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Taxonomy, Phylogeny and Distribution of Tamarins (Genus Saguinus, Hoffmannsegg 1807)

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Taxonomy, Phylogeny and Distribution of Tamarins (Genus Saguinus, Hoffmannsegg 1807) Göttinger Zentrum für Biodiversitätsforschung und Ökologie ‐Göttingen Centre for Biodiversity and Ecology‐ TAXONOMY, PHYLOGENY AND DISTRIBUTION OF TAMARINS (GENUS SAGUINUS, HOFFMANNSEGG 1807) Dissertation zur Erlangung des Doktorgrades der Mathematisch‐Naturwissenschaftlichen Fakultäten der Georg‐August‐Universität zu Göttingen vorgelegt von Dipl.‐Biol. Christian Matauschek aus München Göttingen, Dezember 2010 Referent: Prof. Dr. Eckhard W. Heymann Koreferent: Prof. Dr. Peter M. Kappeler Tag der mündlichen Prüfung: i Contents 1 GENERAL INTRODUCTION.........................................................................................................1 1.1 THE TAMARINS OF THE GENUS SAGUINUS (HOFFMANNSEGG 1807)....................................................... 2 1.2 OVERVIEW OF THE CURRENT STATUS OF TAMARIN TAXONOMY ............................................................... 2 1.3 GEOGRAPHIC ORIGIN AND DISPERSAL OF SAGUINUS........................................................................... 10 1.4 SPECIFIC QUESTIONS .................................................................................................................... 13 2 COMPLETE MITOCHONDRIAL GENOME DATA REVEAL THE PHYLOGENY OF CALLITRICHINE PRIMATES AND A LATE MIOCENE DIVERGENCE OF TAMARIN SPECIES GROUPS ..............................15 2.1 INTRODUCTION ........................................................................................................................... 17 2.2 METHODS .................................................................................................................................. 18 2.2.1 Laboratory methods ........................................................................................................ 18 2.2.2 Phylogenetic analysis....................................................................................................... 20 2.2.3 Estimations of divergence ages ....................................................................................... 21 2.3 RESULTS..................................................................................................................................... 22 2.3.1 Phylogenetic reconstructions........................................................................................... 23 2.3.2 Estimates of divergence ages........................................................................................... 25 2.4 DISCUSSION................................................................................................................................26 2.4.1 Phylogenetic relationships within the Callitrichinae........................................................ 27 2.4.2 Phylogenetic relationships within the genus Saguinus.................................................... 27 2.4.3 Taxonomic implications for the different Saguinus species groups ................................. 29 2.4.4 Biogeographic implications.............................................................................................. 30 3 MITOCHONDRIAL PHYLOGENY OF TAMARINS (SAGUINUS, HOFFMANNSEGG 1807) WITH TAXONOMIC AND BIOGEOGRAPHIC IMPLICATIONS FOR THE S. NIGRICOLLIS SPECIES GROUP.........33 3.1 INTRODUCTION ........................................................................................................................... 35 3.2 METHODS .................................................................................................................................. 36 3.2.1 Sampling sites and sample collection .............................................................................. 36 3.2.2 Laboratory methods ........................................................................................................ 39 3.2.3 Statistical methods .......................................................................................................... 40 3.3 RESULTS..................................................................................................................................... 42 3.4 DISCUSSION................................................................................................................................48 3.4.1 The status of S. tripartitus................................................................................................ 48 3.4.2 The status of S. melanoleucus.......................................................................................... 49 3.4.3 The status of S. fuscicollis subspecies .............................................................................. 49 3.4.4 The status of S. n. nigricollis and S. graellsi ..................................................................... 50 3.4.5 Species concepts and general taxonomic implications .................................................... 51 3.4.6 Biogeographic implications.............................................................................................. 53 ii 4 THE RANGE OF THE GOLDEN‐MANTLE TAMARIN SAGUINUS TRIPARTITUS (MILNE EDWARDS, 1878): DISTRIBUTIONS AND SYMPATRY OF FOUR TAMARINS IN SOUTHERN COLOMBIA, ECUADOR AND NORTHERN PERU ...............................................................................................................55 4.1 INTRODUCTION ........................................................................................................................... 57 4.2 THE DISTRIBUTION OF SAGUINUS TRIPARTITUS.................................................................................. 57 4.3 SYMPATRY .................................................................................................................................. 64 4.3.1 Saguinus fuscicollis lagonotus (Jiménez de la Espada, 1870) .......................................... 64 4.3.2 Saguinus nigricollis nigricollis (Spix, 1823) ...................................................................... 68 4.3.3 Saguinus nigricollis graellsi (Jiménez de la Espada, 1870)............................................... 70 4.4 SYMPATRY, BODY SIZE AND ECOLOGICAL NICHES ............................................................................... 74 4.5 GEOGRAPHIC RANGES, SYMPATRY, AND THE TAXONOMY OF SAGUINUS NIGRICOLLIS AND S. FUSCICOLLIS .... 77 5 GENERAL DISCUSSION ............................................................................................................80 5.1 SUMMARY OF RESULTS ................................................................................................................. 80 5.2 THE IMPORTANCE OF EXTANT FIELD SAMPLING FOR PHYLOGENETIC STUDIES ........................................... 83 5.3 METHODICAL APPROACH: CAN MITOCHONDRIAL DNA SERVE AS A SUCCESSFUL TOOL IN TAMARIN TAXONOMY?.......................................................................................................................................... 84 5.4 SPECIES CONCEPTS AND SPECIES DELIMITATIONS AND THEIR EFFECT ON CONSERVATION ISSUES .................. 85 5.5 THE RELEVANCE OF MOLECULAR STUDIES FOR THE UNDERSTANDING OF AMAZONIA’S DIVERSITY AND BIOGEOGRAPHY...................................................................................................................................... 87 5.6 OUTLOOK................................................................................................................................... 88 SUMMARY ....................................................................................................................................89 ZUSAMMENFASSUNG....................................................................................................................91 BIBLIOGRAPHY ..............................................................................................................................93 APPENDIX ................................................................................................................................... 101 DANKSAGUNG............................................................................................................................. 109 CURRICULUM VITAE .................................................................................................................... 110 ERKLÄRUNG ÜBER EIGENE LEISTUNGEN ...................................................................................... 111 iii iv 1 General Introduction Primates are one of the most diverse orders within the mammals. About 634 taxa are known to science so far (Mittermeier et al., 2009). But the taxonomy of primates is still a field of great discussion and dynamics. Many new species have been described in recent years, oth‐ ers lumped together, because new molecular methods offer new possibilities to review mor‐ phological similar taxa on a molecular basis and new species concepts prevailed (Groves, 2004). As well as the number of newly described primate species increased, the number of primates appearing on the IUCN red list of threatened species increased over the past years. 47.8 % were listed as threatened in the 2008 red list (Mittermeier et al., 2009) Some even face ex‐ tinction within the near future. The need for space of the exploding human population causes a rapid loss of habitat for primates and other animals and plants as well. In many re‐ gions of the tropics hunting for meat is a major threat for the declining numbers of primates (Strier, 2007). So the research on primate diversity more and more gets important in conser‐ vation issues. To contribute to the illumination of primate taxonomy and diversity five research projects have been established by the German
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