Diversity and Biogeography of Frogs in the Genus Amnirana (Anura: Ranidae) Across Sub-Saharan Africa

Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Diversity and biogeography of frogs in the genus Amnirana (Anura: Ranidae) across sub-Saharan Africa Gregory F.M. Jongsmaa,n,⁎, Michael F. Barejb, Christopher D. Barrattc, Marius Burgerd,e, Werner Conradief,g, Raffael Ernsth, Eli Greenbaumi, Mareike Hirschfeldb, Adam D. Leachéj, Johannes Pennerb,k, Daniel M. Portikl, Ange-Ghislain Zassi-Bouloum, Mark-Oliver Rödelb, David C. Blackburna,n a California Academy of Sciences, San Francisco, CA 94118, USA b Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstrasse 43, 10115 Berlin, Germany c University of Basel, Biogeography Research Group, Department of Environmental Sciences, Basel 4056, Switzerland d African Amphibian Conservation Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom 2520, South Africa e Flora Fauna & Man, Ecological Services Ltd., Tortola, British Virgin Island, United Kingdom f Port Elizabeth Museum (Bayworld), Port Elizabeth 6013, South Africa g School of Natural Resource Management, George Campus, Nelson Mandela Metropolitan University, George 6530, South Africa h Senckenberg Natural History Collections Dresden, Königsbrücker Landstr. 159, D-01109 Dresden, Germany i Department of Biological Sciences, University of Texas at El Paso, El Paso, TX, USA j Department of Biology and Burke Museum of Natural History and Culture, University of Washington, Seattle, WA 98195-1800, USA k Chair of Wildlife Ecology & Management, University of Freiburg, Tennenbacher Str. 4, 79106 Freiburg, Germany l Department of Biology, University of Texas at Arlington, 501 S. Nedderman Drive, Box 19498, Arlington, TX 76019-0498, USA m USA Institut national de Recherche en Sciences Exactes et Naturelles (IRSEN), BP 2400 Brazzaville, Democratic Republic of the Congo n Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA ARTICLE INFO ABSTRACT Keywords: Frogs in the genus Amnirana (family Ranidae) are widely distributed across sub-Saharan Africa and present a Africa model system for exploring the relationship between diversification and geography across the continent. Using Anura multiple loci from the mitochondrial (16S) and nuclear genomes (DISP2, FICD, KIAA2013, REV3L), we generated Cryptic species a strongly supported species-level phylogeny that provides insights into the continental biogeography of African Lower Guinean Forests species of Amnirana, which form a monophyletic group within the genus. Species delimitation analyses suggest Phylogeny that there may be as many as seven additional species of Amnirana in Africa. The biogeographic history of Species delimitation Tropics Amnirana is marked by several dispersal and vicariance events, including dispersal from the Lower Guinean Forest into the Congo Basin. In addition, phylogeographic patterns within two widespread species, A. albolabris and A. galamensis, reveal undescribed cryptic diversity. Populations assigned to A. albolabris in western Africa are more closely related to A. fonensis and require recognition as a distinct species. Our analyses reveal that the Lower and Upper Guinean Forest regions served as important centers of interspecific and intraspecific diversi- fications for Amnirana. 1. Introduction 2017), reptiles (Leaché et al., 2014; Shirley et al., 2014; Medina et al., 2016; Stanley et al., 2011), mammals (Bohoussou et al., 2015; Lorenzen Conducting molecular phylogenetic and phylogeographic studies at et al., 2012), birds (Fuchs et al., 2011; Voelker et al., 2010), dragonflies the continental scale in Africa is hampered by its large size, in- (Dijkstra, 2006), and plants (Fayolle et al., 2014; Ley et al. 2014; Dauby accessibility of many regions, and political instabilities. However, in- et al. 2014). These studies are reshaping our understanding of the creased sampling over the past decade and strong global collaborations processes that drive and maintain species diversity across sub-Saharan are now facilitating large-scale phylogenetic and biogeographic studies Africa as well as delimiting important areas of endemism. In addition, across a diversity of African taxa, including amphibians (Blackburn, the cryptic species revealed by these studies are important for desig- 2008; Channing et al., 2016; Evans et al., 2015; Zimkus et al., 2010, nating effective conservation units (Thomassen et al., 2011), and for ⁎ Corresponding author at: Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA. E-mail addresses: [email protected], gjongsma@ufl.edu (G.F.M. Jongsma). https://doi.org/10.1016/j.ympev.2017.12.006 Received 19 April 2017; Received in revised form 30 November 2017; Accepted 5 December 2017 G.F.M. Jongsma et al. Fig. 1. Sampling localities across Africa for specimens of Amnirana sequenced in our study (see Appendix A) are shown for each species. For each species, the approximate distribution is depicted in the same color using IUCN maps layers. These colors match the color-coding used in Fig. 2 and Supplementary Fig. 1. Inset shows distributions of four species restricted to Central Africa and is at the same scale as the larger map. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) accurate phylogenetic estimation and hypothesis testing (Bickford implications for understanding the origins and maintenance of diversity et al., 2007; Heath et al., 2008; Zwickl and Hillis, 2002). in the Afrotropics. The extensive combined distribution of the eleven recognized East Africa hosts several centers of amphibian endemism, including African species in the anuran genus Amnirana (family Ranidae) makes the Eastern Arc Mountains (Loader et al., 2004), the Albertine Rift this taxon ideal for investigating large-scale biogeographic patterns. (Plumptre et al., 2007), and East African Coastal Forest (Burgess and Taken together, these species extend from extreme western Africa Clarke, 2000). Two widespread species (A. albolabris and A. galamensis) across to the Horn of Africa and south into Angola, Mozambique, have populations across several of these centers in East Africa (Fig. 1) Zambia, and Zimbabwe (Fig. 1). Several species have large distribu- and these may contain cryptic species. There is one known subspecies, tions, such as A. galamensis and A. albolabris, each of which is found in A. galamensis bravana, known from the East African Coastal Forests of more than 20 countries. These widespread species span many well- Kenya and Somalia (Poynton, 1964). known biogeographic barriers (e.g., Congo River and Dahomey Gap) While the Lower Guinean Forest (LGF) and the Congo Basin have and several proposed historical forest refugia (e.g., the Cameroon been largely overlooked for their potential to harbor high levels of di- Volcanic Line and the West African Nimba Mountains; Hall and versity (Kingdon, 1990; Mayr and O’Hara, 1986), recent studies across Moreau, 1970; Maley, 1996). The clade comprising African Amnirana is several frog families demonstrate that Central Africa, and the LGF in embedded within a larger radiation of ranid frogs from Southeast Asia. particular, hosts high levels of diversity at both the species and popu- One Asian species—Amnirana nicobariensis—was placed in Amnirana by lation levels (Barej et al., 2010, 2011, 2014b; Blackburn, 2008, 2009, Oliver et al. (2015), though subsequent work by Chan and Brown 2010; Evans et al., 2015; Hirschfeld et al., 2015; Rödel et al., 2012, (2017) found that species to be closer to other Asian taxa. Our study 2015; Zimkus and Gvoždík, 2013; Zimkus et al., 2010). The Lower focuses on the African members of Amnirana and aims to explore pat- Guinean Forest harbors nearly half of the species of Amnirana (A. al- terns of genetic diversity within and across major geographic regions of bolabris, A. amnicola, A. asperrima, A. lepus, and A. longipes; Perret, the continent including West, Central, and East Africa. 1977), and therefore appears to be a center of diversity for the genus. West Africa (west of the Nigerian Cross River) has amphibian as- The Plio-Pleistocene forest refuge hypothesis has been invoked to ex- semblages distinct from Central Africa (Penner et al., 2011) and tends plain heightened diversity in the LGF (Anothony et al., 2007; Bou- to host either divergent lineages (e.g., Odontobatrachus, Pseudhyme- houssen et al., 2015; Jacquet et al., 2014). Based on these studies if nochirus) or relatively young species that have closely related sister there is hidden diversity in Amnirana we predict a recent origin (i.e. species in Central Africa (Barej et al., 2014a; Blackburn, 2008; Evans since the Pliocene). et al., 2004). Two members of Amnirana (A. fonensis and A. occidentalis) This study aims to resolve interspecific relationships of the currently are known only from the Upper Guinean Forests (Perret, 1983; Rödel recognized species of Amnirana found in sub-Saharan Africa. We sam- and Bangoura, 2004). However, the divergence times of these from pled extensively across the distribution of the genus (Fig. 1), including other species of Amnirana remains unclear (Kosuch et al., 2001; Oliver sampling of widespread species across multiple countries, and used et al., 2015; Roelants et al., 2007; Chan and Brown, 2017). Determining DNA sequence data for one mitochondrial and four nuclear genes to whether West African taxa are early

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