Assessing the Cretaceous superordinal divergence times within birds and placental mammals by using whole mitochondrial protein sequences and an extended statistical framework.

Using the set of all vertebrate mtDNA protein sequences published as of May 1998, plus unpublished examples for elephant and birds, we examined divergence times in Placentalia and Aves. Using a parsimony-based test, we identified a subset of slower evolutionary rate placental sequences that do not appear to violate the clock assumption. Analyzing just these sequences decreases support for Marsupionta and the carnivore + perissodactyl group but increases support for armadillo diverging earlier than rabbit (which may represent the whole Glires group). A major theme of the paper is to use more comprehensive estimates of divergence time standard error (SE). From the well-studied horse/rhino split, estimated to be 55 million years before present (mybp), the splitting time within carnivores is confidently shown to be older than 50 million years. Some of our estimates of divergence times within placentals are relatively old, at up to 169 million years, but are within 2 SE of other published estimates. The whale/cow split at 65 mybp may be older than commonly assumed. All the sampled splits between the main groups of fereuungulates (the clade of carnivores, cetartiodactyls, perissodactyls, and pholidotes) seem to be distinctly before the Cretaceous/Tertiary boundary. Analyses suggest a close relationship between elephants (representing Afrotheria) and armadillos (Xenarthra), and our timing of this splitting is coincident with the opening of the South Atlantic, a major vicariant event. Recalibrating with this event (at 100 mybp), we obtain younger estimates for the earliest splits among placentals. Divergence times within birds are also assessed by using previously unpublished sequences. We fail to reject a clock for all bird taxa available. Unfortunately, available deep calibration points for birds are questionable, so a new calibration based on the age of the Anseriform stem lineage is estimated. The divergence time of rhea and ostrich may be much more recent than commonly assumed, while that of passerines may be older. Our major concern is the rooting point of the bird subtree, as the nearest outgroup (alligator) is very distant.

[1]  M. Milinkovitch,et al.  Stability of cladistic relationships between Cetacea and higher-level artiodactyl taxa. , 1999, Systematic biology.

[2]  D. Mindell,et al.  Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. , 1999, Molecular phylogenetics and evolution.

[3]  Ziheng Yang,et al.  PAML: a program package for phylogenetic analysis by maximum likelihood , 1997, Comput. Appl. Biosci..

[4]  D Penny,et al.  Hadamard conjugations and modeling sequence evolution with unequal rates across sites. , 1997, Molecular phylogenetics and evolution.

[5]  N. M. Brooke,et al.  A molecular timescale for vertebrate evolution , 1998, Nature.

[6]  P. Tassy,et al.  The Proboscidea : evolution and palaeoecology of elephants and their relatives , 1996 .

[7]  J. Cracraft,et al.  CHAPTER 7 – The Phylogeny of Ratite Birds: Resolving Conflicts between Molecular and Morphological Data Sets , 1997 .

[8]  A. Janke,et al.  The complete mitochondrial genome of Alligator mississippiensis and the separation between recent archosauria (birds and crocodiles). , 1997, Molecular biology and evolution.

[9]  Diana J. Kao,et al.  Molecular evidence for multiple origins of Insectivora and for a new order of endemic African insectivore mammals. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Archibald Fossil Evidence for a Late Cretaceous Origin of “Hoofed” Mammals , 1996, Science.

[11]  J. J. Flynn,et al.  Phylogeny of early Tertiary Carnivora : with a description of a new species of Protictis from the Middle Eocene of northwestern Wyoming. American Museum novitates ; no. 2725 , 1982 .

[12]  Robert L. Carroll,et al.  Vertebrate Paleontology and Evolution , 1988 .

[13]  S E Stanley,et al.  Body size effects and rates of cytochrome b evolution in tube-nosed seabirds. , 1998, Molecular biology and evolution.

[14]  A. Härlid,et al.  The Complete Mitochondrial Genome of Rhea americana and Early Avian Divergences , 1998, Journal of Molecular Evolution.

