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 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.

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

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

Biogeography Department Trier University Universitätsring 15 Trier 54296 Germany

California Academy of Sciences San Francisco CA 94118 USA

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

Département Origines et Evolution Muséum National d'Histoire Naturelle UMR 7205 ISYEB 25 rue Cuvier Paris 75005 France

Department of Biological Sciences Florida State University Tallahassee FL 32306 USA

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

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

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

Department of Biology Institute of Sciences University of Koblenz Landau Universitätsstr 1 D 56070 Koblenz Germany

Department of Biology Villanova University 800 Lancaster Avenue Villanova PA 19085 USA

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

Department of Ecology Technische Universität Berlin Rothenburgstr 12 Berlin 12165 Germany

Department of Environmental Sciences University of Basel Basel 4056 Switzerland

Department of Vertebrate Zoology National Museum of Natural History Smithsonian Institution Washington DC 20560 0162 USA

Department of Zoology National Museum Prague Czech Republic

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

Flora Fauna and Man Ecological Services Ltd Tortola British Virgin Island

Florida Museum of Natural History University of Florida Gainesville FL 32611 USA

Forestry Research Institute of Ghana P O Box 63 Fumesua Kumasi Ghana

German Centre for Integrative Biodiversity Research Halle Jena Leipzig Leipzig 0413 Germany

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

Life Sciences Department Natural History Museum London SW7 5BD UK

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

Max Planck Institute for Evolutionary Anthropology Leipzig 0413 Germany

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

Museum of Vertebrate Zoology University of California Berkeley CA 94720 USA

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

Natural History Museum of Denmark University of Copenhagen Universitetsparken 15 Copenhagen 2100 Denmark

Pietermaritzburg KwaZulu Natal South Africa

Port Elizabeth Museum P O Box 11347 Humewood 6013 South Africa

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

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

The Czech Academy of Sciences Institute of Vertebrate Biology Brno Czech Republic

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

Unit for Environmental Sciences and Management North West University Potchefstroom 2520 South Africa

Zoological Natural History Museum Addis Ababa University Arat Kilo Addis Ababa Ethiopia

Zobrazit více v PubMed

Ahl E. 1931. Amphibia, Anura III, Polypedatidae. Das Tierreich 55:xvi + 477.

Akopyan M., Kaiser K., Vega A., Savant N.G., Owen C.Y., Dudgeon S.R., Robertson J.M.. 2018. Melodic males and flashy females: geographic variation in male and female reproductive behavior in red-eyed treefrogs (Agalychnis callidryas). Ethology 124:54-64.

Alfaro M.E., Brock C.D., Banbury B.L., Wainwright P.C.. 2009. Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fishes? BMC Evol. Biol. 9:255. PubMed PMC

Aljanabi S., Martinez I.. 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res. 25:4692–4693. PubMed PMC

Amiet J.-L. 2012. Les Rainettes du Cameroun (Amphibiens Anoures). Saint-Nazaire, France: La Nef des Livres; 591 pp.

AmphibiaWeb. 2019. Available at: amphibiaweb.org. University of California, Berkeley; Accessed May 2018.

Andersson M. 1994. Sexual selection. Princeton (NJ): Princeton University Press.

Backwell P.R.Y., Passmore N.I.. 1990. Aggressive interactions and intermale spacing in choruses of the leaf-folding frog, Afrixalus delicatus. S. Afr. J. Zool. 25:133–137.

Baele G., Lemey P., Bedford T., Rambaut A., Suchard M.A., Alekseyenko A.V.. 2012. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol. Biol. Evol. 29:2157–2167. PubMed PMC

Baele G., Li W.L.S., Drummond A.J., Suchard M.A., Lemey P.. 2013. Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Mol. Biol. Evol. 30:239–243. PubMed PMC

Barraclough T.G., Harvey P.H., Nee S.. 1995. Sexual selection and taxonomic diversity in passerine birds. Proc. R. Soc. Lon. B 259:211–215.

Barratt C.D., Lawson L.P., Bittencourt-Silva G.B., Doggart N., Morgan-Brown T., Nagel P., Loader S.P.. 2017. A new, narrowly distributed, and critically endangered species of spiny-throated reed frog (Anura: Hyperoliidae) from a highly threatened coastal forest reserve in Tanzania. Herpetol. J. 27:13–24.

