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      Earth history and the passerine superradiation

      a , 1 , b , c , d , e , f , g , h , i , j , k , l , m , n , o , p , q , r , s , t , u , a , v , w , x , y , m , z , aa , bb , aa , q , cc , dd , p , ee , ff , gg , gg , a , v , u , m , q , r , gg , a , v , 1

      Proceedings of the National Academy of Sciences of the United States of America

      National Academy of Sciences

      Passeriformes, diversification, macroevolution, climate, biogeography

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          Significance

          Our understanding of the factors that affected the diversification of passerines, the most diverse and widespread bird order (Passeriformes), is limited. Here, we reconstruct passerine evolutionary history and produce the most comprehensive time-calibrated phylogenetic hypothesis of the group using extensive sampling of the genome, complete sampling of all passerine families, and a number of vetted fossil calibration points. Our phylogenetic results refine our knowledge of passerine diversity and yield divergence dates that are consistent with the fossil record, and our macroevolutionary analyses suggest that singular events in Earth history, such as increases in Cenozoic global temperature or the colonization of new continents, were not the primary forces driving passerine diversification.

          Abstract

          Avian diversification has been influenced by global climate change, plate tectonic movements, and mass extinction events. However, the impact of these factors on the diversification of the hyperdiverse perching birds (passerines) is unclear because family level relationships are unresolved and the timing of splitting events among lineages is uncertain. We analyzed DNA data from 4,060 nuclear loci and 137 passerine families using concatenation and coalescent approaches to infer a comprehensive phylogenetic hypothesis that clarifies relationships among all passerine families. Then, we calibrated this phylogeny using 13 fossils to examine the effects of different events in Earth history on the timing and rate of passerine diversification. Our analyses reconcile passerine diversification with the fossil and geological records; suggest that passerines originated on the Australian landmass ∼47 Ma; and show that subsequent dispersal and diversification of passerines was affected by a number of climatological and geological events, such as Oligocene glaciation and inundation of the New Zealand landmass. Although passerine diversification rates fluctuated throughout the Cenozoic, we find no link between the rate of passerine diversification and Cenozoic global temperature, and our analyses show that the increases in passerine diversification rate we observe are disconnected from the colonization of new continents. Taken together, these results suggest more complex mechanisms than temperature change or ecological opportunity have controlled macroscale patterns of passerine speciation.

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          Bayes Factors

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            ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes

            Motivation: The estimation of species phylogenies requires multiple loci, since different loci can have different trees due to incomplete lineage sorting, modeled by the multi-species coalescent model. We recently developed a coalescent-based method, ASTRAL, which is statistically consistent under the multi-species coalescent model and which is more accurate than other coalescent-based methods on the datasets we examined. ASTRAL runs in polynomial time, by constraining the search space using a set of allowed ‘bipartitions’. Despite the limitation to allowed bipartitions, ASTRAL is statistically consistent. Results: We present a new version of ASTRAL, which we call ASTRAL-II. We show that ASTRAL-II has substantial advantages over ASTRAL: it is faster, can analyze much larger datasets (up to 1000 species and 1000 genes) and has substantially better accuracy under some conditions. ASTRAL’s running time is O ( n 2 k | X | 2 ) , and ASTRAL-II’s running time is O ( n k | X | 2 ) , where n is the number of species, k is the number of loci and X is the set of allowed bipartitions for the search space. Availability and implementation: ASTRAL-II is available in open source at https://github.com/smirarab/ASTRAL and datasets used are available at http://www.cs.utexas.edu/~phylo/datasets/astral2/. Contact: smirarab@gmail.com Supplementary information: Supplementary data are available at Bioinformatics online.
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              Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times.