[15]  George Gaylord Simpson,et al.  Classification of mammals : above the species level , 1997 .

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

[17]  F. Tajima,et al.  Simple methods for testing the molecular evolutionary clock hypothesis. , 1993, Genetics.

[18]  J. Hartigan,et al.  Asynchronous distance between homologous DNA sequences. , 1987, Biometrics.

[19]  H. Kishino,et al.  Estimation of branching dates among primates by molecular clocks of nuclear DNA which slowed down in Hominoidea , 1989 .

[20]  Michael J. Sanderson,et al.  A Nonparametric Approach to Estimating Divergence Times in the Absence of Rate Constancy , 1997 .

[21]  H Kishino,et al.  Converting distance to time: application to human evolution. , 1990, Methods in enzymology.

[22]  P J Waddell,et al.  Using novel phylogenetic methods to evaluate mammalian mtDNA, including amino acid-invariant sites-LogDet plus site stripping, to detect internal conflicts in the data, with special reference to the positions of hedgehog, armadillo, and elephant. , 1999, Systematic biology.

[23]  R. Hudson Gene genealogies and the coalescent process. , 1990 .

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

[25]  M. Nishida,et al.  The complete nucleotide sequence of a snake (Dinodon semicarinatus) mitochondrial genome with two identical control regions. , 1998, Genetics.

[26]  S. Pääbo,et al.  Conflict Among Individual Mitochondrial Proteins in Resolving the Phylogeny of Eutherian Orders , 1998, Journal of Molecular Evolution.

[27]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[28]  B. Livezey A phylogenetic analysis of basal Anseriformes, the fossil Presbyornis, and the interordinal relationships of waterfowl , 1997 .

[29]  D. Mindell,et al.  Slow Rates of Molecular Evolution in Birds and the Metabolic Rate and Body Temperature Hypotheses , 1996 .

[30]  R. Bleiweiss Relative-Rate Tests and Biological Causes of Molecular Evolution in Hummingbirds , 1998 .

[31]  M. Steel,et al.  General time-reversible distances with unequal rates across sites: mixing gamma and inverse Gaussian distributions with invariant sites. , 1997, Molecular phylogenetics and evolution.

[32]  S. Olson A Giant Presbyornis (Aves, Anseriformes) And Other Birds From The Paleocene Aquia Formation Of Maryland And Virginia , 1994 .

[33]  B. Funnell,et al.  Atlas of Mesozoic and Cenozoic Coastlines , 1994 .

[34]  P. Waddell,et al.  Towards resolving the interordinal relationships of placental mammals. , 1999, Systematic biology.

[35]  M. Steel,et al.  Recovering evolutionary trees under a more realistic model of sequence evolution. , 1994, Molecular biology and evolution.

[36]  A. Cooper CHAPTER 13 – Studies of Avian Ancient DNA: From Jurassic Park to Modern Island Extinctions , 1997 .

[37]  Peter J. Waddell,et al.  Statistical methods of phylogenetic analysis : including Hadamard conjugations, LogDet transforms and maximum likelihood : a thesis presented in partial fulfilment of the requirements for the degree of Ph.D. in Biology at Massey University , 1995 .

[38]  David P. Mindell,et al.  Ribosomal RNA in Vertebrates: Evolution and Phylogenetic Applications , 1990 .

[39]  M. Hasegawa,et al.  Interordinal relationships of birds and other reptiles based on whole mitochondrial genomes. , 1999, Systematic biology.

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

[41]  J. Felsenstein,et al.  A simulation comparison of phylogeny algorithms under equal and unequal evolutionary rates. , 1994, Molecular biology and evolution.

[42]  Ú. Árnason,et al.  Cytochrome b nucleotide sequences and the identification of five primary lineages of extant cetaceans. , 1996, Molecular biology and evolution.

[43]  P. Waddell,et al.  The complete mitochondrial DNA sequence of the shark Mustelus manazo: evaluating rooting contradictions to living bony vertebrates. , 1998, Molecular biology and evolution.