Leapfrogging Into New Territory: How Mascarene Ridged Frogs Diversified Across Africa and Madagascar to Maintain Their Ecological Niche

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Leapfrogging Into New Territory: How Mascarene Ridged Frogs Diversified Across Africa and Madagascar to Maintain Their Ecological Niche Leapfrogging into new territory how Mascarene ridged frogs diversified across Africa and Madagascar to maintain their ecological niche Zimkus, Breda M.; Lawson, Lucinda P.; Barej, Michael F.; Barratt, Christopher D.; Channing, Alan; Dash, Katrina M.; Dehling, J. Maximilian; Du Preez, Louis; Gehring, Philip-Sebastian; Greenbaum, Eli; Gvoždík, Václav; Harvey, James; Kielgast, Jos; Kusamba, Chifundera; Nagy, Zoltán T.; Pabijan, Maciej; Penner, Johannes; Rödel, Mark-Oliver; Vences, Miguel; Lötters, Stefan Published in: Molecular Phylogenetics and Evolution DOI: 10.1016/j.ympev.2016.09.018 Publication date: 2017 Document version Publisher's PDF, also known as Version of record Document license: CC BY-NC-ND Citation for published version (APA): Zimkus, B. M., Lawson, L. P., Barej, M. F., Barratt, C. D., Channing, A., Dash, K. M., ... Lötters, S. (2017). Leapfrogging into new territory: how Mascarene ridged frogs diversified across Africa and Madagascar to maintain their ecological niche. Molecular Phylogenetics and Evolution, 106, 254-269. https://doi.org/10.1016/j.ympev.2016.09.018 Download date: 08. apr.. 2020 Molecular Phylogenetics and Evolution 106 (2017) 254–269 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Leapfrogging into new territory: How Mascarene ridged frogs diversified across Africa and Madagascar to maintain their ecological niche ⇑ Breda M. Zimkus a, , Lucinda P. Lawson b, Michael F. Barej c, Christopher D. Barratt d, Alan Channing e, Katrina M. Dash f,g, J. Maximilian Dehling h, Louis Du Preez i,j, Philip-Sebastian Gehring k, Eli Greenbaum f, Václav Gvozˇdík l,m, James Harvey n, Jos Kielgast o, Chifundera Kusamba p, Zoltán T. Nagy c,q, Maciej Pabijan r, Johannes Penner c,s, Mark-Oliver Rödel c, Miguel Vences t, Stefan Lötters u a Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA b Department of Biological Sciences, University of Cincinnati, 820F Rieveschl Hall, Cincinnati, OH 45221, USA c Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstrasse 43, 10115 Berlin, Germany d University of Basel, Biogeography Research Group, Department of Environmental Sciences, Klingelbergstrasse 27, Basel 4056, Switzerland e University of the Western Cape, Biodiversity and Conservation Biology, Private Bag X17, Bellville 7535, South Africa f Department of Biological Sciences, University of Texas at El Paso, 500 W. University Ave., El Paso, TX 79968, USA g Department of Biology, Tidewater Community College, 120 Campus Dr., Portsmouth, VA 23701, USA h Institute of Integrated Sciences, Department of Biology, University of Koblenz-Landau, Universitätsstraße 1, 56070 Koblenz, Germany i African Amphibian Conservation Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom 2520, South Africa j South African Institute for Aquatic Biodiversity, Somerset Street, Grahamstown 6139, South Africa k Fakultät für Biologie Universität Bielefeld, Abt. Biologiedidaktik, Universitätsstraße 25, 33615 Bielefeld, Germany l Institute of Vertebrate Biology, Czech Academy of Sciences, 603 65 Brno, Czech Republic m National Museum, Department of Zoology, 19300 Prague, Czech Republic n Harvey Ecological, 35 Carbis Road, Pietermaritzburg 3201, KwaZulu-Natal, South Africa o Department of Biology, University of Copenhagen, Copenhagen, Denmark p Centre de Recherche en Sciences Naturelles, Département de Biologie, Lwiro, The Democratic Republic of the Congo q Joint Experimental Molecular Unit, Royal Belgian Institute of Natural Sciences, Rue Vautier 29, 1000 Brussels, Belgium r Department of Comparative Anatomy, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland s Wildlife Ecology & Management, University of Freiburg, Tennenbacher Str. 4, 79106 Freiburg, Germany t Division of Evolutionary Biology, Zoological Institute, Technical University of Braunschweig, Mendelssohnstraße. 