Earth history and the passerine superradiation

doi:10.1073/pnas.1813206116

. 2019 Apr 16;116(16):7916-7925.

doi: 10.1073/pnas.1813206116. Epub 2019 Apr 1.

Earth history and the passerine superradiation

Carl H Oliveros¹, Daniel J Field^{2

3}, Daniel T Ksepka⁴, F Keith Barker^{5

6}, Alexandre Aleixo⁷, Michael J Andersen^{8

9}, Per Alström^{10

11

12}, Brett W Benz^{13

14

15}, Edward L Braun¹⁶, Michael J Braun^{17

18}, Gustavo A Bravo^{19

20

21}, Robb T Brumfield^{22

23}, R Terry Chesser²⁴, Santiago Claramunt^{25

26}, Joel Cracraft¹³, Andrés M Cuervo²⁷, Elizabeth P Derryberry²⁸, Travis C Glenn²⁹, Michael G Harvey²⁸, Peter A Hosner^{17

30}, Leo Joseph³¹, Rebecca T Kimball¹⁶, Andrew L Mack³², Colin M Miskelly³³, A Townsend Peterson³⁴, Mark B Robbins³⁴, Frederick H Sheldon^{22

23}, Luís Fábio Silveira²¹, Brian Tilston Smith¹³, Noor D White^{17

18}, Robert G Moyle³⁴, Brant C Faircloth^{1

23}

Affiliations

¹ Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803; [email protected] [email protected].
² Department of Biology & Biochemistry, Milner Centre for Evolution, University of Bath, Claverton Down, Bath BA2 7AY, United Kingdom.
³ Department of Earth Sciences, University of Cambridge, Cambridge CB2 3EQ, United Kingdom.
⁴ Bruce Museum, Greenwich, CT 06830.
⁵ Department of Ecology, Evolution and Behavior, University of Minnesota, Saint Paul, MN 55108.
⁶ Bell Museum of Natural History, University of Minnesota, Saint Paul, MN 55108.
⁷ Department of Zoology, Museu Paraense Emílio Goeldi, São Braz, 66040170 Belém, PA, Brazil.
⁸ Department of Biology, University of New Mexico, Albuquerque, NM 87131.
⁹ Museum of Southwestern Biology, University of New Mexico, Albuquerque, NM 87131.
¹⁰ Department of Ecology and Genetics, Animal Ecology, Evolutionary Biology Centre, Uppsala University, SE-752 36 Uppsala, Sweden.
¹¹ Swedish Species Information Centre, Swedish University of Agricultural Sciences, SE-750 07 Uppsala, Sweden.
¹² Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, 100101 Beijing, China.
¹³ Division of Vertebrate Zoology, Department of Ornithology, American Museum of Natural History, New York, NY 10024.
¹⁴ Museum of Zoology, University of Michigan, Ann Arbor, MI 48109.
¹⁵ Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109.
¹⁶ Department of Biology, University of Florida, Gainesville, FL 32611.
¹⁷ Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012.
¹⁸ Behavior, Ecology, Evolution and Systematics Graduate Program, University of Maryland, College Park, MD 20742.
¹⁹ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138.
²⁰ Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138.
²¹ Museu de Zoologia da Universidade de São Paulo, 04263-000 Ipiranga, São Paulo, SP, Brazil.
²² Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803.
²³ Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803.
²⁴ US Geological Survey, Patuxent Wildlife Research Center, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560.
²⁵ Department of Natural History, Royal Ontario Museum, Toronto, ON M5S2C6, Canada.
²⁶ Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON M5S3B2, Canada.
²⁷ Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá, Colombia, 111321.
²⁸ Department of Ecology and Evolutionary Biology, University of Tennessee Knoxville, Knoxville, TN 37996.
²⁹ Department of Environmental Health Science, University of Georgia, Athens, GA 30602.
³⁰ Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.
³¹ Australian National Wildlife Collection, CSIRO National Research Collections Australia, Canberra, ACT 2601, Australia.
³² Division of Mathematics and Natural Sciences, Pennsylvania State University-Altoona, Altoona, PA 16601.
³³ Museum of New Zealand Te Papa Tongarewa, 6140 Wellington, New Zealand.
³⁴ Biodiversity Institute, University of Kansas, Lawrence, KS 66045.

PMID: 30936315
PMCID: PMC6475423
DOI: 10.1073/pnas.1813206116

Earth history and the passerine superradiation

Carl H Oliveros et al. Proc Natl Acad Sci U S A. 2019.

. 2019 Apr 16;116(16):7916-7925.

doi: 10.1073/pnas.1813206116. Epub 2019 Apr 1.

