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The Placental Mammal Ancestor and the Post–K-Pg Radiation of Placentals RESEARCHARTICLE

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The Placental Mammal Ancestor and the Post–K-Pg Radiation of Placentals RESEARCHARTICLE RESEARCH ARTICLE When time-calibrated, this tree indicates that none of the six, very complete Mesozoic fos- sil species (e.g., Ukhaatherium, Maelestes,and The Placental Mammal Ancestor Zalambdalestes) sampled falls within crown clade Placentalia. Instead, these Mesozoic fossils emerge – as nonplacental members of Eutheria or at and the Post K-Pg Radiation lower nodes. This tree suggests that interor- dinal and ordinal diversification occurred within of Placentals the first few hundred thousand years after the K-Pg event, and the first members of mod- Maureen A. O’Leary,1,3¶ Jonathan I. Bloch,2 John J. Flynn,3 Timothy J. Gaudin,4 ern placental orders began appearing 2 to 3 mil- Andres Giallombardo,3 Norberto P. Giannini,5* Suzann L. Goldberg,3 Brian P. Kraatz,3,6 lion years (My) later during the Paleocene. All Zhe-Xi Luo,7† Jin Meng,3 Xijun Ni,3‡ Michael J. Novacek,3 Fernando A. Perini,3|| recent clock-based estimates for the ages of key Zachary S. Randall,2 Guillermo W. Rougier,8 Eric J. Sargis,9 Mary T. Silcox,10 clades, with few exceptions, are substantially Nancy B. Simmons,5 Michelle Spaulding,3,11 Paúl M. Velazco,5 Marcelo Weksler,3§ older than indicated by the fossil record (7, 8, 15). John R. Wible,11 Andrea L. Cirranello1,3 Ghost lineage estimates are minimum divergence dates and may underestimate the timing of ac- tual splits. To discover interordinal relationships of living and fossil placental mammals and the time of We find that only the stem lineage to Plac- origin of placentals relative to the Cretaceous-Paleogene (K-Pg) boundary, we scored 4541 entalia crossed the K-Pg boundary and then spe- phenomic characters de novo for 86 fossil and living species. Combining these data with molecular ciated in the early Paleocene. We estimate that sequences, we obtained a phylogenetic tree that, when calibrated with fossils, shows that the minimum age of the diversification of crown crown clade Placentalia and placental orders originated after the K-Pg boundary. Many nodes Placentalia is just younger than the K-Pg bound- discovered using molecular data are upheld, but phenomic signals overturn molecular signals to ary, or ~36 My younger than molecular clock– show Sundatheria (Dermoptera + Scandentia) as the sister taxon of Primates, a close link based mean estimates derived from supertree between Proboscidea (elephants) and Sirenia (sea cows), and the monophyly of echolocating (15) and supermatrix (7) analyses. We do not Chiroptera (bats). Our tree suggests that Placentalia first split into Xenarthra and Epitheria; find support for the hypothesis that 29 to 39 extinct New World species are the oldest members of Afrotheria. (7, 15) mammalian lineages, including Afrothe- ria, Rodentia, Primates, Lipotyphla, Xenarthra, t is disputed whether orders of placental tion of Placentalia after the K-Pg extinction 1Department of Anatomical Sciences, School of Medicine, HSC mammals, the very diverse group of spe- event (11). T-8 (040), Stony Brook University, Stony Brook, NY 11794– cies that includes humans, evolved before Determining placental origins and relation- 8081, USA. 2Florida Museum of Natural History, University of I – 3 or after the significant extinction horizon known ships has met with the practical challenge of Florida, Gainesville, FL 32611 7800, USA. Division of Paleon- tology, American Museum of Natural History, 79th Street and as the Cretaceous-Paleogene (K-Pg) event 66 codifying phenomic data on a scale compara- Central Park West, New York, NY 10024–5192, USA. 4Depart- to 65 million years ago (Ma) (1, 2). Different ble to that for genomic data to produce a max- ment of Biological and Environmental Sciences, University of models have been proposed to describe ordinal- imally informed phylogenetic tree. We built a Tennessee at Chattanooga, 615 McCallie Avenue, Chattanooga, level diversification either before (short-fuse mod- phenomic character matrix (4541 characters; TN 37403–2598, USA. 5Department of Mammalogy, American el), near (long-fuse model), or after (explosive 403 constant and 482 parsimony uninformative) Museum of Natural History, 79th Street and Central Park West, New York, NY 10024–5192, USA. 6Western University of model) this boundary (3). The ~5100 living pla- using MorphoBank (12). The matrix contains Health Sciences, Department of Anatomy, Pomona, CA 91766– cental species collectively exhibit extreme size newly scored characters for 86 species repre- 1854, USA. 7Section of Vertebrate Paleontology, Carnegie ranges (1.5-g bumblebee bat to 190,000-kg blue senting all living placental orders plus 40 fossil Museum of Natural History, 4400 Forbes Avenue, Pittsburgh, – 8 whale); dramatic locomotor diversity (e.g., run- species, with more than 12,000 annotated im- PA 15213 4080, USA. Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY 40292, ning, flying, and swimming); and diverse de- ages supporting the phenomic homologies. These USA. 9Department of Anthropology, Yale University, Post Office grees of encephalization (4). Moreover, extinct data were examined with molecular sequences Box 208277, New Haven, CT 06520–8277, USA. 10Department species in the placental fossil record are even compiled from 27 nuclear genes from GenBank of Anthropology, University of Toronto Scarborough, 1265 11 more numerous and exhibit a broader range of (table S1). Military Trail, Scarborough, Ontario M1C 1A4, Canada. Sec- tion of Mammals, Carnegie Museum of Natural History, 5800 adaptations (5). Given this diversity, it is of in- Placental orders originated after the K-Pg Baum Boulevard, Pittsburgh, PA 15206, USA. terest to determine the phenotype of the ances- boundary. A single tree emerged from our com- *Present address: Consejo Nacional de Investigaciones tral placental mammal. bined phenomic-molecular parsimony analy- Científicas y Tecnológicas, Facultad de Ciencias Naturales The hypothesis that the oldest members of sis (Fig. 1; hereafter, “combined tree”); we also e Instituto Miguel Lillo, Universidad Nacional de Tucumán, crown Placentalia [the clade of all living pla- performed extensive sensitivity analyses using Miguel Lillo 205, Código Postal 4000, Tucumán, Argentina. † cental mammals (6)] were present by ~100 Ma other tree-searching methods (13). We applied Present address: Department of Organismal Biology and Anatomy, University of Chicago, 1027 East 57th Street, in the Mesozoic Era has been supported by mo- multiple fossil ages for the oldest members of Chicago, IL 60637, USA. lecular clock analyses (7–9), which suggest that the clades sampled and ghost lineage analysis ‡Present address: Institute of Vertebrate Paleontology and at least 29 mammalian lineages (7), including (14) to this tree to determine minimum diver- Paleoanthropology, Chinese Academy of Sciences, 142 Xi-Zhi- the stem lineages of Primates and Rodentia, gence dates using fossils alone (13). Results sup- Men-Wai Street, Beijing, 100044, P. R. China. §Present address: Department of Vertebrates, Museu Nacional, appeared in Late Cretaceous ecosystems (8) port the monophyly of most traditional orders Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ and survived the massive K-Pg extinction event. originally identified on the basis of phenotypes, 20940-040, Brazil. However, fossil evidence has not corroborated as well as interordinal groupings discovered Present address: Department of Zoology, Instituto de Ciências this hypothesis, despite discovery of abundant, using molecular sequence data (Fig. 1 and Table Biológicas, Universidade Federal de Minas Gerais, Avenida Antônio Carlos 6627, Belo Horizonte, Minas Gerais 31270- well-preserved, small vertebrates (10). By con- 1). Twenty nodes (over 40%) are congruent in 901, Brazil. trast, phenomic phylogenies incorporating fossils partitioned molecular and phenomic analyses ¶To whom correspondence should be addressed. E-mail: have placed ordinal and intraordinal specia- (fig. S2). [email protected] EMBARGOED UNTIL 2PM U.S. EASTERN TIME ON THE THURSDAY BEFORE THIS DATE: 662 8 FEBRUARY 2013 VOL 339 SCIENCE www.sciencemag.org RESEARCH ARTICLE Fig. 1. Single tree from parsimony analysis of combined molecular and pear: the oldest hypothesized member of the crown clade (the younger date) phenomic data mapped onto the stratigraphic record (tables S2 and S3). and the oldest hypothesized taxon on the stem to the crown clade (the older Crown clade Placentalia diversified after the K-Pg boundary with only the stem date). Crown clades (except Eutheria and Metatheria) are defined (table S4). lineage to Placentalia crossing the boundary. Black boxes indicate fossil taxa Space immediately younger than 65 Ma not to scale showing early Paleo- hypothesized to be on lineages; black lines indicate stratigraphic ranges; cene interordinal diversification of Placentalia. Crown clades Marsupialia and ranges and ghost lineages (orange) provide minimum divergence dates. When Monotremata also diversified post K-Pg boundary. Bremer support (BS) the matrix includes only one terminal taxon of a crown order, two boxes ap- (tableS8)abovenodes,jackknifevaluesbelownodes. EMBARGOED UNTIL 2PM U.S. EASTERN TIME ON THE THURSDAY BEFORE THIS DATE: www.sciencemag.org SCIENCE VOL 339 8 FEBRUARY 2013 663 RESEARCH ARTICLE Table 1. Comparison of divergence datesformammalianclades(ta- trated in Fig. 1; date calculations are described in (14). Names listed bles S2 and S3) between our combined data analysis, a combined data specify crown clades (table S4); older dates in (7, 15)arenegative
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