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Earth History and the Passerine Superradiation

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Earth history and the passerine superradiation Carl H. Oliverosa,1, Daniel J. Fieldb,c, Daniel T. Ksepkad, F. Keith Barkere,f, Alexandre Aleixog, Michael J. Andersenh,i, Per Alströmj,k,l, Brett W. Benzm,n,o, Edward L. Braunp, Michael J. Braunq,r, Gustavo A. Bravos,t,u, Robb T. Brumfielda,v, R. Terry Chesserw, Santiago Claramuntx,y, Joel Cracraftm, Andrés M. Cuervoz, Elizabeth P. Derryberryaa, Travis C. Glennbb, Michael G. Harveyaa, Peter A. Hosnerq,cc, Leo Josephdd, Rebecca T. Kimballp, Andrew L. Mackee, Colin M. Miskellyff, A. Townsend Petersongg, Mark B. Robbinsgg, Frederick H. Sheldona,v, Luís Fábio Silveirau, Brian Tilston Smithm, Noor D. Whiteq,r, Robert G. Moylegg, and Brant C. Fairclotha,v,1 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; uMuseudeZoologiadaUniversidadedeSãoPaulo,04263-000Ipiranga,SãoPaulo,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; yDepartmentofEcology 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; and ggBiodiversity Institute, University of Kansas, Lawrence, KS 66045 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) Avian diversification has been influenced by global climate change, plate tectonic movements, and mass extinction events. However, Significance the impact of these factors on the diversification of the hyper- diverse perching birds (passerines) is unclear because family level Our understanding of the factors that affected the diversifi- relationships are unresolved and the timing of splitting events cation of passerines, the most diverse and widespread bird among lineages is uncertain. We analyzed DNA data from 4,060 order (Passeriformes), is limited. Here, we reconstruct passerine nuclear loci and 137 passerine families using concatenation and evolutionary history and produce the most comprehensive time- coalescent approaches to infer a comprehensive phylogenetic calibrated phylogenetic hypothesis of the group using extensive hypothesis that clarifies relationships among all passerine families. sampling of the genome, complete sampling of all passerine Then, we calibrated this phylogeny using 13 fossils to examine the families, and a number of vetted fossil calibration points. Our effects of different events in Earth history on the timing and rate phylogenetic results refine our knowledge of passerine diversity of passerine diversification. Our analyses reconcile passerine diver- and yield divergence dates that are consistent with the fossil sification with the fossil and geological records; suggest that pas- record, and our macroevolutionary analyses suggest that sin- serines originated on the Australian landmass ∼47 Ma; and show gular events in Earth history, such as increases in Cenozoic that subsequent dispersal and diversification of passerines was global temperature or the colonization of new continents, were affected by a number of climatological and geological events, such not the primary forces driving passerine diversification. as Oligocene glaciation and inundation of the New Zealand land- mass. Although passerine diversification rates fluctuated through- 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 re- out the Cenozoic, we find no link between the rate of passerine search; 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., diversification and Cenozoic global temperature, and our analyses 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., show that the increases in passerine diversification rate we ob- 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., serve are disconnected from the colonization of new continents. 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 Taken together, these results suggest more complex mechanisms and vetted fossil calibrations; and F.K.B. performed lineage-specific diversification analyses. than temperature change or ecological opportunity have controlled The authors declare no conflict of interest. macroscale patterns of passerine speciation. This article is a PNAS Direct Submission. M.E.A. is a guest editor invited by the Editorial Board. This open access article is distributed under Creative Commons Attribution-NonCommercial- Passeriformes | diversification | macroevolution | climate | biogeography NoDerivatives License 4.0 (CC BY-NC-ND). Data deposition: Raw sequencing reads and ultraconserved element (UCE) nucleotide se- he diversification of modern birds (Neornithes) was shaped quences are available from the National Center for Biotechnology Information (NCBI) Se- Tby numerous factors, including a mass extinction event (1–3), quence Read Archive and Genbank as part of BioProjects PRJNA304409 and PRJNA480834. shifts in connectivity between continents (4, 5), and changes in NCBI BioSample accession numbers are available in Dataset S1. The PHYLUCE computer code used in this study is available from https://github.com/faircloth-lab/phyluce. Other custom global climate (4, 6). Specific ecological, geological, and clima- computer code, DNA alignments, analysis inputs, and analysis outputs are available from tological events proposed to be associated with the diversifica- the Dryad Digital Repository database, datadryad.org/ (doi: 10.5061/dryad.2vd01gr). tion and global distribution of Neornithes include opening of 1To whom correspondence may be addressed. Email: [email protected] or [email protected]. ecological niches following the Cretaceous-Paleogene (K-Pg) This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. mass extinction event (2, 3, 7, 8), establishment of dispersal 1073/pnas.1813206116/-/DCSupplemental. corridors linking the geographic origin of modern birds to other Published online April 1, 2019. 7916–7925 | PNAS | April 16, 2019 | vol. 116 | no. 16 www.pnas.org/cgi/doi/10.1073/pnas.1813206116 Downloaded by guest on October 3, 2021 landmasses during the Paleogene (4), rapid continental drift and approaches. We then use our time-calibrated phylogeny and island formation in Wallacea allowing the dispersal of songbirds fossil data to investigate passerine biogeography and diversifi- out of Australia (5, 9), fragmentation of tropical habitats during cation rates, as well as the influence of major events in Earth cooling events of the Late Cretaceous and Cenozoic (4, 10), and history on the
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