Beaulieu J.M., O’Meara B.C.. 2016. Detecting hidden diversification shifts in models of trait-dependent speciation and extinction. Syst. Biol. 65:583–601. PubMed

Bell R.C., Parra J.L., Badjedjea G., Barej M.F., Blackburn D.C., Burger M., Channing A., Dehling J.M., Greenbaum E., Gvoždík V., Kielgast J., Kusamba C., Lötters S., McLaughlin P.J., Nagy Z.T., Rödel M.-O., Portik D.M., Stuart B.L., VanDerWal J., Zamudio K.R.. 2017a. Idiosyncratic responses to climate-driven forest fragmentation and marine incursions in reed frogs from Central Africa and the Gulf of Guinea Islands. Mol. Ecol. 26:5223–5224. PubMed

Bell R.C., Webster G.N., Whiting M.J.. 2017b. Breeding biology and the evolution of dynamic sexual dichromatism in frogs. J. Evol. Biol. 30:2104–2115. PubMed

Bell R.C., Zamudio K.R.. 2012. Sexual dichromatism in frogs: natural selection, sexual selection and unexpected diversity. Proc. R. Soc. Lon. B 279:4687–4693. PubMed PMC

Berglund A., Rosenqvist G., Svensson I.. 1986a. Reversed sex roles and parental energy investment in zygotes of two pipefish (Syngnathidae) species. Mar. Ecol. Prog. Ser. 29:209–215.

Berglund A., Rosenqvist G., Svensson I.. 1986b. Mate choice, fecundity and sexual dimorphism in two pipefish species (Syngnathidae). Behav. Ecol. Sociobiol. 19:301–307.

Bi K., Vanderpool D., Singhal S., Linderoth T., Moritz C., Good J.M.. 2012. Transcriptome-based exon capture enables highly cost-effective comparative genomic data collection at moderate evolutionary scales. BMC Genomics 13:403. PubMed PMC

Bishop P.J., Jennions M.D., Passmore N.I.. 1995. Chorus size and call intensity: female choice in the painted reed frog, Hyperolius marmoratus. Behaviour 132:721–731.

Blaimer B.B., Mawdsley J.R., Brady S.G.. 2018. Multiple origins of sexual dichromatism and aposematism within large carpenter bees. Evolution 72:1874–1889. PubMed

Burnham K.P., Anderson D.R.. 2002. Model selection and multimodel inference: a practical information-theoretic approach. New York: Springer.

Burns K. 1998. A phylogenetic perspective on the evolution of sexual dichromatism in tanagers (Thraupidae): the role of female versus male plumage. Evolution 52:1219–1224. PubMed

Capella-Gutierrez S., Silla-Martinez J.M., Gabaldon T.. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973. PubMed PMC

Channing A. 2001. Amphibians of central and southern Africa. Ithaca (NY): Cornell University Press.

Channing A., Hillers A., Lötters S., Rödel M.-O., Schick S., Conradie W., Rödder D., Mercurio V., Wagner P., Dehling J.M., du Preez L.H., Kielgast J., Burger M.. 2013. Taxonomy of the super-cryptic Hyperolius nasutus group of long reed frogs of Africa (Anura: Hyperoliidae), with descriptions of six new species. Zootaxa 3620:301–350. PubMed

Channing A., Howell K.M.. 2006. Amphibians of East Africa. Frankfurt, Germany: Edition Chimaira.

Conradie W., Branch W.R., Measey G.J., Tolley K.A.. 2012. A new species of Hyperolius Rapp, 1842 (Anura: Hyperoliidae) from the Serra da Chela mountains, south-western Angola. Zootaxa 3269:1–17.

Conradie W., Branch W.R., Tolley K.A.. 2013. Fifty shades of grey: giving colour to the poorly known Angolan Ashy reed frog (Hyperoliidae: Hyperolius cinereus), with the description of a new species. Zootaxa 3635:201–223. PubMed

Conradie W., Verbugt L., Portik D.M., Ohler A., Bwong B.A., Lawson L.P.. 2018. A new reed frog (Hyperoliidae: Hyperolius) from coastal northeastern Mozambique. Zootaxa 4379:177-198. PubMed

Daly J.W. 1995. The chemistry of poisons in amphibian skin In: Eisner T., Meinwald J., editors. Chemical ecology: the chemistry of biotic interaction. Washington (DC): National Academy Press; p. 17–28.

