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Fifteen shades of green: The evolution of Bufotes toads revisited.
Journal article

Fifteen shades of green: The evolution of Bufotes toads revisited.

  • Dufresnes C Laboratory for Conservation Biology, Biophore Building, University of Lausanne, 1015 Lausanne, Switzerland; Hintermann & Weber, Avenue des Alpes 25, 1820 Montreux, Switzerland. Electronic address: Christophe.Dufresnes@hotmail.fr.
  • Mazepa G Department of Ecology and Evolution, Biophore Building, University of Lausanne, 1015 Lausanne, Switzerland; Department of Ecology and Genetics, Evolutionary Biology, Norbyvägen 18D, 75236 Uppsala, Sweden.
  • Jablonski D Department of Zoology, Comenius University in Bratislava, Mlynská dolina, Ilkovičova 6, 842 15 Bratislava, Slovakia.
  • Oliveira RC Laboratory of Socioecology and Social Evolution, Zoological Institute, KU Leuven, Naamsestraat 59, 3000 Leuven, Belgium.
  • Wenseleers T Laboratory of Socioecology and Social Evolution, Zoological Institute, KU Leuven, Naamsestraat 59, 3000 Leuven, Belgium.
  • Shabanov DA Department of Zoology and Animal Ecology, V. N. Karazin Kharkiv National University, Svobody Square 4, Kharkiv 61022, Ukraine.
  • Auer M Museum of Zoology, Senckenberg Natural History Collections Dresden, Königsbrücker Landstr. 159, D-01109 Dresden, Germany.
  • Ernst R Museum of Zoology, Senckenberg Natural History Collections Dresden, Königsbrücker Landstr. 159, D-01109 Dresden, Germany.
  • Koch C Zoologisches Forschungsmuseum Alexander Koenig (Leibniz-Institut für Biodiversität der Tiere), Bonn, Germany.
  • Ramírez-Chaves HE Facultad de Ciencias Exactas y Naturales, Departamento de Ciencias Biológicas, Universidad de Caldas, Calle 65 # 26-10, Manizales, Caldas, Colombia; Centro de Museos, Museo de Historia Natural, Universidad de Caldas, Calle 65 # 26-10, Manizales, Caldas, Colombia.
  • Mulder KP CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal; Center for Conservation Genomics, Smithsonian Conservation Biology Institute, National Zoological Park, 3001 Connecticut Ave NW, Washington, DC 20008, USA; Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 10th St. & Constitution Ave. NW, Washington, DC 20560, USA.
  • Simonov E Institute of Systematics and Ecology of Animals of the Siberian Branch of the Russian Academy of Sciences, Research Group of Physiology and Genetics of Hydrobionts, Novosibirsk 630091, Russia; Federal Research Center "Krasnoyarsk Science Center of the Siberian Branch of the Russian Academy of Sciences", Laboratory of Genomic Research and Biotechnology, Krasnoyarsk 660036, Russia.
  • Tiutenko A University of Erlangen-Nuremberg, Schlossplatz 6, D91054 Erlangen, Germany.
  • Kryvokhyzha D Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala Biomedicinska Centrum (BMC), Box 582, 75123 Uppsala, Sweden.
  • Wennekes PL Plant Systemics and Evolution, School of Biological Sciences, University of Reading, Philip Lyle Building 208, Pepper Ln, RG6 6LA Reading, United Kingdom.
  • Zinenko OI Department of Zoology and Animal Ecology, V. N. Karazin Kharkiv National University, Svobody Square 4, Kharkiv 61022, Ukraine; The Museum of Nature at V. N. Karazin Kharkiv National University, Trinkler St. 8, Kharkiv 61058, Ukraine.
  • Korshunov OV Department of Zoology and Animal Ecology, V. N. Karazin Kharkiv National University, Svobody Square 4, Kharkiv 61022, Ukraine.
  • Al-Johany AM Department of Zoology, King Saud University, Riyadh 11451, Saudi Arabia.
  • Peregontsev EA Zoocomplex MChJ, Gagarin Vil. 14, 100149 Sergeli District, Tashkent City, Uzbekistan.
