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

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 i...

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Vydáno v:Proceedings of the National Academy of Sciences - PNAS Ročník 114; číslo 29; s. E5864
Hlavní autoři: Feng, Yan-Jie, Blackburn, David C, Liang, Dan, Hillis, David M, Wake, David B, Cannatella, David C, Zhang, Peng
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States 18.07.2017
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ISSN:1091-6490, 1091-6490
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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.
AbstractList 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.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.
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.
Author Cannatella, David C
Zhang, Peng
Wake, David B
Hillis, David M
Feng, Yan-Jie
Blackburn, David C
Liang, Dan
Author_xml – sequence: 1
  givenname: Yan-Jie
  surname: Feng
  fullname: Feng, Yan-Jie
  organization: State Key Laboratory of Biocontrol, College of Ecology and Evolution, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510006, China
– sequence: 2
  givenname: David C
  orcidid: 0000-0002-1810-9886
  surname: Blackburn
  fullname: Blackburn, David C
  organization: Department of Natural History, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611
– sequence: 3
  givenname: Dan
  surname: Liang
  fullname: Liang, Dan
  organization: State Key Laboratory of Biocontrol, College of Ecology and Evolution, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510006, China
– sequence: 4
  givenname: David M
  surname: Hillis
  fullname: Hillis, David M
  organization: Department of Integrative Biology and Biodiversity Collections, University of Texas, Austin, TX 78712
– sequence: 5
  givenname: David B
  orcidid: 0000-0003-4835-2497
  surname: Wake
  fullname: Wake, David B
  email: wakelab@berkeley.edu, catfish@utexas.edu, zhangp35@mail.sysu.edu.cn
  organization: Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, CA 94720 wakelab@berkeley.edu catfish@utexas.edu zhangp35@mail.sysu.edu.cn
– sequence: 6
  givenname: David C
  surname: Cannatella
  fullname: Cannatella, David C
  email: wakelab@berkeley.edu, catfish@utexas.edu, zhangp35@mail.sysu.edu.cn
  organization: Department of Integrative Biology and Biodiversity Collections, University of Texas, Austin, TX 78712; wakelab@berkeley.edu catfish@utexas.edu zhangp35@mail.sysu.edu.cn
– sequence: 7
  givenname: Peng
  surname: Zhang
  fullname: Zhang, Peng
  email: wakelab@berkeley.edu, catfish@utexas.edu, zhangp35@mail.sysu.edu.cn
  organization: State Key Laboratory of Biocontrol, College of Ecology and Evolution, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510006, China; wakelab@berkeley.edu catfish@utexas.edu zhangp35@mail.sysu.edu.cn
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28673970$$D View this record in MEDLINE/PubMed
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Keywords Anura
divergence time
phylogeny
nuclear genes
amphibia
Language English
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ORCID 0000-0003-4835-2497
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OpenAccessLink https://www.pnas.org/doi/10.1073/pnas.1704632114
PMID 28673970
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PublicationTitle Proceedings of the National Academy of Sciences - PNAS
PublicationTitleAlternate Proc Natl Acad Sci U S A
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Snippet Frogs (Anura) are one of the most diverse groups of vertebrates and comprise nearly 90% of living amphibian species. Their worldwide distribution and diverse...
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SubjectTerms Amphibian Proteins - genetics
Animals
Anura - genetics
Anura - physiology
Biological Evolution
Extinction, Biological
Fossils
Phylogeny
Phylogeography
Ranidae - genetics
Ranidae - physiology
Title Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous-Paleogene boundary
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