Darwin C.R. 1871. The descent of man, and selection in relation to sex. Vol. 1 1st ed. London: John Murray.

De Lisle S.P., Rowe L.. 2013. Correlated evolution of allometry and sexual dimorphism across higher taxa. Am. Na.t 183:630–639. PubMed

Dehling J.M. 2012. An African glass frog: a new Hyperolius species (Anura: Hyperoliidae) from Nyungwe National Park, southern Rwanda. Zootaxa 3391:52–64.

Dominey W. 1984. Effects of sexual selection and life history on speciation: species flocks in African cichlids and Hawaiian Drosophila In: Echelle A.A., Kornfield I., editors. Evolution of fish species flocks. Orono: University of Maine Press; p. 231–249.

Drewes R.C., Vindum J.V.. 1994. Amphibians of the impenetrable forest, Southwest Uganda. J. Afr. Zool. 108:55–70.

Drummond A.J., Suchard M.A., Xie D., Rambaut A.. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29:1969–1973. PubMed PMC

Duellman W.E., Trueb L.. 1986. Biology of amphibians. New York (NY): McGraw-Hill.

Dunn P.O., Armenta J.K., Whittingham L.A.. 2015. Natural and sexual selection act on different axes of variation in avian plumage color. Sci. Adv. 1:e1400155. PubMed PMC

Dyson M.L., Passmore N.I.. 1988. Two-choice phonotaxis in Hyperolius marmoratus (Anura: Hyperoliidae): the effect of temporal variation in presented stimuli. Anim. Behav. 36:648–652.

Dyson M.L., Passmore N.I., Bishop P.J., Henzi S.P.. 1992. Male behavior and correlates of mating success in a natural population of African painted reed frogs (Hyperolius marmoratus). Herpetologica 48:236–246.

Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792–1797. PubMed PMC

Eens M., Pinxten R.. 2000. Sex-role reversal in vertebrates: behavioural and endocrinological accounts. Behav. Process 51:135–147. PubMed

Feng Y.-J., Blackburn D.C., Liang D., Hillis D.M., Wake D.B., Cannatella D.C., Zhang P.. 2017. Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous-Paleogene boundary. Proc. Natl. Acad. Sci. USA 114:E5864–E5870. PubMed PMC

FitzJohn R.G. 2012. Diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3:1084–1092.

FitzJohn R.G., Maddison W.P., Otto S.P.. 2009. Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Syst. Biol. 58:595–611. PubMed

Gerhardt H.C. 1994. The evolution of vocalization in frogs and toads. Annu. Rev. Ecol. Syst. 25:233–324.

Gerhardt H.C., Huber F.. 2002. Acoustic communication in insects and anurans: common problems and diverse solutions. Chicago (IL): The University of Chicago Press.

Gilbert C.M., Bell R.C.. 2018. Evolution of advertisement calls in an island radiation of African reed frogs. Biol. J. Linn. Soc. 123:1–11.

Gomez D., Richardson C., Lengagne T., Derex M., Plenet S., Joly P., Léna J.-P., Théry M.. 2010. Support for a role of colour vision in mate choice in the nocturnal European treefrog. Behaviour 147:1753–1768.

Gomez D., Richardson C., Lengagne T., Plenet S., Joly P., Léna J.-P., Théry M.. 2009. The role of nocturnal vision in mate choice: females prefer conspicuous males in the European tree frog (Hyla arborea). Proc. Biol. Sci. 276:2351–2358. PubMed PMC

Grafe T.U. 1997. Costs and benefits of mate choice in the lek-breeding reed frog, Hyperolius marmoratus. Anim. Behav. 53:1103–1117.

Greenbaum E., Sinsch U., Lehr E., Valdez F., Kusamba C.. 2013. Phylogeography of the reed frog Hyperolius castaneus (Anura: Hyperoliidae) from the Albertine Rift of Central Africa: implications for taxonomy, biogeography and conservation. Zootaxa 3131:473–494. PubMed

Han X., Fu J.. 2013. Does life history shape sexual size dimorphism in anurans? A comparative analysis. BMC Evol. Biol. 13:27. PubMed PMC

Harrington S., Reeder T.W.. 2017. Rate heterogeneity across Squamata, misleading ancestral state reconstruction and the importance of proper null model specification. J. Evol. Biol. 30:313–325. PubMed

Hayes T.B. 1997. Hormonal mechanisms as potential constraints on evolution: examples from the Anura. Am. Zool. 37:482–490.

