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Proc Natl Acad Sci U S A. 2017 Aug 29;114(35):E7282-E7290. doi: 10.1073/pnas.1616744114. Epub 2017 Aug 14.

Genomic evidence reveals a radiation of placental mammals uninterrupted by the KPg boundary.

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Jiangsu Key Laboratory of Phylogenomics and Comparative Genomics, School of Life Sciences, Jiangsu Normal University, Xuzhou 221116, Jiangsu, China.
Department of Statistics & Institute of Bioinformatics, University of Georgia, Athens, GA 30606.
Key Laboratory of High Performance Computing and Stochastic Information Processing of the Ministry of Education of China, Department of Computer Science, College of Mathematics and Computer Science, Hunan Normal University, Changsha, Hunan 410081, China.
Department of Biological Sciences, National University of Singapore, Singapore 117543.
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
State Key Laboratory of Reproductive Biology & Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
Key Laboratory of Vertebrate Evolution and Human Origins of the Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China.
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China.
Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton CB10 1SA, United Kingdom.
Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Key Laboratory of Integrated Pest Management in Agriculture, Guangdong Institute of Applied Biological Resources, Guangzhou 510260, China.
Jiangsu Key Laboratory of Phylogenomics and Comparative Genomics, School of Life Sciences, Jiangsu Normal University, Xuzhou 221116, Jiangsu, China;
Department of Organismic and Evolutionary Biology & Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138.
Division of Paleontology, American Museum of Natural History, New York, NY 10024.
Department of Biochemistry and Molecular Biology, 2011 Collaborative Innovation Center of Tianjin for Medical Epigenetics, Tianjin Key Laboratory of Medical Epigenetics, School of Basic Medical Sciences, Tianjin Medical University, Tianjin 300070, China.


The timing of the diversification of placental mammals relative to the Cretaceous-Paleogene (KPg) boundary mass extinction remains highly controversial. In particular, there have been seemingly irreconcilable differences in the dating of the early placental radiation not only between fossil-based and molecular datasets but also among molecular datasets. To help resolve this discrepancy, we performed genome-scale analyses using 4,388 loci from 90 taxa, including representatives of all extant placental orders and transcriptome data from flying lemurs (Dermoptera) and pangolins (Pholidota). Depending on the gene partitioning scheme, molecular clock model, and genic deviation from molecular clock assumptions, extensive sensitivity analyses recovered widely varying diversification scenarios for placental mammals from a given gene set, ranging from a deep Cretaceous origin and diversification to a scenario spanning the KPg boundary, suggesting that the use of suboptimal molecular clock markers and methodologies is a major cause of controversies regarding placental diversification timing. We demonstrate that reconciliation between molecular and paleontological estimates of placental divergence times can be achieved using the appropriate clock model and gene partitioning scheme while accounting for the degree to which individual genes violate molecular clock assumptions. A birth-death-shift analysis suggests that placental mammals underwent a continuous radiation across the KPg boundary without apparent interruption by the mass extinction, paralleling a genus-level radiation of multituberculates and ecomorphological diversification of both multituberculates and therians. These findings suggest that the KPg catastrophe evidently played a limited role in placental diversification, which, instead, was likely a delayed response to the slightly earlier radiation of angiosperms.


data partitioning; molecular clock; placental diversification timing; species tree estimation; trans-KPg model

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