4, 38106 Braunschweig, Germany u Trier University, Department of Biogeography, 54286 Trier, Germany article info abstract Article history: The Mascarene ridged frog, Ptychadena mascareniensis, is a species complex that includes numerous lin- Received 2 June 2016 eages occurring mostly in humid savannas and open forests of mainland Africa, Madagascar, the Revised 15 September 2016 Seychelles, and the Mascarene Islands. Sampling across this broad distribution presents an opportunity Accepted 18 September 2016 to examine the genetic differentiation within this complex and to investigate how the evolution of bio- Available online 21 September 2016 climatic niches may have shaped current biogeographic patterns. Using model-based phylogenetic meth- ods and molecular-clock dating, we constructed a time-calibrated molecular phylogenetic hypothesis for Keywords: the group based on mitochondrial 16S rRNA and cytochrome b (cytb) genes and the nuclear RAG1 gene Amphibia from 173 individuals. Haplotype networks were reconstructed and species boundaries were investigated Historical biogeography Pan-African using three species-delimitation approaches: Bayesian generalized mixed Yule-coalescent model Phylogeny (bGMYC), the Poisson Tree Process model (PTP) and a cluster algorithm (SpeciesIdentifier). Estimates Ptychadena of similarity in bioclimatic niche were calculated from species-distribution models (MAXENT) and Species delimitation multivariate statistics (Principal Component Analysis, Discriminant Function Analysis). Ancestral-area Species distribution modeling reconstructions were performed on the phylogeny using probabilistic approaches implemented in BioGeoBEARS. We detected high levels of genetic differentiation yielding ten distinct lineages or operational taxonomic units, and Central Africa was found to be a diversity hotspot for these frogs. Most speciation events took place throughout the Miocene, including ‘‘out-of-Africa” overseas dispersal ⇑ Corresponding author. E-mail addresses: [email protected] (B.M. Zimkus), [email protected] (L.P. Lawson), [email protected] (M.F. Barej), [email protected] (C.D. Barratt), [email protected] (A. Channing), [email protected], [email protected] (K.M. Dash), [email protected] (J.M. Dehling), [email protected] (L. Du Preez), [email protected] (P.-S. Gehring), [email protected] (E. Greenbaum), [email protected] (V. Gvozˇdík), [email protected] (J. Harvey), [email protected] (J. Kielgast), [email protected] (C. Kusamba), [email protected] (Z.T. Nagy), [email protected] (M. Pabijan), johannes. [email protected] (J. Penner), [email protected] (M.-O. Rödel), [email protected] (M. Vences), [email protected] (S. Lötters). http://dx.doi.org/10.1016/j.ympev.2016.09.018 1055-7903/Ó 2016 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). B.M. Zimkus et al. / Molecular Phylogenetics and Evolution 106 (2017) 254–269 255 events to Madagascar in the East and to São Tomé in the West. Bioclimatic niche was remarkably well conserved, with most species tolerating similar temperature and rainfall conditions common to the Central African region. The P. mascareniensis complex provides insights into how bioclimatic niche shaped the current biogeographic patterns with niche conservatism being exhibited by the Central African radi- ation and niche divergence shaping populations in West Africa and Madagascar. Central Africa, including the Albertine Rift region, has been an important center of diversification for this species complex. Ó 2016 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 1. Introduction genus Phrynobatrachus (Zimkus et al., 2010). To date, no study has integrated biogeography and species distribution modeling to Reconstructing the spatial and temporal history of organisms is examine diversification of an amphibian clade with a Pan-African one of the primary goals of evolutionary biology, yet obtaining a distribution. clear picture of evolutionary history can be challenging given that The Ptychadena mascareniensis species complex is an ideal phylogenetics, species distributions, climatic history, and ecologi- model system to evaluate the processes of speciation, diversifica- cal processes, such as environmental tolerance and niche partition- tion, and bioclimatic niche evolution within a pan-continental ing, must be taken into consideration (Wiens, 2011; Wiens and radiation, as members of this complex are found across the entire Graham, 2005). New methods are emerging that integrate ecolog- sub-Saharan region and along the Nile River in Egypt and Sudan ical modeling, biogeographic reconstructions, and phylogenetic (Frost, 2016). In addition, this species complex is widely dis- analyses to allow a more complete understanding of the contribu- tributed across Madagascar and other islands within the Indian tions of geological and climatological phenomena, as well as eco- Ocean, so it presents a unique opportunity to investigate patterns logical dimensions (Ahmadzadeh et al., 2016; Blair et al., 2015; of diversification on contrasting ecological landscapes. The Chan et al., 2011; Dowell and Hekkala, 2016; Rato et al., 2015). P. mascareniensis complex includes: (1) P. mascareniensis sensu lato These methods also assist in the identification
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