Hayes T.B., Menendez K.P.. 1999. The effect of sex steroids on primary and secondary sex differentiation in the sexually dichromatic reedfrog (Hyperolius argus: Hyperolidae) from the Arabuko Sokoke forest of Kenya. Gen. Comp. Endocr. 115:188–199. PubMed

Heinsohn R., Legge S., Endler J.A.. 2005. Extreme reversed sexual dichromatism in a bird without sex role reversal. Science 309:617–619. PubMed

Hofmann C.M., Cronin T.W., Omland K.E.. 2008. Evolution of sexual dichromatism. 1. Convergent losses of elaborate female coloration in New World orioles (Icterus spp.). Auk 125:778–789.

Huang H., Rabosky D.L.. 2014. Sexual selection and diversification: reexamining the correlation between dichromatism and speciation rate in birds. Am. Nat. 184(5):E104–E114. PubMed

Jacobs L.E., Vega A., Dudgeon S., Kaiser K., Robertson J.M.. 2016. Local not vocal: assortative female choice in divergent populations of red-eyed treefrogs, Agalychnis callidryas (Hylidae: Phyllomedusinae). Biol. J. Linn. Soc. 120:171–178.

Jeckel A.M., Grant T., Saporito R.A.. 2015. Sequestered and synthesized chemical defenses in the poison frog Melanophryniscus moreirae. J. Chem. Ecol. 41:505–512. PubMed

Jennions M.D., Bishop P.J., Backwell P.R.Y., Passmore N.I.. 1995. Call rate variability and female choice in the African frog, Hyperolius marmoratus. Behaviour 132:709–720.

Johnson A.E., Price J.J., Pruett-Jones S.. 2013. Different modes of evolution in males and females generate dichromatism in fairy-wrens (Maluridae). Ecol. Evol. 3:3030–3046. PubMed PMC

Katoh K., Standley D.M.. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30:722–780. PubMed PMC

Katoh K., Kuma K., Toh H., Miyata T.. 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33:511–518. PubMed PMC

Katoh K., Misawa K., Kuma K., Miyata T.. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30:3059–3066. PubMed PMC

Kazancıoglu E., Near T.J., Hanel R., Wainwright P.C.. 2009. Influence of sexual selection and feeding functional morphology on diversification rate of parrotfishes. Proc. R. Soc. B. 276:3439–3446. PubMed PMC

Kimball R.T., Braun E.L., Ligon J.D., Lucchini V., Randi E.. 2001. A molecular phylogeny of the peacock-pheasants (Galliformes: Polyplectron spp.) indicates loss and reduction of ornamental traits and display behaviours. Biol. J. Linn. Soc. 73:187–198.

Kimball R.T., Ligon J.D.. 1999. Evolution of avian plumage dichromatism from a proximate perspective. Am. Nat. 154:182–193.

Kindermann C., Hero J.-M.. 2016. Rapid dynamic colour change is an intrasexual signal in a lek breeding frog (Litoria wilcoxii). Behav. Ecol. Sociobiol. 70:1995–2003.

King B., Lee M.S.Y.. 2015. Ancestral state reconstruction, rate heterogeneity, and the evolution of reptile viviparity. Syst. Biol. 64:532–544. PubMed

Kirkpatrick M. 1982. Sexual selection and the evolution of female choice. Evolution 36:1–12. PubMed

Kouamé A.M., Kouamé N’.G.G., Konan J.C.B.Y.N’G, Adepo-Gourène B., Rödel M.-O.. 2015. Contributions to the reproductive biology and behaviour of the dotted reed frog, Hyperolius guttulatus, in southern-central Ivory Coast, West Africa. Herpetol. Notes 8:633–641.

Kouamé N’.G.G., Boateng C.O., Rödel M.-O.. 2013. A rapid survey of the amphibians from the Atewa Range Forest Reserve, Eastern Region, Ghana In: Conservation International , editor. A rapid biological assessment of the Atewa Range Forest Reserve, Eastern Ghana. Conservation International Arlington, Virginia: p. 76–83.

