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Comparative Population Genetics, Larval Dispersal and Evolutionary Aspects of Antarctic Fishes (Notothenioidei)

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Comparative Population Genetics, Larval Dispersal and Evolutionary Aspects of Antarctic Fishes (Notothenioidei) Comparative population genetics, larval dispersal and evolutionary aspects of Antarctic fishes (Notothenioidei) Dissertation zur Erlangung des Doktorgrades der Mathematisch-Naturwissenschaftlichen Fakultät der Christian-Albrechts-Universität zu Kiel vorgelegt von Malte Damerau Kiel, Oktober 2013 Referent: PD Dr. Reinhold Hanel Korreferent: Prof. Dr. Thorsten Reusch Tag der mündlichen Prüfung: 20.12.2013 Zum Druck genehmigt: 20.12.2013 Kiel, Der Dekan SUMMARY In this thesis, population genetic structures and evolutionary aspects of speciation in notothenioid fishes from the Southern Ocean have been investigated. Special emphasis was given to the role of pelagic larval dispersal on gene flow between geographically separated populations, since notothenioids are characterized by unusually long pelagic larval durations of up to one year, which is assumed to counteract genetic divergence of populations and ultimately allopatric speciation processes. By elucidating the population genetic structures of selected notothenioid species, inferences were made about the level of gene flow between populations. The major goal of this thesis was to compare the population genetic structures of sympatric species within the Atlantic sector of the Southern Ocean to determine factors responsible for regulating gene flow. Species-specific traits, such as larval durations, were expected to result in differences between the observed patterns, while environmental factors, such as oceanographic currents or frontal systems, were assumed to influence multiple species in a similar way. In addition, it has been tested whether the evolution of notothenioids fulfills the criteria of an adaptive radiation, of which only a few examples are known from the marine realm. In Chapter I, the population genetic structure of seven notothenioid species from the southern Scotia Arc, collected at the area of the Antarctic Peninsula and South Orkney Islands, have been compared with mitochondrial DNA sequences and microsatellite markers. The investigated species comprise three crocodile icefishes (Channichthyidae: Chaenocephalus aceratus, Champsocephalus gunnari, Chionodraco rastrospinosus) and four cod icefishes (Nototheniidae: Gobionotothen gibberifrons, Lepidonotothen squamifrons, Trematomus eulepidotus, T. newnesi). The results show that in the investigated area, populations of all species are genetically not significantly differentiated over distances of about 250 km, and that the direction of gene flow is in congruence with the prevailing current of the Antarctic Circumpolar Current (ACC). The results from this comparative approach highlight the role of passive larval dispersal with the currents for gene flow. The only exceptions are the channichthyids C. aceratus and C. gunnari, which show a small, but significant differentiation with microsatellite markers. In order to investigate the role of larval dispersal on gene flow on a larger geographic scale, the population genetic structures of C. aceratus and C. gunnari have been investigated over large parts of their distribution range in the Atlantic sector of the Southern Ocean (Chapter II). More specifically, populations at the Antarctic Peninsula region, South Orkney Islands, South Georgia Island and Bouvet Island, which are connected by the ACC, but separated by long stretches of deep ocean basins, were investigated. The examined populations show significant differentiation except for the area of the southern Scotia Arc. Therefore, long distances of open ocean seem to restrict gene flow. At the same time, levels of self-recruitment are high indicating that larvae are effectively retained near their spawning locations. In addition, the levels of population divergence are likely influenced by demographic factors, such as effective population sizes and generation times. Population size reductions during the last glacial maximum inferred from Bayesian Skyline Plots (BSPs) indicate that sub- V Antarctic populations are largely influenced by glacial cycles, similar to populations in the high-Antarctic realm, further driving population divergences and speciation events. In Chapter III, the population genetic structure of the nototheniid Lepidonotothen larseni in the Atlantic sector of the Southern Ocean has been examined, whose early pelagic developmental stages are among the longest known from notothenioids (about 18 months). The results indicate significant population structure among specimens from South Orkneys, South Georgia and Bouvet Island. In combination with the results of Chapter II, the study suggests that the pelagic larval time per se does not imply high levels