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Research Article

Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous–Paleogene boundary

Yan-Jie Feng, View ORCID ProfileDavid C. Blackburn, Dan Liang, David M. Hillis, View ORCID ProfileDavid B. Wake, David C. Cannatella, and Peng Zhang
  1. aState Key Laboratory of Biocontrol, College of Ecology and Evolution, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510006, China;
  2. bDepartment of Natural History, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611;
  3. cDepartment of Integrative Biology and Biodiversity Collections, University of Texas, Austin, TX 78712;
  4. dMuseum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, CA 94720

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PNAS first published July 3, 2017; https://doi.org/10.1073/pnas.1704632114
Yan-Jie Feng
aState Key Laboratory of Biocontrol, College of Ecology and Evolution, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510006, China;
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David C. Blackburn
bDepartment of Natural History, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611;
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  • ORCID record for David C. Blackburn
Dan Liang
aState Key Laboratory of Biocontrol, College of Ecology and Evolution, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510006, China;
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David M. Hillis
cDepartment of Integrative Biology and Biodiversity Collections, University of Texas, Austin, TX 78712;
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David B. Wake
dMuseum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, CA 94720
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  • ORCID record for David B. Wake
  • For correspondence: wakelab@berkeley.edu catfish@utexas.edu zhangp35@mail.sysu.edu.cn
David C. Cannatella
cDepartment of Integrative Biology and Biodiversity Collections, University of Texas, Austin, TX 78712;
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  • For correspondence: wakelab@berkeley.edu catfish@utexas.edu zhangp35@mail.sysu.edu.cn
Peng Zhang
aState Key Laboratory of Biocontrol, College of Ecology and Evolution, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510006, China;
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  • For correspondence: wakelab@berkeley.edu catfish@utexas.edu zhangp35@mail.sysu.edu.cn
  1. Contributed by David B. Wake, June 2, 2017 (sent for review March 22, 2017; reviewed by S. Blair Hedges and Jonathan B. Losos)

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Significance

Frogs are the dominant component of semiaquatic vertebrate faunas. How frogs originated and diversified has long attracted the attention of evolutionary biologists. Here, we recover their evolutionary history by extensive sampling of genes and species and present a hypothesis for frog evolution. In contrast to prior conclusions that the major frog clades were established in the Mesozoic, we find that ∼88% of living frogs originated from three principal lineages that arose at the end of the Mesozoic, coincident with the Cretaceous–Paleogene (K–Pg) mass extinction event that decimated nonavian dinosaurs 66 Mya. The K–Pg extinction events played a pivotal role in shaping the current diversity and geographic distribution of modern frogs.

Abstract

Frogs (Anura) are one of the most diverse groups of vertebrates and comprise nearly 90% of living amphibian species. Their worldwide distribution and diverse biology make them well-suited for assessing fundamental questions in evolution, ecology, and conservation. However, despite their scientific importance, the evolutionary history and tempo of frog diversification remain poorly understood. By using a molecular dataset of unprecedented size, including 88-kb characters from 95 nuclear genes of 156 frog species, in conjunction with 20 fossil-based calibrations, our analyses result in the most strongly supported phylogeny of all major frog lineages and provide a timescale of frog evolution that suggests much younger divergence times than suggested by earlier studies. Unexpectedly, our divergence-time analyses show that three species-rich clades (Hyloidea, Microhylidae, and Natatanura), which together comprise ∼88% of extant anuran species, simultaneously underwent rapid diversification at the Cretaceous–Paleogene (K–Pg) boundary (KPB). Moreover, anuran families and subfamilies containing arboreal species originated near or after the KPB. These results suggest that the K–Pg mass extinction may have triggered explosive radiations of frogs by creating new ecological opportunities. This phylogeny also reveals relationships such as Microhylidae being sister to all other ranoid frogs and African continental lineages of Natatanura forming a clade that is sister to a clade of Eurasian, Indian, Melanesian, and Malagasy lineages. Biogeographical analyses suggest that the ancestral area of modern frogs was Africa, and their current distribution is largely associated with the breakup of Pangaea and subsequent Gondwanan fragmentation.

  • amphibia
  • Anura
  • nuclear genes
  • phylogeny
  • divergence time

Footnotes

  • ↵1To whom correspondence may be addressed. Email: wakelab{at}berkeley.edu, catfish{at}utexas.edu, or zhangp35{at}mail.sysu.edu.cn.
  • Author contributions: D.C.B., D.M.H., D.B.W., D.C.C., and P.Z. designed research; D.C.B., D.M.H., D.B.W., D.C.C., and P.Z. designed and carried out taxon sampling; D.C.B. and D.C.C. selected and vetted calibration points; Y.-J.F. and D.L. performed laboratory research; Y.-J.F., D.L., and P.Z. analyzed data; and Y.-J.F., D.C.B., D.L., D.M.H., D.B.W., D.C.C., and P.Z. wrote the paper.

  • Reviewers: S.B.H., Temple University; and J.B.L., Harvard University.

  • The authors declare no conflict of interest.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database. For a list of accession numbers, see Dataset S1.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1704632114/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Explosive radiation of frogs at the K–Pg boundary
Yan-Jie Feng, David C. Blackburn, Dan Liang, David M. Hillis, David B. Wake, David C. Cannatella, Peng Zhang
Proceedings of the National Academy of Sciences Jul 2017, 201704632; DOI: 10.1073/pnas.1704632114

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Explosive radiation of frogs at the K–Pg boundary
Yan-Jie Feng, David C. Blackburn, Dan Liang, David M. Hillis, David B. Wake, David C. Cannatella, Peng Zhang
Proceedings of the National Academy of Sciences Jul 2017, 201704632; DOI: 10.1073/pnas.1704632114
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