Kraaijeveld K., Kraaijeveld-Smit F.J.L., Maan M.E.. 2011. Sexual selection and speciation: the comparative evidence revisited. Biol. Rev. 86:367–377. PubMed

Kurabayashi A., Sumida M.. 2013. Afrobatrachian mitochondrial genomes: genome reorganization, gene rearrangement mechanisms, and evolutionary trends of duplicated and rearranged genes. BMC Genomics 14:633. PubMed PMC

Lande R. 1981. Models of speciation by sexual selection on polygenic traits. Proc. Natl. Acad. Sci. USA 78:3721–3725. PubMed PMC

Lande R. 1982. Rapid origin of sexual isolation and character displacement in a cline. Evolution 36:213–223. PubMed

Lewis P.O. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50:913–925. PubMed

Liedtke H.C., Hügil D., Dehling J.M., Pupin F., Menegon M., Plumptre A.J., Kujirakwinja D., Loader S.P.. 2014. One or two species? On the case of Hyperolius discodactylus Ahl, 1931 and H. alticola Ahl, 1931 (Anura: Hyperoliidae). Zootaxa 3768:253–290. PubMed

Liu L., Yu L., Edwards S.V.. 2010. A maximum pseudo-likelihood approach for estimating species trees under the coalescent model. BMC Evol. Biol. 10:302. PubMed PMC

Loader S.P., Ceccarelli F.S., Menegon M., Howell K.M., Kassahun R., Mengistu A.A., Saber S.A., Gebresenbet F., de Sa R., Davenport T.R.B., Larson J.G., Müller H., Wilkinson M., Gower D.J.. 2014. Persistence and stability of Eastern Afromontane forests: evidence from brevicipitid frogs. J. Biogeogr. 41:1781–1792.

Loader S.P., Lawson L.P., Portik D.M., Menegon M.. 2015. Three new species of spiny throated reed frogs (Anura: Hyperoliidae) from evergreen forests of Tanzania. BMC Res. Notes 8:167. PubMed PMC

Luiselli L., Bikikoro L., Odegbune E., Wariboko S.M., Rugiero L., Akani G.C., Politano E.. 2004. Feeding relationships between sympatric Afrotropical frogs (genus Hyperolius): the effects of predator body size and season. Anim. Biol. 54:293–302.

Maan M.E., Cummings M.E.. 2009. Sexual dimorphism and directional sexual selection on aposematic signals in a poison frog. Proc. Natl. Acad. Sci. USA. 106:19072–19077. PubMed PMC

Maddison W.P., Midford P.E., Otto S.P.. 2007. Estimating a binary character’s effect on speciation and extinction. Syst. Biol. 56:701–710. PubMed

McDiarmid R.W. 1975. Glass frog romance along a tropical stream. Nat. Hist. Mus. Los Angeles Co Terra 13(4):14–18.

Mendelson T.C., Shaw K.L.. 2012. The (mis)concept of species recognition. Trends Ecol. Evol. 27:421–427. PubMed

Meyer M., Kircher M.. 2010. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb. Protoc. 2010:pdb.prot5448. PubMed

Mirarab S., Reaz R., Bayzid M.D.S., Zimmermann T., Swenson M.S., Warnow T.. 2014. ASTRAL: genome-scale coalescent-based species tree estimation. Bioinformatics 30:i541–i548. PubMed PMC

Mirarab S., Warnow T.. 2015. ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31:i44–i52. PubMed PMC

Misof B. 2002. Diversity of Anisoptera (Odonata): inferring speciation processes from patterns of morphological diversity. Zoology 105:355–365. PubMed

Morrow E.H., Pitcher T.E., Anrqvist G.. 2003. No evidence that sexual selection is an `engine of speciation’ in birds. Ecol. Lett. 6:228–234.

Nali R.C., Zamudio K.R., Haddad C.F.B., Prado C.P.A.. 2014. Size-dependent selective mechanisms on males and females and the evolution of sexual size dimorphism in frogs. Am. Nat. 184:727–740. PubMed

Omland K.E. 1997. Examining two standard assumptions of ancestral reconstructions: repeated loss of dichromatism in dabbling ducks. Evolution 51:1636–1646. PubMed

Oring L.W. 1982. Avian mating systems In: Farner DS, King JS, Parkes KC, editors. Avian Biology. New York (NY): Academic Press; p. 1–92.

