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Sexual Dichromatism Drives Diversification Within a Major Radiation of African Amphibians

View ORCID ProfileDaniel M. Portik, Rayna C. Bell, David C. Blackburn, Aaron M. Bauer, Christopher D. Barratt, William R. Branch, Marius Burger, Alan Channing, Timothy J. Colston, Werner Conradie, J. Maximillian Dehling, Robert C. Drewes, Raffael Ernst, Eli Greenbaum, Václav Gvoždík, James Harvey, Annika Hillers, Mareike Hirschfeld, Gregory F.M. Jongsma, Jos Kielgast, Marcel T. Kouete, Lucinda P. Lawson, Adam D. Leaché, Simon P. Loader, Stefan Lötters, Arie van der Meijden, Michele Menegon, Susanne Müller, Zoltán T. Nagy, Caleb Ofori-Boateng, Annemarie Ohler, Theodore J. Papenfuss, Daniela Rößler, Ulrich Sinsch, Mark-Oliver Rödel, Michael Veith, Jens Vindum, Ange-Ghislain Zassi-Boulou, Jimmy A. McGuire
doi: https://doi.org/10.1101/372250
Daniel M. Portik
1Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721 USA
2Museum of Vertebrate Zoology, University of California, Berkeley, California 94720, USA
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  • ORCID record for Daniel M. Portik
  • For correspondence: danielportik@email.arizona.edu
Rayna C. Bell
2Museum of Vertebrate Zoology, University of California, Berkeley, California 94720, USA
3Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560-0162 USA
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David C. Blackburn
4Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, USA
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Aaron M. Bauer
5Department of Biology, Villanova University, 800 Lancaster Avenue, Villanova, Pennsylvania 19085, USA
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Christopher D. Barratt
6Department of Environmental Sciences, University of Basel, Basel 4056, Switzerland
7German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, 0413 Leipzig, Germany
8Max Planck Institute for Evolutionary Anthropology, 0413 Leipzig, Germany
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William R. Branch
9Port Elizabeth Museum, P.O. Box 11347, Humewood 6013, South Africa
10Department of Zoology, P.O. Box 77000, Nelson Mandela Metropolitan University, Port Elizabeth 6031, South Africa
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Marius Burger
11African Amphibian Conservation Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom 2520, South Africa
12Flora Fauna & Man, Ecological Services Ltd. Tortola, British Virgin Island
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Alan Channing
13Unit for Environmental Sciences and Management, North-West University, Potchefstroom 2520, South Africa
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Timothy J. Colston
14Department of Biological Sciences, Florida State University, Tallahassee, FL 32306, USA
15Zoological Natural History Museum, Addis Ababa University, Arat Kilo, Addis Ababa, Ethiopia
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Werner Conradie
9Port Elizabeth Museum, P.O. Box 11347, Humewood 6013, South Africa
16School of Natural Resource Management, George Campus, Nelson Mandela University, George 6530, South Africa
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J. Maximillian Dehling
17Institute of Sciences, Department of Biology, University of Koblenz-Landau, Universitätsstr. 1, D-56070 Koblenz, Germany
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Robert C. Drewes
18California Academy of Sciences, San Francisco, California 94118, USA
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Raffael Ernst
19Museum of Zoology, Senckenberg Natural History Collections Dresden, Königsbrücker Landstr. 159, 01109 Dresden, Germany
20Department of Ecology, Technische Universität Berlin, Rothenburgstr. 12, 12165 Berlin, Germany
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Eli Greenbaum
21Department of Biological Sciences, University of Texas at El Paso, El Paso, TX 79968, USA
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Václav Gvoždík
22The Czech Academy of Sciences, Institute of Vertebrate Biology, Brno, Czech Republic
23National Museum, Department of Zoology, Prague, Czech Republic
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James Harvey
24Pietermaritzburg, KwaZulu-Natal, South Africa
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Annika Hillers
25Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Biodiversity Dynamics, Invalidenstr. 43, 10115 Berlin, Germany
26Across the River – a Transboundary Peace Park for Sierra Leone and Liberia, The Royal Society for the Protection of Birds, 164 Dama Road, Kenema, Sierra Leone
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Mareike Hirschfeld
25Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Biodiversity Dynamics, Invalidenstr. 43, 10115 Berlin, Germany
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Gregory F.M. Jongsma
4Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, USA
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Jos Kielgast
27Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark
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Marcel T. Kouete
4Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, USA
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Lucinda P. Lawson
28University of Cincinnati, Department of Biological Sciences, 614 Rieveschl Hall, Cincinnati OH 45220, USA.
29Life Sciences, Field Museum of Natural History, 1400 S. Lake Shore Dr., Chicago IL, 60605 USA.
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Adam D. Leaché
30Department of Biology and Burke Museum of Natural History and Culture, University of Washington, Seattle, Washington, USA
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Simon P. Loader
31Life Sciences Department, Natural History Museum, London SW7 5BD, UK.
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Stefan Lötters
32Trier University, Biogeography Department, Universitätsring 15, 54295 Trier, Germany
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Arie van der Meijden
33CIBIO Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto, Campus Agrario de Vairão, Rua Padre Armando Quintas, No. 7, 4485-661 Vairão, Vila do Conde, Portugal
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Michele Menegon
34Tropical Biodiversity Section, Science Museum of Trento, Corso del lavoro e della Scienza 3, 38122 Trento, Italy
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Susanne Müller
32Trier University, Biogeography Department, Universitätsring 15, 54295 Trier, Germany
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Zoltán T. Nagy
35Royal Belgian Institute of Natural Sciences, OD Taxonomy and Phylogeny, Rue Vautier 29, B-1000 Brussels, Belgium
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Caleb Ofori-Boateng
36Forestry Research Institute of Ghana, P.O. Box 63, Fumesua, Kumasi, Ghana
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Annemarie Ohler
37Muséum National d’Histoire Naturelle, Département Origines et Evolution, UMR 7205 ISYEB, 25 rue Cuvier, 75005 Paris, France
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Theodore J. Papenfuss
2Museum of Vertebrate Zoology, University of California, Berkeley, California 94720, USA
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Daniela Rößler
32Trier University, Biogeography Department, Universitätsring 15, 54295 Trier, Germany
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Ulrich Sinsch
17Institute of Sciences, Department of Biology, University of Koblenz-Landau, Universitätsstr. 1, D-56070 Koblenz, Germany
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Mark-Oliver Rödel
25Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Biodiversity Dynamics, Invalidenstr. 43, 10115 Berlin, Germany
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Michael Veith
32Trier University, Biogeography Department, Universitätsring 15, 54295 Trier, Germany
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Jens Vindum
18California Academy of Sciences, San Francisco, California 94118, USA
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Ange-Ghislain Zassi-Boulou
38Institut National de Recherche en Sciences Exactes et Naturelles, BP 2400 Brazzaville, République du Congo
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Jimmy A. McGuire
2Museum of Vertebrate Zoology, University of California, Berkeley, California 94720, USA
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ABSTRACT