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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                16 April 2019
                1 April 2019
                1 April 2019
                : 116
                : 16
                : 7916-7925
                Affiliations
                aDepartment of Biological Sciences, Louisiana State University , Baton Rouge, LA 70803;
                bDepartment of Biology & Biochemistry, Milner Centre for Evolution, University of Bath , Claverton Down, Bath BA2 7AY, United Kingdom;
                cDepartment of Earth Sciences, University of Cambridge , Cambridge CB2 3EQ, United Kingdom;
                dBruce Museum , Greenwich, CT 06830;
                eDepartment of Ecology, Evolution and Behavior, University of Minnesota , Saint Paul, MN 55108;
                fBell Museum of Natural History, University of Minnesota , Saint Paul, MN 55108;
                gDepartment of Zoology, Museu Paraense Emílio Goeldi , São Braz, 66040170 Belém, PA, Brazil;
                hDepartment of Biology, University of New Mexico , Albuquerque, NM 87131;
                iMuseum of Southwestern Biology, University of New Mexico , Albuquerque, NM 87131;
                jDepartment of Ecology and Genetics, Animal Ecology, Evolutionary Biology Centre, Uppsala University , SE-752 36 Uppsala, Sweden;
                kSwedish Species Information Centre, Swedish University of Agricultural Sciences , SE-750 07 Uppsala, Sweden;
                lKey Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences , 100101 Beijing, China;
                mDivision of Vertebrate Zoology, Department of Ornithology, American Museum of Natural History , New York, NY 10024;
                nMuseum of Zoology, University of Michigan , Ann Arbor, MI 48109;
                oDepartment of Ecology and Evolutionary Biology, University of Michigan , Ann Arbor, MI 48109;
                pDepartment of Biology, University of Florida , Gainesville, FL 32611;
                qDepartment of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution , Washington, DC 20013-7012;
                rBehavior, Ecology, Evolution and Systematics Graduate Program, University of Maryland , College Park, MD 20742;
                sDepartment of Organismic and Evolutionary Biology, Harvard University , Cambridge, MA 02138;
                tMuseum of Comparative Zoology, Harvard University , Cambridge, MA 02138;
                uMuseu de Zoologia da Universidade de São Paulo , 04263-000 Ipiranga, São Paulo, SP, Brazil;
                vMuseum of Natural Science, Louisiana State University , Baton Rouge, LA 70803;
                wUS Geological Survey, Patuxent Wildlife Research Center, National Museum of Natural History, Smithsonian Institution , Washington, DC 20560;
                xDepartment of Natural History, Royal Ontario Museum , Toronto, ON M5S2C6, Canada;
                yDepartment of Ecology and Evolutionary Biology, University of Toronto , Toronto, ON M5S3B2, Canada;
                zInstituto de Ciencias Naturales, Universidad Nacional de Colombia , Bogotá, Colombia, 111321;
                aaDepartment of Ecology and Evolutionary Biology, University of Tennessee Knoxville , Knoxville, TN 37996;
                bbDepartment of Environmental Health Science, University of Georgia , Athens, GA 30602;
                ccCenter for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen , Universitetsparken 15, DK-2100 Copenhagen, Denmark;
                ddAustralian National Wildlife Collection, CSIRO National Research Collections Australia , Canberra, ACT 2601, Australia;
                eeDivision of Mathematics and Natural Sciences, Pennsylvania State University-Altoona , Altoona, PA 16601;
                ffMuseum of New Zealand Te Papa Tongarewa , 6140 Wellington, New Zealand;
                ggBiodiversity Institute, University of Kansas , Lawrence, KS 66045
                Author notes
                1To whom correspondence may be addressed. Email: oliveros@ 123456lsu.edu or brant@ 123456faircloth-lab.org .

                Edited by Michael E. Alfaro, University of California, Los Angeles, CA, and accepted by Editorial Board Member David Jablonski February 26, 2019 (received for review August 9, 2018)

                Author contributions: C.H.O., D.J.F., D.T.K., F.K.B., P.A., P.A.H., R.G.M., and B.C.F. designed research; C.H.O., D.J.F., D.T.K., F.K.B., and B.C.F. performed research; C.H.O., D.J.F., D.T.K., and F.K.B. analyzed data; C.H.O. and B.C.F. wrote the paper with contributions from D.J.F., D.T.K., F.K.B., P.A., E.L.B., R.T.B., S.C., and R.T.K.; C.H.O., A.A., M.J.A., P.A., B.W.B., E.L.B., M.J.B., G.A.B., R.T.B., R.T.C., S.C., J.C., A.M.C., E.P.D., T.C.G., M.G.H., P.A.H., L.J., R.T.K., A.L.M., C.M.M., A.T.P., M.B.R., F.H.S., L.F.S., B.T.S., N.D.W., R.G.M., and B.C.F. contributed samples; D.J.F. and D.T.K. selected and vetted fossil calibrations; and F.K.B. performed lineage-specific diversification analyses.

                Article
                201813206
                10.1073/pnas.1813206116
                6475423
                30936315
                Copyright © 2019 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                Page count
                Pages: 10
                Product
                Funding
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: DEB-1655624
                Award Recipient : Daniel T. Ksepka Award Recipient : F Keith Barker Award Recipient : Alexandre Aleixo Award Recipient : Edward L Braun Award Recipient : Robb Brumfield Award Recipient : R. Terry Chesser Award Recipient : Joel Cracraft Award Recipient : Elizabeth P Derryberry Award Recipient : Rebecca T. Kimball Award Recipient : Frederick H Sheldon Award Recipient : Brian Tilston Smith Award Recipient : Robert G Moyle Award Recipient : Brant C Faircloth
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                Award Recipient : Daniel T. Ksepka Award Recipient : F Keith Barker Award Recipient : Alexandre Aleixo Award Recipient : Edward L Braun Award Recipient : Robb Brumfield Award Recipient : R. Terry Chesser Award Recipient : Joel Cracraft Award Recipient : Elizabeth P Derryberry Award Recipient : Rebecca T. Kimball Award Recipient : Frederick H Sheldon Award Recipient : Brian Tilston Smith Award Recipient : Robert G Moyle Award Recipient : Brant C Faircloth
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                Funded by: Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) 501100001807
                Award ID: 2012-23852-0
                Award Recipient : Gustavo A Bravo Award Recipient : Luís Fábio Silveira
                Funded by: Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) 501100001807
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                Funded by: MCTI | Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) 501100003593
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                Funded by: MCTI | Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) 501100003593
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                Categories
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                Biological Sciences
                Evolution
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