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The Phylogeny of the Genus Gazella and Phylogeography And The phylogeny of the genus Gazella and the phylogeography and population genetics of Arabian species Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften vorgelegt beim Fachbereich 15 der Johann Wolfgang Goethe-Universität in Frankfurt am Main von Hannes Lerp aus Ilmenau Frankfurt, August 2013 (D 30) - II - I Summary Biodiversity is caused by a fundamental evolutionary process: speciation. When species can spread into new habitats and are allowed to colonize new ecological niches, speciation can become accelerated and is then called radiation. This can happen, e.g., when formerly separated land masses become connected. A prime example of such a scenario is the Arabian Peninsula that connects Africa and Asia since the Oligocene (approx. 30 Ma ago). Since then, the peninsula promoted several faunal exchanges between both continents. The mammalian genus Gazella is an excellent candidate for investigating this faunal exchange. Species are distributed on both, the African and Asian continent as well as on the Arabian Peninsula that is located in between. The aim of my thesis was to cast new light on the evolution and speciation of the genus and, furthermore, to evaluate the currently problematic taxonomy to infer suggestions for improved conservation actions for threatened gazelle species. Therefore, I investigated the taxon Gazella genetically and identified factors that promoted the speciation of this diverse genus. I assessed intraspecific genetic variability for species that inhabited the Arabian Peninsula to infer the past demography of those species and to estimate the history of species divergence and past population parameters. In the first part of my thesis I inferred a mitochondrial phylogeny based on cytochrome b gene sequences using samples of all nine extant species of Gazella and also of closely related taxa (chapter 2). Besides the monophyly of the genus Gazella two reciprocally monophyletic clades were detected that evolved in allopatry: one pre- dominantly African and one predominantly Asian clade. Within both clades species pairs could be inferred with species being ecologically adapted to different habitats: one species is a desert-dweller (probably the ancestral character state combination), while the other one is adapted to rather mountainous and humid habitats. These adaptations also correlate with the behavior of the species with the mountainous forms being sedentary, territorial and living in small groups and the desert forms being migratory, non-territorial and living in larger herds. - III - The second part of my thesis focuses on the Arabian gazelle species. In a study about G. subgutturosa I could show that the Arabian form G. marica (sand gazelle)—previously recognized as a subspecies of G. subgutturosa—is genetically distinct from the nominate form (chapter 3). Moreover, a phylogenetic tree based on cytochrome b gene sequences revealed a polyphyly of G. subgutturosa and G. marica with sand gazelles being more closely related to G. leptoceros and G. cuvieri of North Africa. Consequently, I suggested the restoration to full species level for G. marica corroborating earlier conservation practices of breeding both taxa separately in captivity. In case of G. dorcas such a genetic differentiation could not be detected (chapter 4). Despite the large distribution range from Mali in the west to Saudi Arabia in the east only low genetic variation was detectable in mitochondrial sequence data. Statistically parsimony network analyses revealed pronounced haplotype sharing across regions. Using a coalescence approach I observed a steep population decline that started about 25,000 years ago and which is still ongoing. The decline could be correlated with human hunting activities in the Sahara. Hence, hunting of G. dorcas (already in ancient times) had a much larger impact on gazelle populations than previously thought and even led to the extinction of the Arabian form of G. dorcas. In chapter 5 of my thesis I provided a rigorous test to genetically distinguish between the potential species G. gazella and G. arabica. Previously recognized as a single species mitochondrial sequence analyses provided first hints for the separation of both taxa. But without the investigation of nuclear loci the observed pattern could also be the result of male biased dispersal combined with female philopatry. Therefore, I amplified mito- chondrial sequence markers and nuclear microsatellite loci for both taxa and found support for the earlier view of two separate species. No signs of recurrent gene flow could be detected between neighboring populations of G. arabica and G. gazella. The split of both species could be estimated one million years ago and the recommendation of breeding both taxa separately in captivity for conservation purposes is fully justified. Several populations of G. arabica suffer from a severe decline. In chapter 6 I asked whether the population occurring on the Farasan archipelago—being at stable individual numbers for decades—may serve as potential source for future reintroduction on the Arabian mainland, although the gazelles show a reduced body size. Analyzing the genetic differentiation of Farasan gazelles, a genetic cluster could be inferred being endemic to the archipelago. However, only approx. 