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      Earth history and the passerine superradiation

      research-article
      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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          Most cited references73

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          Trends, rhythms, and aberrations in global climate 65 Ma to present.

          Since 65 million years ago (Ma), Earth's climate has undergone a significant and complex evolution, the finer details of which are now coming to light through investigations of deep-sea sediment cores. This evolution includes gradual trends of warming and cooling driven by tectonic processes on time scales of 10(5) to 10(7) years, rhythmic or periodic cycles driven by orbital processes with 10(4)- to 10(6)-year cyclicity, and rare rapid aberrant shifts and extreme climate transients with durations of 10(3) to 10(5) years. Here, recent progress in defining the evolution of global climate over the Cenozoic Era is reviewed. We focus primarily on the periodic and anomalous components of variability over the early portion of this era, as constrained by the latest generation of deep-sea isotope records. We also consider how this improved perspective has led to the recognition of previously unforeseen mechanisms for altering climate.
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            Bayes Factors

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              Model selection in historical biogeography reveals that founder-event speciation is a crucial process in Island Clades.

              Founder-event speciation, where a rare jump dispersal event founds a new genetically isolated lineage, has long been considered crucial by many historical biogeographers, but its importance is disputed within the vicariance school. Probabilistic modeling of geographic range evolution creates the potential to test different biogeographical models against data using standard statistical model choice procedures, as long as multiple models are available. I re-implement the Dispersal-Extinction-Cladogenesis (DEC) model of LAGRANGE in the R package BioGeoBEARS, and modify it to create a new model, DEC + J, which adds founder-event speciation, the importance of which is governed by a new free parameter, [Formula: see text]. The identifiability of DEC and DEC + J is tested on data sets simulated under a wide range of macroevolutionary models where geography evolves jointly with lineage birth/death events. The results confirm that DEC and DEC + J are identifiable even though these models ignore the fact that molecular phylogenies are missing many cladogenesis and extinction events. The simulations also indicate that DEC will have substantially increased errors in ancestral range estimation and parameter inference when the true model includes + J. DEC and DEC + J are compared on 13 empirical data sets drawn from studies of island clades. Likelihood-ratio tests indicate that all clades reject DEC, and AICc model weights show large to overwhelming support for DEC + J, for the first time verifying the importance of founder-event speciation in island clades via statistical model choice. Under DEC + J, ancestral nodes are usually estimated to have ranges occupying only one island, rather than the widespread ancestors often favored by DEC. These results indicate that the assumptions of historical biogeography models can have large impacts on inference and require testing and comparison with statistical methods. © The Author(s) 2014. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: journals.permissions@oup.com.
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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
                [1] aDepartment of Biological Sciences, Louisiana State University , Baton Rouge, LA 70803;
                [2] bDepartment of Biology & Biochemistry, Milner Centre for Evolution, University of Bath , Claverton Down, Bath BA2 7AY, United Kingdom;
                [3] cDepartment of Earth Sciences, University of Cambridge , Cambridge CB2 3EQ, United Kingdom;
                [4] dBruce Museum , Greenwich, CT 06830;
                [5] eDepartment of Ecology, Evolution and Behavior, University of Minnesota , Saint Paul, MN 55108;
                [6] fBell Museum of Natural History, University of Minnesota , Saint Paul, MN 55108;
                [7] gDepartment of Zoology, Museu Paraense Emílio Goeldi , São Braz, 66040170 Belém, PA, Brazil;
                [8] hDepartment of Biology, University of New Mexico , Albuquerque, NM 87131;
                [9] iMuseum of Southwestern Biology, University of New Mexico , Albuquerque, NM 87131;
                [10] jDepartment of Ecology and Genetics, Animal Ecology, Evolutionary Biology Centre, Uppsala University , SE-752 36 Uppsala, Sweden;
                [11] kSwedish Species Information Centre, Swedish University of Agricultural Sciences , SE-750 07 Uppsala, Sweden;
                [12] lKey Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences , 100101 Beijing, China;
                [13] mDivision of Vertebrate Zoology, Department of Ornithology, American Museum of Natural History , New York, NY 10024;
                [14] nMuseum of Zoology, University of Michigan , Ann Arbor, MI 48109;
                [15] oDepartment of Ecology and Evolutionary Biology, University of Michigan , Ann Arbor, MI 48109;
                [16] pDepartment of Biology, University of Florida , Gainesville, FL 32611;
                [17] qDepartment of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution , Washington, DC 20013-7012;
                [18] rBehavior, Ecology, Evolution and Systematics Graduate Program, University of Maryland , College Park, MD 20742;
                [19] sDepartment of Organismic and Evolutionary Biology, Harvard University , Cambridge, MA 02138;
                [20] tMuseum of Comparative Zoology, Harvard University , Cambridge, MA 02138;
                [21] uMuseu de Zoologia da Universidade de São Paulo , 04263-000 Ipiranga, São Paulo, SP, Brazil;
                [22] vMuseum of Natural Science, Louisiana State University , Baton Rouge, LA 70803;
                [23] wUS Geological Survey, Patuxent Wildlife Research Center, National Museum of Natural History, Smithsonian Institution , Washington, DC 20560;
                [24] xDepartment of Natural History, Royal Ontario Museum , Toronto, ON M5S2C6, Canada;
                [25] yDepartment of Ecology and Evolutionary Biology, University of Toronto , Toronto, ON M5S3B2, Canada;
                [26] zInstituto de Ciencias Naturales, Universidad Nacional de Colombia , Bogotá, Colombia, 111321;
                [27] aaDepartment of Ecology and Evolutionary Biology, University of Tennessee Knoxville , Knoxville, TN 37996;
                [28] bbDepartment of Environmental Health Science, University of Georgia , Athens, GA 30602;
                [29] ccCenter for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen , Universitetsparken 15, DK-2100 Copenhagen, Denmark;
                [30] ddAustralian National Wildlife Collection, CSIRO National Research Collections Australia , Canberra, ACT 2601, Australia;
                [31] eeDivision of Mathematics and Natural Sciences, Pennsylvania State University-Altoona , Altoona, PA 16601;
                [32] ffMuseum of New Zealand Te Papa Tongarewa , 6140 Wellington, New Zealand;
                [33] 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.

                Author information
                http://orcid.org/0000-0002-3356-246X
                http://orcid.org/0000-0002-1786-0352
                http://orcid.org/0000-0001-7488-2470
                http://orcid.org/0000-0002-7220-5588
                http://orcid.org/0000-0001-7182-2763
                http://orcid.org/0000-0001-5889-2767
                http://orcid.org/0000-0003-2307-0688
                http://orcid.org/0000-0002-8926-5974
                http://orcid.org/0000-0001-7499-6224
                http://orcid.org/0000-0001-7564-1978
                http://orcid.org/0000-0001-5449-5481
                http://orcid.org/0000-0003-0243-2379
                http://orcid.org/0000-0003-2576-7657
                http://orcid.org/0000-0002-9510-3744
                http://orcid.org/0000-0002-1943-0217
                Article
                201813206
                10.1073/pnas.1813206116
                6475423
                30936315
                9d7de5a1-2f6d-461d-a1de-ffad0935fdf0
                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).

                History
                Page count
                Pages: 10
                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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                Funded by: Swedish Research Foundation
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                Categories
                PNAS Plus
                Biological Sciences
                Evolution
                From the Cover
                PNAS Plus

                passeriformes,diversification,macroevolution,climate,biogeography

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