of gene flow in notothenioids, although it allows for occasional long-distance dispersal. Consequently, it can be assumed that allopatric speciation (in its peripatric subform) plays a major role in the evolution of notothenioid fishes, similar to Antarctic invertebrates, which are characterized by short, if at all, pelagic larval stages. In Chapter IV, the ecological diversification of notothenioids has been tested as evidence for an adaptive radiation. Based on stable carbon (C) and nitrogen (N) isotopes, 25 species were characterized for their feeding ecology and foraging habitats to test whether ecological diversification along the benthic-pelagic axis followed a single directional trend or evolved independently in several lineages. Phylogenetic and isotopic disparity-through-time analyses showed that the trophic diversification did not follow a single directional trend but evolved several times in parallel within different notothenioid lineages possibly as a result of interspecific competition, which is characteristic for adaptive radiations. The results presented in this thesis show that gene flow between notothenioid populations is highly restricted in the Atlantic sector of the Southern Ocean, despite a high potential for gene flow by long pelagic larval phases and strong oceanographic currents. Moreover, the degrees of population divergences seem to be further related to demographic factors and specific life-history traits, such as generation-time-effects and spawning behavior (inshore vs. offshore). Allopatric speciation in the subform of peripatric speciation is a highly eligibile mode of speciation in sub-Antarctic notothenioids and may have been driven by glacial periods, during which population sizes were substantially decreased, similar to high-Antarctic species and Antarctic invertebrates. In addition, the ecological diversification of notothenioids is in congruence with an adaptive radiation. VI ZUSAMMENFASSUNG In dieser Doktorarbeit wurden die populationsgenetischen Strukturen und weitere evolutionäre Aspekte von Artbildungsprozessen innerhalb von Antarktisfischen (Notothenioidei) aus dem Südpolarmeer untersucht. Ein besonderer Schwerpunkt war es, den Einfluss pelagischer Larvenverdriftung auf den Genfluss zwischen geografisch getrennten Populationen zu ermitteln, da notothenioide Fische durch ungewöhnlich lange, pelagische Larvenphasen von bis zu über einem Jahr charakterisiert sind, wodurch erhöhter Genfluss einer Auseinanderentwicklung von Populationen und damit auch allopatrischer Artbildung entgegen wirken kann. Die Untersuchung der populationsgenetischen Strukturen erlaubt es, Rückschlüsse auf das Ausmaß des genetischen Austauschs zwischen Populationen zu ziehen. Das Hauptziel dieser Arbeit war es, durch einen Vergleich der genetischen Populationsstrukturen sympatrischer Arten, Faktoren zu identifizieren, die maßgeblich den Genfluss beeinflussen. Dabei wurde angenommen, das artspezifische Merkmale, wie z. B. die Dauer der Larvenphase, in Unterschieden zwischen den beobachteten Populationsstrukturen zum Ausdruck kommen, während Umweltfaktoren, wie ozeanografische Strömungen und Fronten, verschiedene Arten gleichermaßen beeinflussen. Des weiteren wurde untersucht, ob die Evolution der Antarktisfische den Kriterien einer Adaptativen Radiation entspricht, für welche es im marinen Lebensraum bisher nur wenige bekannte Beispiele gibt. In Kapitel I wurden, basierend auf mitochondrialen Gensequenzen und Mikrosatelliten, die populationsgenetischen Strukturen von sieben notothenioiden Arten verglichen, die am südlichen Schottischen Bogen im Gebiet der Antarktischen Halbinsel und den Südlichen Orkneyinseln vorkommen. Zu den untersuchten Arten gehören drei Krokodileisfische (Channichthyidae: Chaenocephalus aceratus, Champsocephalus gunnari, Chionodraco rastrospinosus) und vier Antarktisdorsche (Nototheniidae: Gobionotothen gibberifrons, Lepidonotothen squamifrons, Trematomus eulepidotus, T. newnesi). Die Ergebnisse zeigen, dass im Untersuchungsgebiet die Populationen aller Arten über eine Distanz von ca. 250 km genetisch nicht oder nur marginal zu differenzieren sind und dass die Richtung des Genflusses mit der der vorherrschenden Strömungsrichtung des Antarktischen Zirkumpolarstromes übereinstimmt. Die Ergebnisse dieser vergleichenden Untersuchung unterstreichen die Bedeutung passiver, pelagischer Larvenverdriftung mit der Strömung für den Genfluss. Die einzigen Ausnahmen waren die Krokodileisfische C. aceratus und C. gunnari, die anhand von Mikrosatelliten eine geringe, aber dennoch signifikante genetische Differenzierung zeigten. Um den Einfluss der Verdriftung pelagischer Entwicklungsstadien auf den Genfluss eingehender zu untersuchen, wurden in Kapitel II die populationsgenetischen Strukturen von C. aceratus und C. gunnari über weite Teile ihres Verbreitungsgebietes im atlantischen Sektor des Südpolarmeeres analysiert. Hierbei
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