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Actinopterygii, Cyprinidae) En La Cuenca Del Mediterráneo Occidental

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Actinopterygii, Cyprinidae) En La Cuenca Del Mediterráneo Occidental UNIVERSIDAD COMPLUTENSE DE MADRID FACULTAD DE CIENCIAS BIOLÓGICAS TESIS DOCTORAL Filogenia, filogeografía y evolución de Luciobarbus Heckel, 1843 (Actinopterygii, Cyprinidae) en la cuenca del Mediterráneo occidental MEMORIA PARA OPTAR AL GRADO DE DOCTOR PRESENTADA POR Miriam Casal López Director Ignacio Doadrio Villarejo Madrid, 2017 © Miriam Casal López, 2017 UNIVERSIDAD COMPLUTENSE DE MADRID Facultad de Ciencias Biológicas Departamento de Zoología y Antropología física Phylogeny, phylogeography and evolution of Luciobarbus Heckel, 1843, in the western Mediterranean Memoria presentada para optar al grado de Doctor por Miriam Casal López Bajo la dirección del Doctor Ignacio Doadrio Villarejo Madrid - Febrero 2017 Ignacio Doadrio Villarejo, Científico Titular del Museo Nacional de Ciencias Naturales – CSIC CERTIFICAN: Luciobarbus Que la presente memoria titulada ”Phylogeny, phylogeography and evolution of Heckel, 1843, in the western Mediterranean” que para optar al grado de Doctor presenta Miriam Casal López, ha sido realizada bajo mi dirección en el Departamento de Biodiversidad y Biología Evolutiva del Museo Nacional de Ciencias Naturales – CSIC (Madrid). Esta memoria está además adscrita académicamente al Departamento de Zoología y Antropología Física de la Facultad de Ciencias Biológicas de la Universidad Complutense de Madrid. Considerando que representa trabajo suficiente para constituir una Tesis Doctoral, autorizamos su presentación. Y para que así conste, firmamos el presente certificado, El director: Ignacio Doadrio Villarejo El doctorando: Miriam Casal López En Madrid, a XX de Febrero de 2017 El trabajo de esta Tesis Doctoral ha podido llevarse a cabo con la financiación de los proyectos del Ministerio de Ciencia e Innovación. Además, Miriam Casal López ha contado con una beca del Ministerio de Ciencia e Innovación. INDEX Acknowledgements/Agradecimientos SUMMARY 1-5 1. INTRODUCTION 6-16 1.1 Cyprinids Luciobarbus 6-8 1.2 Biogeographical models of , Heckel 1843 9-11 in the westernLuciobarbus Paleartic region. , 1.3 The genus , Heckel 1843 a brief summary 11-13 on its evolution and biogeography Luciobarbus 1.4 Biology and ecological remarks of the genus , Heckel 1843 13 1.5 Polyploidy in fishes 13-15 2.1.6Chapter Objectives I 16 25-59 Luciobarbus Taxonomic review of the genus , Heckel 1843 from Northwestern Morocco with the description of three new species. Chapter II 3. 61-94 Luciobarbus Taxonomy of rheophilic Heckel, 1843 from Morocco with the description of two new species. Chapter III 4. 95-146 Luciobarbus sclateri Paleobiogeography of an Iberian endemism ( Günther, 1868) inferred from mitochondrial and nuclear markers. Chapter IV 5. 147-188 BiogeographyLuciobarbus patterns on the evolution of freshwater fishes of the genus Heckel, 1843 in the western Mediterranean. Chapter V 6. 189-222 Luciobarbus Re-examination of the phylogeny of the genus Heckel, 1843 based on mitochondrial and nuclear data. 7. GENERAL DISCUSSION 223-232 Ackowledgments/Agradecimientos 1 SUMMARY This dissertation is composed oLfu5cciohbaaprtbeurs which try to assess the evolutionary patterns of the genus Heckel, 1843 in the western Palearctic at different scales: from taxonomic remarks that have led to the description of new species, to the study of the phylogenetic relationships and the biogeographical patterns shaping the diversification and evolution processes that gave origin to the species currently inhabiting the Palearctic region with an special emphasis in the western Mediterranean. In chapters I and II, five new species from North Africa are being described based on morphologic and molecular characters; chapter III deals with the influence of paleohidrogeological changes on the history; and population structure of an endemism from the Iberian Peninsula chapter IV focuses on the history and evolution of populations inhabiting both sides of the Strait of Gibraltar and chapter V addresses a thorough phylogenetic revision of the genus in its entire distribution range. In this thesis, the integration of different types of molecular tools, phylogenetic analyses and biogeographical methodologies have provided a wide scope for understanding thLeucpioabttaerrbnuss. and factors underlying the evolutionary history of the genus A detailed summary of each of the chapters is described as follows: Chapter I Barbus The taxonomy of sensu stricto Cuvier and Cloquet, 1816, has been reviewed in the last years and as consequence Mediterranean speciesLupcrieovbiaorubsulys included in this genus are presently assigned to the genLusciobarbus Heckel, 1843. The population of North African species of shows high diversification in Morocco, but there have