LACUNA MOZAMBIQUE: ADDING AN IMPORTANT PIECE TO THE AFRICAN JIGSAW PUZZLE Inauguraldissertation zur Erlangung der Würde eines Doktors der Philosophie vorgelegt der Philosophisch-Naturwissenschaftlichen Fakultät der Universität Basel von Gabriela Bueno Bittencourt-Silva aus Brasilien Basel, 2017 Originaldokument gespeichert auf dem Dokumentenserver der Universität Basel edoc.unibas.ch Genehmigt von der Philosophisch-Naturwissenschaftlichen Fakultät auf Antrag von Prof. Dr. Peter Nagel (Fakultätsverantwortlicher) PD Dr. Simon P. Loader (Dissertationsleiter) Dr. Stefan Lötters (Korreferent) Basel, den 18 April 2017 Prof. Dr. Martin Spiess (Dekan) TABLE OF CONTENTS Introduction 1 Abstract 2 Historical Biogeography 2 East African biogeography 5 Mozambique 9 Objectives 11 Chapters Overview 12 References 14 Chapter I 20 The phylogenetic position and diversity of the enigmatic mongrel frog Nothophryne Poynton, 1963 (Amphibia, Anura) Chapter II 35 Impact of species delimitation and sampling on niche models and phylogeographical inference: a case study of the East African reed frog Hyperolius substriatus Ahl 1931 Chapter III 61 Phylogeny and historical biogeography of the shovel-footed squeaker Arthroleptis stenodactylus Pfeffer, 1893 Synthesis 86 Acknowledgements 100 Supplementary Materials 102 Chapter I 102 Chapter II 124 Chapter III 136 Additional Publications 151 Curriculum Vitae 173 INTRODUCTION INTRODUCTION ________________________________________________________________ Abstract Reconstructing historical biogeography is similar to assembling a jigsaw puzzle, every piece added reveals a little bit more of the overall picture. In this thesis I present and discuss the diversity of species found on the mountains of northern Mozambique and explore the relationships between assemblages of different mountains. This study reveals a complex history of lineage diversification within species of amphibians and proposes hypotheses to explain the biogeographical patterns observed. The mountains of northern Mozambique are in the crossroads between two faunal groups, Afrotemperate and Afrotropical, which partially explain the complexity of this regions biota. Most of the species found on these mountains are biogeographically related to the lowland forest of East Africa, though some strictly montane species are also present. Furthermore, this thesis provides predictions regarding species potential distributions across other unexplored mountains of this region. Some of the hypotheses and predictions presented in this thesis can potentially be tested in the future. Finally, this thesis adds another piece to the African jigsaw puzzle shedding light on the complex biogeographical history of amphibians. Historical Biogeography Not everything is everywhere. Different species and higher taxa of animals and plants have their own characteristic patterns of distribution in space, and, if we do not restrict ourselves to the present, in time also. This is the fundamental observation of the science of biogeography, the aim of which is to understand what determines organismal distributions in general, and how the particular distributions we can observe today came to be (de Candolle, 1855; Wallace, 1876). Decades before the emergence of the theory of plate tectonics, Alfred Wegener, puzzled by the similarity between fossils of plants and animals found on opposite sides of the Atlantic, started developing the theory of continental drift (Wegener, 1966). While the distribution of organisms gives us clues about their ecological preferences (i.e. their niches) both now and in the past from the fossil record, phylogenies provide insights into intra and interspecific relationships of species. Geological and palynological studies are fundamental for the reconstruction of past climatic conditions and landscapes. Like in a jigsaw puzzle, these pieces of information put together help biogeographers to formulate and test hypotheses and theories about the history of species distribution. 2 INTRODUCTION ________________________________________________________________ Recent technological developments in Geographical Information Systems (GIS) have provided new ways to identify and examine patterns of the distribution of species – assisting in conducting biogeographical analyses. In particular, ecological niche models (ENMs) are widely used to predict current, future and past distribution of species (Elith and Leathwick, 2009). These models combine species locality records with environmental data (e.g. elevation, temperature, precipitation) potentially relevant to the organism in question to generate maps of habitat suitability. These models’ predictions of species potential distributions have assisted in formulating and testing hypotheses of relationships between