70% of Farasan individuals were assigned to this specific cluster, while the others showed at least intermediate or even complete assignment - IV - to the mainland cluster. This indicates ongoing introgression that is probably mediated by human translocations of gazelles from and onto the islands. Considering the uniform dwarfism of Farasan gazelles, reasons for the smaller body size might be direct consequences of resource limitations, i.e., phenotypic plasticity. If the population decline on the mainland will hold on Farasan gazelles could serve as stocks for future reintroductions. - V - II Zusammenfassung Die Erforschung der Entstehung der Arten bildet einen Schlüssel für das Verständnis von Evolution und Biodiversität. Der Prozess der Artbildung kann beschleunigt werden, wenn Arten neue Habitate oder neue ökologische Nischen besiedeln können. Dieser Prozess wird als Radiation bezeichnet. Bestimmte geologische Prozesse können Radiationen auslösen, wenn Arten sich dadurch ausbreiten können. Solche eine Radiation kann zum Beispiel durch geologische Prozesse ausgelöst werden, die es Organismen überhaupt erst ermöglichen sich weiter auszubreiten. Zum Beispiel kann die Verbindung zweier Kontinente durch eine Landbrücke für Festland bewohnende Arten ein solches geologisches Ereignis darstellen. Die wissenschaftliche Untersuchung solcher Radiationsereignisse kann damit zum Verständnis von Artbildung und Evolution beitragen. Ein Beispiel für eine solche Verbindung stellt die Arabische Halbinsel dar. Sie repräsentiert eine biogeographische Kontaktzone der Flora und Fauna Afrikas und Asiens. Seit dem Oligozän (vor etwa 30 Millionen Jahren) hat es mehrfach Austausche zwischen den beiden Kontinenten über die Arabische Halbinsel hinweg gegeben. Dabei war der Transfer der Fauna asymmetrisch und änderte sich über geologische Zeiträume (für eine Erläuterung siehe Kapitel 2). Ob eine Art über die Arabische Halbinsel erfolgreich neue Habitate besiedeln konnte, hing dabei von ihren ökologischen Voraussetzungen und den vorherrschenden klimatischen Bedingungen ab. Eine Tiergruppe, die sich besonders zur Untersuchung einer Radiation in dieser Region eignet, ist die Gattung Gazella, da sie sowohl auf den Kontinenten Afrika und Asien als auch auf der Arabischen Halbinsel selbst verbreitet ist. Mit neun rezenten Arten gehört sie zu einer der artenreichsten Gattungen innerhalb der Bovidae. Allerdings gehört die Gattung Gazella auch zu einer der am wenigsten verstandenen Gruppen innerhalb der Säugetiere. Viele, zum Teil widersprüchliche, Studien über ihre Entstehung und ihre Taxonomie wurden bereits veröffentlicht. Doch beruhen diese Studien hauptsächlich auf morphologischen Eigenschaften oder der Anzahl und Eigenschaft der Chromosomen der verschiedenen Arten. Genetisch ist die Gruppe der Gazellen bisher unzureichend charakterisiert, vor allem bezogen auf die Feststellung innerartlicher, genetischer Variabilität. Dies wirkst sich zudem negativ auf Bemühungen aus, diese gefährdeten - VI - Gazellenarten zu schützen. So besteht zum Beispiel Unsicherheit darüber, welche Populationen an welchen Orten wieder ausgewildert werden können. Ziel meiner Dissertation war es daher eine molekulare Phylogenie der Gattung Gazella zu erstellen und dabei alle rezenten Arten mit einzubeziehen. Des Weiteren wurde untersucht, welche Faktoren die Diversifizierung der Gattung unter Berücksichtigung der demographischen Entwicklung, Ökologie und des Verhaltens der entsprechenden Arten vorangetrieben haben (erster Teil der Dissertation, der einen bereits veröffentlichten Artikel enthält). Um die innerartliche, genetische Variabilität ausgewählter Arten – also derer, die auf der Arabischen Halbinsel verbreitet sind – einschätzen zu können, wurden kleiner skalierte Studien mit mehr Individuen (möglichst aus dem gesamten Verbreitungs- gebiet der Art) durchgeführt (zweiter Teil der Dissertation der drei bereits veröffentlichte und einen eingereichten Artikel enthält). Damit sollte auch das Verständnis historischer Wanderbewegungen und die Besiedlung neuer Habitate durch bestimmte Gazellenarten im Speziellen und somit der Evolution der Gattung Gazella im Allgemeinen gesteigert werden. Kapitel 2 repräsentiert den ersten Teil der Arbeit. Es wurde eine
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