Sexual Dichromatism Drives Diversification within a Major Radiation of African Amphibians

Author:

Portik Daniel M12,Bell Rayna C13,Blackburn David C4,Bauer Aaron M5,Barratt Christopher D678,Branch William R910,Burger Marius1112,Channing Alan13,Colston Timothy J1415,Conradie Werner916,Dehling J Maximilian17,Drewes Robert C18,Ernst Raffael1920,Greenbaum Eli21,Gvoždík Václav2223,Harvey James24,Hillers Annika2526,Hirschfeld Mareike25,Jongsma Gregory F M4,Kielgast Jos27,Kouete Marcel T4,Lawson Lucinda P2829,Leaché Adam D30,Loader Simon P31,Lötters Stefan32,Meijden Arie Van Der33,Menegon Michele34,Müller Susanne32,Nagy Zoltán T35,Ofori-Boateng Caleb36,Ohler Annemarie37,Papenfuss Theodore J1,Rößler Daniela32,Sinsch Ulrich17,Rödel Mark-Oliver25,Veith Michael32,Vindum Jens18,Zassi-Boulou Ange-Ghislain38,McGuire Jimmy A1

Affiliation:

1. Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720, USA

2. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA

3. Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560-0162, USA

4. Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA

5. Department of Biology, Villanova University, 800 Lancaster Avenue, Villanova, PA 19085, USA

6. Department of Environmental Sciences, University of Basel, Basel 4056, Switzerland

7. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig 0413, Germany

8. Max Planck Institute for Evolutionary Anthropology, Leipzig 0413, Germany

9. Port Elizabeth Museum, P.O. Box 11347, Humewood 6013, South Africa

10. Department of Zoology, Nelson Mandela Metropolitan University, P.O. Box 77000, Port Elizabeth 6031, South Africa

11. African Amphibian Conservation Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom 2520, South Africa

12. Flora Fauna & Man, Ecological Services Ltd. Tortola, British Virgin, Island

13. Unit for Environmental Sciences and Management, North-West University, Potchefstroom 2520, South Africa

14. Department of Biological Sciences, Florida State University, Tallahassee, FL 32306, USA

15. Zoological Natural History Museum, Addis Ababa University, Arat Kilo, Addis Ababa, Ethiopia

16. School of Natural Resource Management, Nelson Mandela University, George Campus, George 6530, South Africa

17. Department of Biology, Institute of Sciences, University of Koblenz-Landau, Universitätsstr. 1, D-56070 Koblenz, Germany

18. California Academy of Sciences, San Francisco, CA 94118, USA

19. Museum of Zoology, Senckenberg Natural History Collections Dresden, Königsbrücker Landstr. 159, Dresden 01109, Germany

20. Department of Ecology, Technische Universität Berlin, Rothenburgstr. 12, Berlin 12165, Germany

21. Department of Biological Sciences, University of Texas at El Paso, El Paso, TX 79968, USA

22. The Czech Academy of Sciences, Institute of Vertebrate Biology, Brno, Czech Republic

23. Department of Zoology, National Museum, Prague, Czech Republic

24. Pietermaritzburg, KwaZulu-Natal, South Africa

25. Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Biodiversity Dynamics, Invalidenstr. 43, Berlin 10115, Germany

26. Across 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

27. Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, Copenhagen 2100, Denmark

28. Department of Biological Sciences, University of Cincinnati, 614 Rieveschl Hall, Cincinnati, OH 45220, USA

29. Life Sciences, Field Museum of Natural History, 1400 S. Lake Shore Dr., Chicago, IL 60605, USA

30. Department of Biology, Burke Museum of Natural History and Culture, University of Washington, Seattle, WA, USA

31. Life Sciences Department, Natural History Museum, London SW7 5BD, UK

32. Biogeography Department, Trier University, Universitätsring 15, Trier 54296, Germany

33. CIBIO 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

34. Tropical Biodiversity Section, Science Museum of Trento, Corso del lavoro e della Scienza 3, Trento 38122, Italy

35. Royal Belgian Institute of Natural Sciences, OD Taxonomy and Phylogeny, Rue Vautier 29, B-1000 Brussels, Belgium

36. Forestry Research Institute of Ghana, P.O. Box 63, Fumesua, Kumasi, Ghana

37. Département Origines et Evolution, Muséum National d’Histoire Naturelle, UMR 7205 ISYEB, 25 rue Cuvier, Paris 75005, France

38. Institut National de Recherche en Sciences Exactes et Naturelles, Brazzaville BP 2400, République du Congo

Abstract

AbstractTheory 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 Afrobatrachia 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 that 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 micro- and macroevolutionary timescales.

Funder

National Science Foundation Doctoral Dissertation Improvement

National Science Foundation

UC Berkeley President’s Postdoctoral Fellowship

Museum of Vertebrate Zoology

NIH

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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