populations and an overall better framework for interpreting phylogeographic hypotheses (Chan et al., 2011; Lawson, 2013; Pearson et al., 2007). For example, Lawson (2013) modelled the distribution of the East African reed frog Hyperolius substriatus using locality data from Tanzania and Malawi and predicted its occurrence on mountains of Northern Mozambique. The predictions were later ground-truthed by Portik et al. (2013), highlighting the usefulness of ENMs in providing insights into biogeographical patterns, notwithstanding the numerous caveats concerning the interpretation of these models (Araújo and Guisan, 2006; Yackulic et al., 2013). Furthermore, ENMs have also been used to identify cryptic species or new allopatric populations (Raxworthy et al., 2007). Overall, ENMs have provided another useful tool for analysing historical biogeographical patterns. Species are considered the basic unit for biogeographers (Riddle and Hafner, 1999). However, the meaning of the term “species” is probably one of the most debated topics in biology since earliest times. Although taxonomists have traditionally relied mainly on morphological characters to make inferences about species, there has been increased use of genetic characters to distinguish species. These molecular data, however, often produce discordant results (Lahr et al., 2014). Evidence for multiple genetic lineages in the absence of morphological differentiation can occur in cases of convergent evolution or stasis leading to cryptic diversity, whereas multiple morphologies but genetic homogeneity can occur in cases of phenotypic plasticity (Lahr et al., 2014). As Mayr (1963, p.24) states, “Evolution is a gradual process and, in general, so is the multiplication of species… As a consequence one finds many populations in nature that have progressed only part of the way toward species status”. Because biogeography focuses on the distribution of species in time and space the science of biogeography is intimately linked to understanding speciation processes. The main 3 INTRODUCTION ________________________________________________________________ biogeographic processes thought to promote speciation are vicariance and dispersal, and often diversification patterns are explained by a combination of both (Ronquist, 1997). Vicariance occurs when populations become separated by the emergence of a physical barrier to gene flow (e.g. forest fragmentation due to aridification). Given enough time and absence of gene flow between these disjunct populations, allopatric speciation is likely to occur. With the disappearance of the vicariant barrier, for instance during moister periods when forest fragments coalesce, previously isolated populations/lineages can disperse. Lineages dispersing back into formerly occupied areas after isolation (referred to as secondary contact zones) may result in one of the situations described in Table 1. Such scenarios are perhaps commonplace, particularly in tropical biomes where climates have fluctuated periodically and where diversity is high. Table 1. Possible outcomes of secondary contact after isolation according to Haffer (1969). Speciation Reproductive Ecologically Secondary contact Prediction process isolation compatible Geographic overlap Complete Yes Yes Sympatric species Geographic exclusion Incomplete Yes No Mutual exclusion Hybridization Incomplete No - Same species Biogeographers endeavour to untangle vicariance and dispersal processes when looking at evidence from both phylogenetic and spatial data of species. Attempts to interpret speciation processes can be problematic and often inconclusive but by using integrative approaches with different sets of data (as applied in this thesis) it can be possible to evaluate alternatives and identify most likely scenarios. Particular study areas have been important for studying speciation processes, and these include most prominently insular systems. Typically, research has been conducted on oceanic islands, with great progress made in understanding historical biogeographical processes given the relatively simple geographical situation (known geological origin, size, and isolation of each island) (Gillespie, 2004; Simberloff, 1976; Vences et al., 2003). Because of the isolation by altitude (and thus by temperature), mountains are also often considered good, island-like systems for investigating vicariance and allopatric speciation. Montane systems, sometimes referred to as “sky islands”, have recently attracted interest as important study subject for historical biogeography (Branch et al., 2014; 4 INTRODUCTION ________________________________________________________________ Conradie et al., 2016; Morrone and Crisci, 1995; Stanley et al., 2015). This thesis focuses on mountains and therefore