been few taxonomic studies focusing on these populations. Previous phylogenetic studies based on morphological characters and molecular 2 cytb markers (isozymes and mitochondrial ) found that the populations belonging to north-western Morocco presented high levels of genetic differentiation compared to other populations of the genus, that were already assigned to separate species. The aim of this work was to describe those populations as distinct species based on morphological, meristic and genetic traits. For this purpose, a total of 200 specimens were morphological studied from Laou, Loukos, Hachef, Grou and Sebou basins. Twenty-three morphometric measurements and nine meristic variables were recorded and compared through different tests and diagnose osteological structures were investigated through comcpyutbter tomography. Phylogenetic analyses of the entire mitochondrial gene of each population under study were included. Both morphological and genetic aLpupciroobaacrhbeuss msuapgphorretbeednsitsh,eLudcisotbinarcbtiuosnraobfattehnrseies diffeLruecniotbanrebwussrpifeecniseis:. and Chapter II Luciobarbus The genus strictly occurs in freshwater systems and shows wide habitat versatility and is usually present in rivers of different topology, allowing the existence ofLluimcionbeatircbuasnd rheophilic species. In Morocco the rLhuecoipohbialircbusspecniaesusof have been tLruacdiiotiboanrablulys amsasgignniaedtlanttois (Günther, 1874) and (Pellegrin, 1919), althouLgh.nathsuiss.last species is considered by sLoumcioebaaurtbhuosrs as a junior synonym of These rheophilic species of Luciobsahrobwusa series of morphological characteristics that differ from other species, placing them in an uLnurecisooblvaerdbustaxonomic position and they could not be assigned to the genus when the genus was formally defined on Lt.hneasbuassis of osteoloLguicciaolbacrhbaursacters. Previous molecular studies placed in the genus along with other North African species. Therefore and for disentangling this puzzle the populations of the rheophilic barbs of the three basins in which they are currently present were studied. A total of 60 specimens were morphological studied from Tensift, Oum er Rbia and Moulouya basins. 3 Twenty-four morphometric measurements and ten meristic variables were counted. Osteological characteristic were investigated through compuctyetbr tomography and phylogenetic analyses of the entire mitochondrial gene from up-to-five individuals from each population under study were included. The three studied population from the Tensift, Oum er Rbia and Moulouya basins possessed molecular, osteological and morphometric traits that identified them as diffeLruecnitobsaprebcuiessg.uBearcsiefdenosins theseLuecviiodbeanrcbeuss, ztwayoanenwsissp. ecies were described: and Chapter III Luciobarbus The genus shows high levels of local endemicity across its distribution range and its species are genetically and morphologically well-differLeunctiioabteadrbbuosthsculantdeerir sympatric and allopatric conditions. The species (Günther, 1868) is an endemism of the Iberian Peninsula, confined to the mid-south basins of this region, including Guadalquivir, Guadiana, Segura and small southern basins. The Iberian Peninsula, at the western area of the Mediterranean Basin is considered a hotspot, well-known for its species richness and high levels of endemisms. Since Cenozoic, Iberia has undergone several geological and climatic changes such as the Alpine orogeny that led to the uplift of its major mountain chains; the Messinian Salinity Crisis, an event that almost dried the Mediterranean Sea; the reopening of the Strait of Gibraltar and the influence of the Last Glacial Maximum. This complex past has shaped the freshwater network of this region through time and since this species disperses only via freshwater, it is expected that its present- day distributionLuhcaiosbbaerebnusgsrcelaattleyriinfluenced by hydrogeological changes. In this context, represents an ideal biological model to describe the imprint of these historical processes on the population structure and diversification patterns of the species. A total of 505 individuals from 22 basins covering the entire distribution range of the species were analyzed through molecular markers. Three major lineages 4 were found and the mtDNA distribution patterns supported the isolation of the hydrographic basins as main factor driving intraspecific differentiation, followed by secondary contact, admLixutcuiroebaarnbdusres-cilsaotleartii.on processes that led to the present-day distribution of Chapter IV The history of the western Mediterranean region has been strongly influenced by tectonic dynamics that have alternately connected and separated Eurasian and African landmasses, allowing fauna exchange. The independent movement of the Alboran domain during the Alpine orogeny created the Betic-Rif
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