Theory predicts that sexually dimorphic traits under strong sexual selection, particularly those involved with intersexual signaling, can accelerate speciation and produce bursts of diversification. Sexual dichromatism (sexual dimorphism in color) is widely used as a proxy for sexual selection and is associated with rapid diversification in several animal groups, yet studies using phylogenetic comparative methods to explicitly test for an association between sexual dichromatism and diversification have produced conflicting results. Sexual dichromatism is rare in frogs, but it is both striking and prevalent in African reed frogs, a major component of the diverse frog radiation termed Afrobatrachia. In contrast to most other vertebrates, reed frogs display female-biased dichromatism in which females undergo color transformation, often resulting in more ornate coloration in females than in males. We produce a robust phylogeny of Afrobrachia to investigate the evolutionary origins of sexual dichromatism in this radiation and examine whether the presence of dichromatism is associated with increased rates of net diversification. We find that sexual dichromatism evolved once within hyperoliids and was followed by numerous independent reversals to monochromatism. We detect significant diversification rate heterogeneity in Afrobatrachia and find that sexually dichromatic lineages have double the average net diversification rate of monochromatic lineages. By conducting trait simulations on our empirical phylogeny, we demonstrate our inference of trait-dependent diversification is robust. Although sexual dichromatism in hyperoliid frogs is linked to their rapid diversification and supports macroevolutionary predictions of speciation by sexual selection, the function of dichromatism in reed frogs remains unclear. We propose that reed frogs are a compelling system for studying the roles of natural and sexual selection on the evolution of sexual dichromatism across both micro- and macroevolutionary timescales.

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Sexual Dichromatism Drives Diversification Within a Major Radiation of African Amphibians
Daniel M. Portik, Rayna C. Bell, David C. Blackburn, Aaron M. Bauer, Christopher D. Barratt, William R. Branch, Marius Burger, Alan Channing, Timothy J. Colston, Werner Conradie, J. Maximillian Dehling, Robert C. Drewes, Raffael Ernst, Eli Greenbaum, Václav Gvoždík, James Harvey, Annika Hillers, Mareike Hirschfeld, Gregory F.M. Jongsma, Jos Kielgast, Marcel T. Kouete, Lucinda P. Lawson, Adam D. Leaché, Simon P. Loader, Stefan Lötters, Arie van der Meijden, Michele Menegon, Susanne Müller, Zoltán T. Nagy, Caleb Ofori-Boateng, Annemarie Ohler, Theodore J. Papenfuss, Daniela Rößler, Ulrich Sinsch, Mark-Oliver Rödel, Michael Veith, Jens Vindum, Ange-Ghislain Zassi-Boulou, Jimmy A. McGuire
bioRxiv 372250; doi: https://doi.org/10.1101/372250
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Sexual Dichromatism Drives Diversification Within a Major Radiation of African Amphibians
Daniel M. Portik, Rayna C. Bell, David C. Blackburn, Aaron M. Bauer, Christopher D. Barratt, William R. Branch, Marius Burger, Alan Channing, Timothy J. Colston, Werner Conradie, J. Maximillian Dehling, Robert C. Drewes, Raffael Ernst, Eli Greenbaum, Václav Gvoždík, James Harvey, Annika Hillers, Mareike Hirschfeld, Gregory F.M. Jongsma, Jos Kielgast, Marcel T. Kouete, Lucinda P. Lawson, Adam D. Leaché, Simon P. Loader, Stefan Lötters, Arie van der Meijden, Michele Menegon, Susanne Müller, Zoltán T. Nagy, Caleb Ofori-Boateng, Annemarie Ohler, Theodore J. Papenfuss, Daniela Rößler, Ulrich Sinsch, Mark-Oliver Rödel, Michael Veith, Jens Vindum, Ange-Ghislain Zassi-Boulou, Jimmy A. McGuire
bioRxiv 372250; doi: https://doi.org/10.1101/372250

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