  • Masroor R Pakistan Museum of Natural History, Garden Avenue, Shakarparian, Islamabad 44000, Pakistan.
  • Betto-Colliard C Department of Ecology and Evolution, Biophore Building, University of Lausanne, 1015 Lausanne, Switzerland.
  • Denoël M Laboratory of Fish and Amphibian Ethology, Behavioural Biology Group, Freshwater and OCeanic science Unit of reSearch (FOCUS), University of Liège, Liège, Belgium.
  • Borkin LJ Department of Herpetology, Zoological Institute, Russian Academy of Sciences, 199034 St. Petersburg, Russia.
  • Skorinov DV Institute of Cytology, Russian Academy of Sciences, Saint Petersburg, Russia.
  • Pasynkova RA Institute of Cytology, Russian Academy of Sciences, Saint Petersburg, Russia.
  • Mazanaeva LF Dagestan State University, Makhachkala, Russia.
  • Rosanov JM Institute of Cytology, Russian Academy of Sciences, Saint Petersburg, Russia.
  • Dubey S Hintermann & Weber, Avenue des Alpes 25, 1820 Montreux, Switzerland; Department of Ecology and Evolution, Biophore Building, University of Lausanne, 1015 Lausanne, Switzerland; Agrosustain SA, Route de Duillier 50, 1260 Nyon, Switzerland.
  • Litvinchuk S Institute of Cytology, Russian Academy of Sciences, Saint Petersburg, Russia; Dagestan State University, Makhachkala, Russia.
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  • 2019-09-15
Published in:
  • Molecular phylogenetics and evolution. - 2019
Allopolyploidization
Bufonidae
Cryptic species
Green toads
Hybrid speciation
RAD sequencing
Animals
Biological Evolution
Bufonidae
DNA, Mitochondrial
Genetic Speciation
Genome Size
Genome, Mitochondrial
Genomics
Hybridization, Genetic
Mitochondria
Phenotype
Phylogeny
Phylogeography
Principal Component Analysis
Time Factors
English The radiation of Palearctic green toads (Bufotes) holds great potential to evaluate the role of hybridization in phylogeography at multiple stages along the speciation continuum. With fifteen species representing three ploidy levels, this model system is particularly attractive to examine the causes and consequences of allopolyploidization, a prevalent yet enigmatic pathway towards hybrid speciation. Despite substantial efforts, the evolutionary history of this species complex remains largely blurred by the lack of consistency among the corresponding literature. To get a fresh, comprehensive view on Bufotes phylogeography, here we combined genome-wide multilocus analyses (RAD-seq) with an extensive compilation of mitochondrial, genome size, niche modelling, distribution and phenotypic (bioacoustics, morphometrics, toxin composition) datasets, representing hundreds of populations throughout Eurasia. We provide a fully resolved nuclear phylogeny for Bufotes and highlight exceptional cyto-nuclear discordances characteristic of complete mtDNA replacement (in 20% of species), mitochondrial surfing during post-glacial expansions, and the formation of homoploid hybrid populations. Moreover, we traced the origin of several allopolyploids down to species level, showing that all were exclusively fathered by the West Himalayan B. latastii but mothered by several diploid forms inhabiting Central Asian lowlands, an asymmetry consistent with hypotheses on mate choice and Dobzhansky-Muller incompatibilities. Their intermediate call phenotypes potentially allowed for rapid reproductive isolation, while toxin compositions converged towards the ecologically-closest parent. Across the radiation, we pinpoint a stepwise progression of reproductive isolation through time, with a threshold below which hybridizability is irrespective of divergence (<6My), above which species barely admix and eventually evolve different mating calls (6-10My), or can successfully cross-breed through allopolyploidization (>15My). Finally, we clarified the taxonomy of Bufotes (including genetic analyses of type series) and formally described two new species, B. cypriensis sp. nov. (endemic to Cyprus) and B. perrini sp. nov. (endemic to Central Asia). Embracing the genomic age, our framework marks the advent of a new exciting era for evolutionary research in these iconic amphibians.
Language
  • English
Open access status
closed
Identifiers
Persistent URL
https://sonar.ch/global/documents/44286
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