Owens I.P.F., Bennett P.M., Harvey P.H.. 1999. Species richness among birds: body size, life history, sexual selection or ecology? Proc. R. Soc. Lon. B 266:933–939.

Palumbi S., Martin A., Romano S., McMillan W.O., Stice L., Grabowski G.. 1991. The simple fool’s guide to PCR. Version 2. Honolulu: University of Hawaii.

Panhuis T.M., Butlin R., Zuk M., Tregenza T.. 2001. Sexual selection and speciation. Trends Ecol. Evol. 16:364–371. PubMed

Paradis E., Claude J., Strimmer K.. 2004. APE: analysis of phylogenetics and evolution in R language. Bioinformatics 20:289–290. PubMed

Phillimore A.B., Freckleton R.P., Orme C.D.L., Owens I.P.F.. 2006. Ecology predicts large-scale patterns of phylogenetic diversification in birds. Am. Nat. 168:220–229. PubMed

Portik D.M. 2015. Diversification of afrobatrachian frogs and the herpetofauna of the Arabian Peninsula [PhD Thesis]. Berkeley (CA): University of California.

Portik D.M., Blackburn D.C.. 2016. The evolution of reproductive diversity in Afrobatrachia: a phylogenetic comparative analysis of an extensive radiation of African frogs. Evolution 70: 2017–2032. PubMed PMC

Portik D.M., Jongsma G.F., Kouete M.T., Scheinberg L.A., Freiermuth B., Tapondjou W.P., Blackburn D.C. 2016a. A survey of amphibians and reptiles in the foothills of Mount Kupe, Cameroon. Amphib. Reptile Conserv. 10(2)[Special Section]:37–67(e131).

Portik D.M., Jongsma G.F., Kouete M.T., Scheinberg L.A., Freiermuth B., Tapondjou W.P., Blackburn D.C.. 2018. Ecological, morphological, and reproductive aspects of a diverse assemblage of hyperoliid frogs (Family: Hyperoliidae) surrounding Mt. Kupe, Cameroon. Herpetol. Rev. 49:397–408.

Portik D.M., Scheinberg L., Blackburn D.C., Saporito R.A.. 2015. Lack of defensive alkaloids in the integumentary tissue of four brilliantly colored African reed frog species (Hyperoliidae: Hyperolius). Herpetol. Conserv. Biol. 10:833–838.

Portik D.M., Smith L.L., Bi K.. 2016b. An evaluation of transcriptome-based exon capture for frog phylogenomics across multiple scales of divergence (Class: Amphibia, Order: Anura). Mol. Ecol. Resour. 16:1069–1083. PubMed

Portik D.M., Smith L.L., Bi K.. 2016c. Data from: An evaluation of transcriptome-based exon capture for frog phylogenomics across multiple scales of divergence (Class: Amphibia, Order: Anura). Dryad Digital Repository. 10.5061/dryad.pr3pr PubMed DOI

Price J.J., Eaton M.D.. 2014. Reconstructing the evolution of sexual dichromatism: current color diversity does not reflect past rates of male and female change. Evolution 68:2026–2037. PubMed

Price T. 2008. Sexual selection and natural selection in bird speciation. Phil. Trans. R. Soc. Lond. B 353:251–260.

Price T., Birch G.L.. 1996. Repeated evolution of sexual color dimorphism in passerine birds. Auk 113:842–848.

Pyron R.A., Wiens J.J.. 2011. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol. Phylogenet. Evol. 61:543–583. PubMed

Rabosky D.L., Goldberg E.E.. 2015. Model inadequacy and mistaken inferences of trait-dependent speciation. Syst. Biol. 64:340–355. PubMed

Rambaut A., Drummond A.J., Suchard M.. 2013. Tracer v1.6.0. Available from: http://beast.bio.ed.ac.uk/

Revell L.J. 2012. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3:217–223.

Richards C.M. 1982. The alteration of chromatophore expression by sex hormones in the Kenyan Reed Frog, Hyperolius viridiflavus. Gen. Comp. Endocr. 46:59–67. PubMed

Ritchie M.G. 2007. Sexual selection and speciation. Ann. Rev. Ecol. Evol. Syst. 38:79–102.