Authors

Affiliations

¹ Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803; [email protected] [email protected].
² Department of Biology & Biochemistry, Milner Centre for Evolution, University of Bath, Claverton Down, Bath BA2 7AY, United Kingdom.
³ Department of Earth Sciences, University of Cambridge, Cambridge CB2 3EQ, United Kingdom.
⁴ Bruce Museum, Greenwich, CT 06830.
⁵ Department of Ecology, Evolution and Behavior, University of Minnesota, Saint Paul, MN 55108.
⁶ Bell Museum of Natural History, University of Minnesota, Saint Paul, MN 55108.
⁷ Department of Zoology, Museu Paraense Emílio Goeldi, São Braz, 66040170 Belém, PA, Brazil.
⁸ Department of Biology, University of New Mexico, Albuquerque, NM 87131.
⁹ Museum of Southwestern Biology, University of New Mexico, Albuquerque, NM 87131.
¹⁰ Department of Ecology and Genetics, Animal Ecology, Evolutionary Biology Centre, Uppsala University, SE-752 36 Uppsala, Sweden.
¹¹ Swedish Species Information Centre, Swedish University of Agricultural Sciences, SE-750 07 Uppsala, Sweden.
¹² Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, 100101 Beijing, China.
¹³ Division of Vertebrate Zoology, Department of Ornithology, American Museum of Natural History, New York, NY 10024.
¹⁴ Museum of Zoology, University of Michigan, Ann Arbor, MI 48109.
¹⁵ Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109.
¹⁶ Department of Biology, University of Florida, Gainesville, FL 32611.
¹⁷ Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012.
¹⁸ Behavior, Ecology, Evolution and Systematics Graduate Program, University of Maryland, College Park, MD 20742.
¹⁹ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138.
²⁰ Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138.
²¹ Museu de Zoologia da Universidade de São Paulo, 04263-000 Ipiranga, São Paulo, SP, Brazil.
²² Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803.
²³ Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803.
²⁴ US Geological Survey, Patuxent Wildlife Research Center, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560.
²⁵ Department of Natural History, Royal Ontario Museum, Toronto, ON M5S2C6, Canada.
²⁶ Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON M5S3B2, Canada.
²⁷ Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá, Colombia, 111321.
²⁸ Department of Ecology and Evolutionary Biology, University of Tennessee Knoxville, Knoxville, TN 37996.
²⁹ Department of Environmental Health Science, University of Georgia, Athens, GA 30602.
³⁰ Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.
³¹ Australian National Wildlife Collection, CSIRO National Research Collections Australia, Canberra, ACT 2601, Australia.
³² Division of Mathematics and Natural Sciences, Pennsylvania State University-Altoona, Altoona, PA 16601.
³³ Museum of New Zealand Te Papa Tongarewa, 6140 Wellington, New Zealand.
³⁴ Biodiversity Institute, University of Kansas, Lawrence, KS 66045.

PMID: 30936315
PMCID: PMC6475423
DOI: 10.1073/pnas.1813206116

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.

Keywords: Passeriformes; biogeography; climate; diversification; macroevolution.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

**Fig. 1.**
Family-level phylogenetic relationships in passerines reconciled from concatenation and coalescent analyses (connects to top of Fig. 2 at the circled star). Maximum likelihood bootstrap support (BS) values are indicated by boxes (BS > 70) or circles (BS j model using BioGeoBEARS from the distribution of clades represented by each tip [shown by boxes at tips coded according to the map (*Inset*)]. Light blue and pink bars indicate Oligocene glaciation and warming events, respectively. The estimate of Cenozoic global surface temperatures (red curve) was taken from ref. . Branches with the strongest support for diversification rate shifts are indicated by pink arrows in their descendant node for internal branches or at the base of the branch for terminal branches. Geological and climatic events are indicated above the timeline with descriptions provided in the key (*Inset*). Plei., Pleistocene; Plio., Pliocene.

**Fig. 2.**
Family-level phylogenetic relationships in passerines reconciled from concatenation and coalescent analyses (connects to bottom of Fig. 1 at the circled star). Biogeographic reconstruction including fossil taxa (*Inset*, tree) yields identical ancestral areas for crown lineages of passerines, suboscines, and oscines (also *SI Appendix*, Fig. S8). Plei., Pleistocene; Plio., Pliocene.

**Fig. 3.**
Comparison of date estimates of key nodes in passerine phylogeny across three fossil calibration schemes (sets A–C; a detailed description is provided in *Materials and Methods*) using log-normally distributed priors. Bars represent 95% credible intervals of joint priors [Markov chain Monte Carlo (MCMC) without data] and posteriors of random samples of 25 loci. Color boxes in the heading for each node indicate the set(s) of calibrations in which the node was used as a calibration point. Date estimates from previous studies (–5, 19) for the same node are also shown, if available.

**Fig. 4.**
Estimate of episodic diversification rate of passerines (solid line) and 95% credible interval (light blue band) based on RevBayes analysis of our chronogram (Figs. 1 and 2) across time periods of 2 million y. Global deep ocean temperature data used in the analysis (dotted red line) were taken from ref. . Geological and climatic events from Figs. 1 and 2 (excluding events a and b) are indicated above the time line with descriptions provided in the key (*Inset*). Plei., Pleistocene; Plio., Pliocene.

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References

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[1] Feduccia A. Explosive evolution in tertiary birds and mammals. Science. 1995;267:637–638. - PubMed

[2] Feduccia A. Explosive evolution in tertiary birds and mammals. Science. 1995;267:637–638. - PubMed

[3] Jarvis ED, et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014;346:1320–1331. - PMC - PubMed

[4] Jarvis ED, et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014;346:1320–1331. - PMC - PubMed

[5] Prum RO, et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature. 2015;526:569–573. - PubMed

[6] Prum RO, et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature. 2015;526:569–573. - PubMed

[7] Claramunt S, Cracraft J. A new time tree reveals Earth history’s imprint on the evolution of modern birds. Sci Adv. 2015;1:e1501005. - PMC - PubMed

[8] Claramunt S, Cracraft J. A new time tree reveals Earth history’s imprint on the evolution of modern birds. Sci Adv. 2015;1:e1501005. - PMC - PubMed

[9] Moyle RG, et al. Tectonic collision and uplift of Wallacea triggered the global songbird radiation. Nat Commun. 2016;7:12709. - PMC - PubMed

[10] Moyle RG, et al. Tectonic collision and uplift of Wallacea triggered the global songbird radiation. Nat Commun. 2016;7:12709. - PMC - PubMed

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Earth history and the passerine superradiation

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Earth history and the passerine superradiation

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