorebirds , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[42]  G. Dyke,et al.  The Fossil Galliform Bird Paraortygoides from the Lower Eocene of the United Kingdom , 2002 .

[43]  M. Lockley,et al.  New pterosaur tracks (Pteraichnidae) from the Late Cretaceous Uhangri Formation, southwestern Korea , 2001, Geological Magazine.

[44]  P. Jadwiszczak,et al.  Taxonomic revision of Eocene Antarctic penguins based on tarsometatarsal morphology , 2002 .

[45]  L. Witmer,et al.  Mesozoic Birds: Above the Heads of Dinosaurs , 2002 .

[46]  J. Raine,et al.  Indication of Global Deforestation at the Cretaceous-Tertiary Boundary by New Zealand Fern Spike , 2001, Science.

[47]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[48]  J. Cracraft.  Avian evolution, Gondwana biogeography and the Cretaceous–Tertiary mass extinction event , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[49]  S. Hedges,et al.  Calibration of avian molecular clocks. , 2001, Molecular biology and evolution.

[50]  M. Norell,et al.  Fossil that fills a critical gap in avian evolution , 2001, Nature.

[51]  B. Livezey,et al.  Higher-Order Phylogenetics of Modern Aves Based On Comparative Anatomy , 2001 .

[52]  G. Paul,et al.  AN AVIAN QUADRATE FROM THE LATE CRETACEOUS LANCE FORMATION OF WYOMING , 2001 .

[53]  M. Hendy,et al.  Can fast early rates reconcile molecular dates with the Cambrian explosion? , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[54]  R. Holdaway,et al.  Rapid extinction of the moas (Aves: Dinornithiformes): model, test, and implications. , 2000, Science.

[55]  P. Wagner.  The quality of the fossil record and the accuracy of phylogenetic inferences about sampling and diversity. , 2000, Systematic biology.

[56]  L. Hills,et al.  Hesperornis (Aves) from Ellesmere Island and palynological correlation of known Canadian localities , 1999 .

[57]  J. Sepkoski,et al.  Evolutionary and preservational constraints on origins of biologic groups: divergence times of eutherian mammals. , 1999, Science.

[58]  M. Lockley.  The vertebrate track record , 1998, Nature.

[59]  S. Morris.  Early Metazoan Evolution: Reconciling Paleontology and Molecular Biology' , 1998 .

[60]  A. Chinsamy,et al.  Bone microstructure of the divingHesperornisand the voltantIchthyornisfrom the Niobrara Chalk of western Kansas , 1998 .

[61]  R. Bleiweiss.  Fossil gap analysis supports early Tertiary origin of trophically diverse avian orders , 1998 .

[62]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[63]  A. Härlid,et al.  The mtDNA sequence of the ostrich and the divergence between paleognathous and neognathous birds. , 1997, Molecular biology and evolution.

[64]  D Penny,et al.  Mass Survival of Birds Across the Cretaceous- Tertiary Boundary: Molecular Evidence , 1997, Science.

[65]  S. Olson,et al.  A new genus and two new species of gigantic Plotopteridae from Japan (Aves: Pelecaniformes) , 1996 .

[66]  S. Bennett.  Year-classes of pterosaurs from the Solnhofen Limestone of Germany: taxonomic and systematic implications , 1996 .

[67]  Sudhir Kumar,et al.  Continental breakup and the ordinal diversification of birds and mammals , 1996, Nature.

[68]  A. Feduccia.  The origin and evolution of birds , 1996 .

[69]  L. Chiappe,et al.  The first 85 million years of avian evolution , 1995, Nature.

[70]  Jon E. Ahlquist,et al.  Phylogeny and Classification of the Birds: A Study in Molecular Evolution , 1991 .

[71]  Peter Wellnhofer,et al.  The illustrated encyclopedia of pterosaurs , 1991 .

[72]  R. Fordyce,et al.  18 – Penguin History and New Fossil Material from New Zealand , 1990 .

[73]  G. Larwood.  Extinction and survival in the fossil record , 1988 .

[74]  J. Cracraft.  The origin and early diversification of birds , 1986, Paleobiology.

[75]  Michael J. Benton,et al.  The phylogeny and classification of tetrapods , 1986 .

[76]  R. C. Fox.  Ichthyornis (Aves) from the early Turonian (Late Cretaceous) of Alberta , 1984 .

[77]  J. Stewart,et al.  An ichthyornithiform bird from the Campanian of Canada , 1982 .

[78]  L. W. Alvarez,et al.  Extraterrestrial Cause for the Cretaceous-Tertiary Extinction , 1980, Science.

[79]  S. Olson.  A new genus of penguin-like pelecaniform bird from the Oligocene of Washington (Pelecaniformes: Plotopteridae) , 1980, Contributions in science.

[80]  S. Olson,et al.  Fossil Counterparts of Giant Penguins from the North Pacific , 1979, Science.

[81]  M. Harris,et al.  The Biology of Penguins , 1976 .

[82]  H. Howard.  A review of the extinct avian genus, Mancalla , 1970, Contributions in science.

[83]  H. Howard.  A possible ancestor of the Lucus Auk (family Mancallidae) from the Tertiary of Orange County, California , 1966, Contributions in science.

[84]  Robert W. Wilson.  Some tertiary mammals and birds from North America , 1949 .