Rödel M.-O., Grafe T.U., Rudolf V.H.W., Ernst R.. 2002. A review of West African spotted Kassina, including a description of Kassina schioetzi sp. nov. (Amphibia: Anura: Hyperoliidae). Copeia 2002:800–814.

Rödel M.-O., Kosuch J., Grafe T.U., Boistel R., Assemian N.E., Kouamé N.G., Tohé B., Gourène G., Perret J.-L., Henle K., Tafforeau P., Pollet N., Veith M.. 2009. A new tree-frog genus and species from Ivory Coast, West Africa (Amphibia: Anura: Hyperoliidae). Zootaxa 2044:23–45.

Rödel M.-O., Kosuch J., Veith M., Ernst R.. 2003. First record of the genus Acanthixalus Laurent, 1944 from the Upper Guinean Rain Forest, West Africa, with the description of a new species. J. Herpetol. 37:43–52.

Rödel M.-O., Sandberger L., Penner J., Mané Y., Hillers A.. 2010. The taxonomic status of Hyperolius spatzi Ahl, 1931 and Hyperolius nitidulus Peters, 1875 (Amphibia: Anura: Hyperoliidae). Bonn. Zool. Bull. 57:177–188.

Roede M. 1972. Color as related to size, sex and behavior in seven Caribbean labrid fish species (genera Thalasoma, Halichoeres and Hemipteronotus). Studies on the Fauna of Curacao and other Caribbean Islands 42:1–266.

Roelants K., Gower D.J., Wilkinson M., Loader S.P., Biju S.D., Guillaume K., Moriau L., Bossuyt F.. 2007. Global patterns of diversification in the history of modern amphibians. Proc. Natl. Acad. Sci. USA 104:887–892. PubMed PMC

Rojas B. 2017. Behavioural, ecological, and evolutionary aspects of diversity in frog colour patterns. Biol. Rev. 92:1059–1080. PubMed

Ryan M.J. 1980. Female choice in a Neotropical frog. Science 209:523–525. PubMed

Safran R.J., Scordato E.S.C., Symes L.B., Rodríguez R.L., Mendelson T.C.. 2013. Contributions of natural and sexual selection to the evolution of premating reproductive isolation: a research agenda. Trends Ecol. Evol. 28:643–650. PubMed

Salthe S.N., Duellman W.E.. 1973. Quantitative constraints associated with reproductive mode in anurans In: Vial J.L., editor. Evolutionary Biology of the Anurans. Missouri: University of Missouri Press; p. 229–249.

Sanderson M.J. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19:101–109. PubMed

Saporito R.A., Donnelly M.A., Madden A.A., Garraffo H.M., Spande T.F.. 2010. Sex-related differences in alkaloid defenses of the dendrobatid frog Oophaga pumilio from Cayo Nancy, Bocas del Toro, Panama. J. Nat. Prod. 73:317–321. PubMed PMC

Saporito R.A., Donnelly M.A., Spande T.F., Garraffo H.M.. 2012. A review of chemical ecology in poison frogs. Chemoecology 22:159–168.

Sayyari E., Mirarab S. 2016. Fast coalescent-based computation of local branch support from quartet frequencies. Mol. Biol. Evol. 33:1654–1668. PubMed PMC

Schick S., Kielgast J., Rödder D., Muchai V., Burger M., Lötters S.. 2010. New species of reed frog from the Congo Basin with discussion of paraphyly in cinnamon-belly reed frogs. Zootaxa 2501:23–36.

Schiøtz A. 1967. The treefrogs (Rhacophoridae) of West Africa. Spolia Zoologica Musei Hauniensis 25:1–346.

Schiøtz A. 1999. Treefrogs of Africa. Frankfurt, Germany: Edition Chimaira.

Seddon N., Botero C.A., Tobias J.A., Dunn P.O., MacGregor H.E.A., Rubenstein D.R., Uy A.C., Weir J.T., Whittingham L.A., Safran R.J.. 2013. Sexual selection accelerates signal evolution during speciation in birds. Proc. Biol. Sci. 280:20131065. PubMed PMC

Selander R.K. 1966. Sexual dimorphism and differential niche utilization in birds. Condor 68:113–151.

Seo T.-K. 2008. Calculating bootstrap probabilities of phylogeny using multilocus sequence data. Mol. Biol. Evol. 25:960–971. PubMed

Shine R. 1979. Sexual selection and sexual dimorphism in the Amphibia. Copeia 1979:297–306.

