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Genomic Evidence Reveals a Radiation of Placental Mammals Uninterrupted

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Genomic Evidence Reveals a Radiation of Placental Mammals Uninterrupted Genomic evidence reveals a radiation of placental PNAS PLUS mammals uninterrupted by the KPg boundary Liang Liua,b,1, Jin Zhangc,1, Frank E. Rheindtd,1, Fumin Leie, Yanhua Que, Yu Wangf, Yu Zhangf, Corwin Sullivang, Wenhui Nieh, Jinhuan Wangh, Fengtang Yangi, Jinping Chenj, Scott V. Edwardsa,k,2, Jin Mengl, and Shaoyuan Wua,m,2 aJiangsu Key Laboratory of Phylogenomics and Comparative Genomics, School of Life Sciences, Jiangsu Normal University, Xuzhou 221116, Jiangsu, China; bDepartment of Statistics & Institute of Bioinformatics, University of Georgia, Athens, GA 30606; cKey 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; dDepartment of Biological Sciences, National University of Singapore, Singapore 117543; eKey Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; fState Key Laboratory of Reproductive Biology & Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; gKey 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; hState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China; iWellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton CB10 1SA, United Kingdom; jGuangdong 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; kDepartment of Organismic and Evolutionary Biology & Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138; lDivision of Paleontology, American Museum of Natural History, New York, NY 10024; and mDepartment 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 Contributed by Scott V. Edwards, June 3, 2017 (sent for review October 17, 2016; reviewed by Zhe-Xi Luo, William J. Murphy, and Nicolas Salamin) The timing of the diversification of placental mammals relative to shortly after the KPg boundary (13). By contrast, the long-fuse the Cretaceous–Paleogene (KPg) boundary mass extinction remains model posits a Cretaceous origin of Placentalia with intraordinal highly controversial. In particular, there have been seemingly irrec- diversification shortly after the KPg boundary, and the short-fuse oncilable differences in the dating of the early placental radiation not model places the origin and intraordinal diversification of Pla- only between fossil-based and molecular datasets but also among centalia in the Cretaceous (13). Paleontological evidence supports EVOLUTION molecular datasets. To help resolve this discrepancy, we performed the explosive model, because all modern lineages of crown-group genome-scale analyses using 4,388 loci from 90 taxa, including rep- placentals first appear in the fossil record after the KPg boundary resentatives of all extant placental orders and transcriptome data (15, 16). Molecular analyses, in contrast, provide almost unani- from flying lemurs (Dermoptera) and pangolins (Pholidota). Depend- ing on the gene partitioning scheme, molecular clock model, and mous support for a pre-KPg origin of Placentalia, although they genic deviation from molecular clock assumptions, extensive sensi- disagree on the timing of intraordinal diversification relative to the tivity analyses recovered widely varying diversification scenarios for KPg boundary (3, 5, 8–10). The resolution of the discrepancy placental mammals from a given gene set, ranging from a deep between molecular and fossil evidence has remained one of the Cretaceous origin and diversification to a scenario spanning the most crucial issues in mammalian evolutionary research, because KPg boundary, suggesting that the use of suboptimal molecular clock markers and methodologies is a major cause of controversies regard- Significance ing placental diversification timing. We demonstrate that reconcilia- tion between molecular and paleontological estimates of placental We produced a genome-scale dataset from representatives of all divergence times can be achieved using the appropriate clock model placental mammal orders to infer diversification timing relative and gene partitioning scheme while accounting for the degree to to the Cretaceous–Paleogene (KPg) boundary. Our sensitivity which individual genes violate molecular clock assumptions. A analyses show that divergence time estimates within placentals birth-death-shift analysis suggests that placental mammals under- are considerably biased by the specific way in which a given went a continuous radiation across the KPg boundary without ap- dataset is processed. We examined the performance of various parent interruption by the mass extinction, paralleling a genus-level dating approaches using a comprehensive scheme of likelihood radiation of multituberculates and ecomorphological diversification analyses and computational simulations, allowing us to identify of both multituberculates and therians. These findings suggest that the optimal molecular clock parameters, gene sets, and gene the KPg catastrophe evidently played a limited role in placental di- partitioning schemes for reliable dating. Based on the optimal versification, which, instead, was likely a delayed response to the methodology, we present a hypothesis of mammalian divergence slightly earlier radiation of angiosperms. timing that is more consistent with the fossil record than previous molecular clock reconstructions, suggesting that placental mam- molecular clock | data partitioning | species tree estimation | mals underwent a continuous radiation across the KPg boundary. placental diversification timing | trans-KPg model Author contributions: L.L., S.V.E., and S.W. designed research; L.L., F.E.R., C.S., S.V.E., J.M., ammalian evolution has been intensively studied and is and S.W. performed research; L.L., J.Z., F.E.R., and S.W. analyzed data; F.L., Y.Q., Y.W., Y.Z., W.N., J.W., F.Y., and J.C. contributed new reagents/analytic tools; S.W. wrote Mrelatively well understood compared with the evolution of the paper; and L.L., F.E.R., S.V.E., and J.M. contributed to the writing and discussion. – other animal clades (1 6). Despite significant recent progress, Reviewers: Z.-X.L., The University of Chicago; W.J.M., Texas A&M University; and N.S., however, fundamental aspects of the pattern and timing of mam- University of Lausanne. malian diversification remain vigorously debated (1–7). One highly The authors declare no conflict of interest. controversial issue is whether the diversification of placental Data deposition: The sequence reported in this paper has been deposited in the DRYAD mammals took place before or after the Cretaceous–Paleogene database (accession no. 10.5061/dryad.bp462), and the RNA-seq raw data of pangolin and flying lemur were deposited in GenBank (accession nos. SRX3014245 and SRX3014246). (KPg) boundary (∼66 Ma), which marked the extinction of 1L.L., J.Z., and F.E.R. contributed equally to this work. nonavian dinosaurs and many other Mesozoic vertebrates (8–16). 2To whom correspondence may be addressed. Email: [email protected] or Three main models have been proposed to characterize the evo- [email protected]. lutionary history of placental crown groups. The explosive model This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. puts both the origin and intraordinal diversification of Placentalia 1073/pnas.1616744114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1616744114 PNAS Early Edition | 1of9 Downloaded by guest on September 26, 2021 the severity of the end-Cretaceous mass extinction implies that embedded within them [bootstrap percentage (BP) = 100; SI Ap- pre-KPg and post-KPg diversification events would have taken pendix,Figs.S3andS4]. place in radically different ecological contexts. The concatenation trees, by contrast, differ substantially from Successful molecular dating of divergence events depends on each other and from the coalescence trees. In concatenation trees, various factors, the most critical of which are a rigorous set of fossil tenrecs are consistently placed as sister to golden moles (BP = calibration points, a reliable phylogenetic topology, and rigorous 100), while the aardvark is placed basally within Afroinsectiphilia application of molecular clock methodologies (17, 18). However, (BP = 100; SI Appendix, Figs. S5 and S6). Hyraxes and elephants fossil calibrations used previously have varied in both number and are sister taxa in the concatenation trees (BP = 100 for C12, BP = quality (19, 20), and several important features of the mammalian 99 for CDS, and BP = 70 for C3), whereas elephants and sirenians phylogenetic tree remain unresolved despite considerable recent are sister taxa in the coalescence trees (BP = 100; SI Appendix, effort (1–4, 21–26). In addition, there has been limited assessment Figs. S3–S6). The C12 and CDS concatenation trees recover of the impact of different analytical parameters and clock models
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