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. Maximilian Dehling; Robert C. Drewes; Raffael Ernst; Eli Greenbaum; Vaclav Gvozdik; 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:10.1093/sysbio/syz023

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. Maximilian Dehling, Robert C. Drewes, Raffael Ernst, Eli Greenbaum, Vaclav Gvozdik, James Harvey, Annika Hillers, Mareike Hirschfeld, Gregory F.M. Jongsma, Jos KielgastMarcel 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

^*Corresponding author for this work

Freshwater Biology

13 Citations (Scopus)

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 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.

Original language	English
Journal	Systematic Biology
Volume	68
Issue number	6
Pages (from-to)	859-875
Number of pages	17
ISSN	1063-5157
DOIs	https://doi.org/10.1093/sysbio/syz023
Publication status	Published - 1 Nov 2019

Keywords

Afrobatrachia
Anura
color evolution
diversification
macroevolution
sexual selection

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Portik, D. M., Bell, R. C., Blackburn, D. C., Bauer, A. M., Barratt, C. D., Branch, W. R., Burger, M., Channing, A., Colston, T. J., Conradie, W., Maximilian Dehling, J., Drewes, R. C., Ernst, R., Greenbaum, E., Gvozdik, V., Harvey, J., Hillers, A., Hirschfeld, M., Jongsma, G. F. M., ... McGuire, J. A. (2019). Sexual Dichromatism Drives Diversification within a Major Radiation of African Amphibians. Systematic Biology, 68(6), 859-875. https://doi.org/10.1093/sysbio/syz023

Portik, DM, Bell, RC, Blackburn, DC, Bauer, AM, Barratt, CD, Branch, WR, Burger, M, Channing, A, Colston, TJ, Conradie, W, Maximilian Dehling, J, Drewes, RC, Ernst, R, Greenbaum, E, Gvozdik, V, Harvey, J, Hillers, A, Hirschfeld, M, Jongsma, GFM, Kielgast, J, Kouete, MT, Lawson, LP, Leaché, AD, Loader, SP, Lötters, S, Meijden, AVD, Menegon, M, Müller, S, Nagy, ZT, Ofori-Boateng, C, Ohler, A, Papenfuss, TJ, Rößler, D, Sinsch, U, Rödel, MO, Veith, M, Vindum, J, Zassi-Boulou, AG & McGuire, JA 2019, 'Sexual Dichromatism Drives Diversification within a Major Radiation of African Amphibians', Systematic Biology, vol. 68, no. 6, pp. 859-875. https://doi.org/10.1093/sysbio/syz023

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title = "Sexual Dichromatism Drives Diversification within a Major Radiation of African Amphibians",

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 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.",

keywords = "Afrobatrachia, Anura, color evolution, diversification, macroevolution, sexual selection",

author = "Portik, {Daniel M.} and Bell, {Rayna C.} and Blackburn, {David C.} and Bauer, {Aaron M.} and Barratt, {Christopher D.} and Branch, {William R.} and Marius Burger and Alan Channing and Colston, {Timothy J.} and Werner Conradie and {Maximilian Dehling}, J. and Drewes, {Robert C.} and Raffael Ernst and Eli Greenbaum and Vaclav Gvozdik and James Harvey and Annika Hillers and Mareike Hirschfeld and Jongsma, {Gregory F.M.} and Jos Kielgast and Kouete, {Marcel T.} and Lawson, {Lucinda P.} and Leach{\'e}, {Adam D.} and Loader, {Simon P.} and Stefan L{\"o}tters and Meijden, {Arie Van Der} and Michele Menegon and Susanne M{\"u}ller and Nagy, {Zolt{\'a}n T.} and Caleb Ofori-Boateng and Annemarie Ohler and Papenfuss, {Theodore J.} and Daniela R{\"o}{\ss}ler and Ulrich Sinsch and R{\"o}del, {Mark Oliver} and Michael Veith and Jens Vindum and Zassi-Boulou, {Ange Ghislain} and McGuire, {Jimmy A.}",

year = "2019",

month = nov,

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doi = "10.1093/sysbio/syz023",

language = "English",

volume = "68",

pages = "859--875",

journal = "Systematic Biology",

issn = "1063-5157",

publisher = "Oxford University Press",

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T1 - Sexual Dichromatism Drives Diversification within a Major Radiation of African Amphibians

AU - Portik, Daniel M.

AU - Bell, Rayna C.

AU - Blackburn, David C.

AU - Bauer, Aaron M.

AU - Barratt, Christopher D.

AU - Branch, William R.

AU - Burger, Marius

AU - Channing, Alan

AU - Colston, Timothy J.

AU - Conradie, Werner

AU - Maximilian Dehling, J.

AU - Drewes, Robert C.

AU - Ernst, Raffael

AU - Greenbaum, Eli

AU - Gvozdik, Vaclav

AU - Harvey, James

AU - Hillers, Annika

AU - Hirschfeld, Mareike

AU - Jongsma, Gregory F.M.

AU - Kielgast, Jos

AU - Kouete, Marcel T.

AU - Lawson, Lucinda P.

AU - Leaché, Adam D.

AU - Loader, Simon P.

AU - Lötters, Stefan

AU - Meijden, Arie Van Der

AU - Menegon, Michele

AU - Müller, Susanne

AU - Nagy, Zoltán T.

AU - Ofori-Boateng, Caleb

AU - Ohler, Annemarie

AU - Papenfuss, Theodore J.

AU - Rößler, Daniela

AU - Sinsch, Ulrich

AU - Rödel, Mark Oliver

AU - Veith, Michael

AU - Vindum, Jens

AU - Zassi-Boulou, Ange Ghislain

AU - McGuire, Jimmy A.

PY - 2019/11/1

Y1 - 2019/11/1

N2 - 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.

AB - 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.

KW - Afrobatrachia

KW - Anura

KW - color evolution

KW - diversification

KW - macroevolution

KW - sexual selection

U2 - 10.1093/sysbio/syz023

DO - 10.1093/sysbio/syz023

M3 - Journal article

C2 - 31140573

AN - SCOPUS:85073279354

SN - 1063-5157

VL - 68

SP - 859

EP - 875

JO - Systematic Biology

JF - Systematic Biology

IS - 6

ER -

Sexual Dichromatism Drives Diversification within a Major Radiation of African Amphibians

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Keywords

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