Shine R. 1989. Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q. Rev. Biol. 64:419–461. PubMed

Shultz A.J., Burns K.J.. 2017. The role of sexual and natural selection in shaping patterns of sexual dichromatism in the largest family of songbirds (Aves: Thraupidae). Evolution 71:1061–1074. PubMed

Singhal S. 2013. De novo transcriptomic analyses for non-model organisms: an evaluation of methods across a multi-species data set. Mol. Ecol. Resour. 13:403–416. PubMed

Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. PubMed PMC

Starnberger I., Poth D., Peram P.S., Schulz S., Vences M., Knudsen J., Barej M.F., Rödel M.-O., Walzl M., Hödl W.. 2013. Take time to smell the frogs: vocal sac glands of reed frogs (Anura: Hyperoliidae) contain species-specific chemical cocktails. Biol. J. Linn. Soc. 110:828–838. PubMed PMC

Starnberger I., Preininger D., Hödl W.. 2014. From uni- to multi-modality: towards an integrative view on anuran communication. J. Comp. Physiol. A 200:777–787. PubMed PMC

Stuart-Fox D., Owens I.P.F.. 2003. Species richness in agamid lizards: chance, body size, sexual selection or ecology? J. Evol. Biol. 16:659–669. PubMed

Sztatecsny M., Preininger D., Freudmann A., Loretto M.-C., Maier F., Hödl W.. 2012. Don’t get the blues: conspicuous nuptial colouration of male moor frogs (Rana arvalis) supports visual mate recognition during scramble competition in large breeding aggregations. Behav. Ecol. Sociobiol. 66:1587–1593. PubMed PMC

Telford S.R. 1985. Mechanisms of evolution and inter-male spacing in the painted reedfrog (Hyperolius marmoratus). Anim. Behav. 33:1353–1361.

Telford S.R., Dyson M.L.. 1988. Some determinants of the mating system in a population of painted reed frogs (Hyperolius marmoratus). Behaviour 106:265–278.

Telford S.R., Passmore N.I.. 1981. Selective phonotaxis of four sympatric species of African reed frogs (genus Hyperolius). Herpetologica 37:29–32.

Toledo L.F., Haddad C.F.B.. 2009. Colors and some morphological traits as defensive mechanisms in anurans. Int. J. Zool. 2009:910892.

Turelli M., Barton N.H., Coyne J.A.. 2001. Theory and speciation. Trends Ecol. Evol. 16:330–342. PubMed

Veith M., Kosuch J., Rödel M.-O., Hillers A., Schmitz A., Burger M., Lötters S.. 2009. Multiple evolution of sexual dichromatism in African reed frogs. Mol. Phylogenet. Evol. 51:388–393. PubMed

Wagner C.E., Harmon L.J., Seehausen O.. 2012. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487:366–369. PubMed

Wells K.D. 1977. The social behavior of anuran amphibians. Anim. Behav. 25:666–693.

West-Eberhard M.J. 1983. Sexual selection, social competition, and speciation. Q. Rev. Biol. 58:155–183.

Wieczorek A., Drewes R., Channing A.. 2000. Biogeography and evolutionary history of Hyperolius species: application of molecular phylogeny. J. Biogeogr. 27:1231–1243.

Wollenberg K.C., Glaw F., Meyer A., Vences M.. 2007. Molecular phylogeny of Malagasy reed frogs, Heterixalus, and the relative performance of bioacoustics and color-patterns for resolving their systematics. Mol. Phylogenet. Evol. 45:14–22. PubMed

Woolbright L.L. 1983. Sexual selection and size dimorphism in anuran Amphibia. Am. Nat. 121:110–119.

Yovanovich C.A.M., Koskela S.M., Nevala N., Kondrashev S.L., Kelber A., Donner K.. 2017. The dual rod system of amphibians supports colour discrimination at the absolute visual threshold. Phil. Trans. R. Soc. 372:20160066. PubMed PMC

Zhang C., Sayyari E., Mirarab S.. 2017. ASTRAL-III: increased scalability and impacts of contracting low support branches In: Meidanis J, Nakhleh L, editors. Comparative Genomics. RECOMB-CG 2017. Lecture Notes in Computer Science, vol. 10562 Cham: Springer; p. 53–75.

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