Molecular Phylogeny and Biogeography of Ranoid Frogs
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Molecular phylogeny and biogeography of ranoid frogs Dissertation zur Erlangung des akademischen Grades des Doktors der Naturwissenschaften (Dr. rer. nat.) an der Universität Konstanz, Mathematisch- Naturwissenschaftliche Sektion Fachbereich Biologie vorgelegt von Arie van der Meijden, M.Sc. Konstanz, März 2006 Prüfungskommission: Prof. Iwona Adamska Prof. Axel Meyer Prof. Miguel Vences ..love for all living creatures [is] the most noble attribute of man.. Charles Darwin (1809-1882), in “The Descent of Man and Selection in Relation to Sex” (1872). 2 Acknowledgements First and foremost I would like to thank Prof. Axel Meyer for hiring me as a technician, and for subsequently showing his confidence in me by allowing me to start my PhD work in his lab. Working in his lab, I have acquired knowledge and skills indispensable to further pursue a career at the high level of biology that Prof. Meyer so adamantly exemplifies, and for this I am very grateful. No less essential to the realization of this thesis was the guidance of Prof. Miguel Vences, who installed in me a purposeful mode of research, and who showed me the field of amphibian biology as more vibrant, dynamic and enticing as I could have thought. I am greatly indebted to my collaborators, without whom much of my research would not have been possible, or the results greatly diminished. Apart from Axel Meyer and Miguel Vences, I am therefore thankful to (alphabetical oder) Renaud Boistel, Allan Channing, Ylenia Chiari, Justin Gerlach, Simone Hoegg, Annemarie Ohler, Meike Thomas and David Vieites. Since my first arrival in Konstanz on October 15th 2002, I have had the privilege of learning lab and analysis techniques from the skilled people who make up the Meyer-lab. In particular I would like to mention Simone Hoegg, Dirk Steinke and Elke Hespeler for their patience with my initial ignorance. Outside the realm directly related to my work, I have many people to thank for making the time I spent in Konstanz a lot of fun. The people of the Meyer-lab form a tightly knit community with whom I greatly enjoyed talking and partying with. I would like to thank Ylenia Chiari here in particular, for discussions of work and many other things, and for weathering all the fun and not-so-fun times together with me. This thesis is a direct result of my incurable affinity to biology, and herpetology in particular, since an early age. Many people have suffered at my hands because of this and I would like to take this space to thank them: Most of all, I could not have achieved this without the unwavering and full support from my parents. Despite initially poor school results, astronomical electricity bills, lizards in the curtains, snakes in the kitchen, and numerous other escapees, my parents supported 3 my interests. My sister too patiently endured her share of unexpected encounters around the house. My travels would certainly have never been without my family supporting me. For the support, understanding and guidance of my family I am therefore especially grateful. To all my friends who, despite my traveling, kept close contact and who made my every visit to the Netherlands a joy, and who showed or feigned interest all those times I told them something “interesting” about animals, I am very grateful. Special thanks to Lennart Pors for printing and binding this thesis. I would like to thank Arendo Flipse for putting a steady stream of herpetological biodiversity into my very hands for over twelve years, and for teaching me a lot about herpetology. To all these people and many more I am greatly indebted, and to all I dedicate this thesis. 4 Table of Contents General Introduction ___________________________________________________ 7 Amphibian declines____________________________________________________ 7 Continuous discovery __________________________________________________ 8 Phylogenetic theory as a framework for evolutionary discovery _________________ 9 An introduction to frogs in the superfamily Ranoidea ________________________ 10 Biogeography of the Ranoidea __________________________________________ 12 Taxonomic difficulties owing to homoplasious characters_____________________ 13 Structure of this thesis_________________________________________________ 13 1. Novel phylogenetic relationships of the enigmatic brevicipitine and scaphiophrynine toads as revealed by sequences from the nuclear rag-1 gene____ 16 1.1 Abstract_________________________________________________________ 16 1.2 Introduction______________________________________________________ 17 1.3 Materials and methods _____________________________________________ 18 1.4 Results__________________________________________________________ 19 1.5 Discussion_______________________________________________________ 20 Acknowledgements ___________________________________________________ 23 2. Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians___________________________________________________________ 25 2.1 Abstract_________________________________________________________ 25 2.2 Introduction______________________________________________________ 26 2.3 Materials and methods _____________________________________________ 27 2.4 Results__________________________________________________________ 29 2.5 Discussion_______________________________________________________ 37 Acknowledgements ___________________________________________________ 41 3. A previously unrecognised radiation of ranid frogs in Southern Africa revealed by nuclear and mitochondrial DNA sequences _____________________________ 43 3.1 Abstract_________________________________________________________ 43 3.2 Introduction______________________________________________________ 44 3.3 Materials and methods _____________________________________________ 47 5 3.4 Results__________________________________________________________ 51 3.5 Discussion_______________________________________________________ 54 3.6 Conclusion ______________________________________________________ 59 Acknowledgements ___________________________________________________ 60 4. Molecular phylogenetic evidence for paraphyly of the genus Sooglossus, with the description of a new genus of Seychellean frogs ____________________________ 62 4.1 Abstract_________________________________________________________ 62 4.2 Introduction______________________________________________________ 63 4.3 Materials and methods _____________________________________________ 65 4.4 Results__________________________________________________________ 69 4.5 Discussion_______________________________________________________ 72 Acknowledgements ___________________________________________________ 79 5. Nuclear gene phylogeny of narrow-mouthed toads, family Microhylidae, and a discussion of competing hypotheses for their origin _________________________ 81 5.1 Abstract_________________________________________________________ 81 5.2 Introduction______________________________________________________ 81 5.3 Materials and methods _____________________________________________ 84 5.4 Results__________________________________________________________ 88 5.5 Discussion_______________________________________________________ 91 Acknowledgements ___________________________________________________ 98 Summary ____________________________________________________________ 99 Zusammenfassung____________________________________________________ 102 General references ___________________________________________________ 106 Appendix 1__________________________________________________________ 116 Appendix 2__________________________________________________________ 117 Results produced by collaborators ______________________________________ 119 6 General Introduction General Introduction In this thesis I provide the first broad molecular phylogenetic hypotheses for well known ranoid frog groups, in particular the Brevicipitinae (chapter 1), the Ranidae (chapter 3) and the Microhylidae (chapter 5). Also included in this thesis is a phylogenetic study of the enigmatic Sooglossidae, basal neobatrachians endemic to the Seychelles (chapter 4). I discuss the taxonomic and biogeographic consequences of the recovered phylogenies. Furthermore the relative merit of the genes 16S and CO1 for genetic barcoding of amphibians is discussed (chapter 2). Amphibian declines Since the initial identification of worldwide enigmatic amphibian declines at the world congress of herpetology in 1989, more reports on the disappearance of amphibian populations from all parts of the world have been published (Wake, 1991). The global amphibian assessment (GAA) published their findings on this phenomenon in the journal Science (Stuart et al., 2004), showing that a sobering 32.5% of amphibian species are suffering declines. Moreover, although many are declining due to well understood factors such as introduced species (Vredenburg, 2004), overexploitation (Lannoo et al., 1994) and habitat loss, alteration and fragmentation due to human encroachment (Fisher and Shaffer, 1996; Marsh and Pearman, 1997), 48% of the declining populations are doing so due to unknown reasons. Many factors have been proposed as possible causes of these enigmatic declines; climate change (Pounds et al., 1999; Pounds et al., 2006), chemical contaminants (Hayes et al., 2002), UV radiation (Blaustein et al., 2003), infectious diseases (Daszak, 1998) or a combination of these factors. Four families contribute most to the total number of declining species; Bufonidae, Leptodactylidae, Hylidae and Ranidae (figure