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Impact of Gamete Production on Breeding Systems And Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2013 Impact of gamete production on breeding systems and population structure of hybridogenetic frogs of the Pelophylax esculentus complex: The evolutionary potential of interspecific hybridization Pruvost, Nicolas B M Abstract: The European water frog Pelophylax esculentus (genome LR) is a natural hybrid between P. lessonae (LL) and P. ridibundus (RR). It presents a peculiar quasi-sexual reproductive mode known as hybridogenesis: the hybrid excludes one of the parental species’ genomes at a pre-meiotic stage of gametogenesis, thus producing gametes containing clonal copies of the other parental genome. By mating with the parental species whose genome has been excluded it re-establishes hybridity at each generation. Moreover, because of its hybrid nature and resulting problems of chromosome pairing at gametogenesis, P. esculentus also produces diploid gametes from time to time. These gametes often lead to the generation of triploid frogs which will allow, under certain ecological conditions, the establishment of all hybrid populations which are maintained without the genetic contribution of either parental species. Over the past decade, such populations have been well studied in the north-western part of Europe, but the presence of triploid water frogs has also been reported for various areas in Central Europe. However, for those localities details on the breeding system, i.e. the genetic contribution of the various frog types, are usually lacking. The major goals of this thesis were to (a) investigate the Central European populations more closely, (b) to compare the breeding systems there with that in all-hybrid populations from Northern Europe and (c) find out whether triploid water frogs in different areas are ofmono- or polyphyletic origin. In chapter one I used microsatellite DNA analyses and crossing experiments to compare five populations (one in Poland, two in Germany and two in Slovakia) presenting different population structures. Indices of 2 heterozygosity and of genetic differentiation allowed to depict the genetic interactions between the different type of frogs (LL, LLR, LR, LRR and RR). I was then ableto define and differentiate the breeding systems occurring in each of them and to propose an evolutionary scenario for the appearance and maintenance of the all-hybrid populations. Chapter two presents a collaborative study with Alexandra Hoffmann. Here we enlarged our survey to populations distributed all over Europe and used microsatellite DNA and mitochondrial DNA (mtDNA) analyses to find patterns of genetic structure among different breeding system types. We found that genetic diversity among hybrid populations is influenced by geographic location (latitude, longitude) and by the proportions of parental genotypes in the hybrid population. Furthermore, we identified genetic clusters from both microsatellites and mtDNA, which indicate that there are at least two separate polyploid hybrid clades existing today: one in Northern and East- Central Europe and one in Eastern Europe (Eastern Ukraine). Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-86529 Dissertation Published Version Originally published at: Pruvost, Nicolas B M. Impact of gamete production on breeding systems and population structure of hybridogenetic frogs of the Pelophylax esculentus complex: The evolutionary potential of interspecific hybridization. 2013, University of Zurich, Faculty of Science. 2 IMPACT OF GAMETE PRODUCTION ON BREEDING SYSTEMS AND POPULATION STRUCTURE OF HYBRIDOGENETIC FROGS OF THE PELOPHYLAX ESCULENTUS COMPLEX: THE EVOLUTIONARY POTENTIAL OF INTERSPECIFIC HYBRIDIZATION Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Nicolas B.M. Pruvost aus Frankreich Promotionskomitee Prof. Dr. Heinz-Ulrich Reyer (Vorsitz und Leitung) Prof. Dr. Christian Lehner Prof. Dr. Maria Ogielska Zürich 2013 « Le biologiste passe, la grenouille reste » J. Rostand Illustration : Water frog couple, from August Rösel von Rosenhof, in Historia naturalis Ranarum nostratium, 1758 Contents 1 Contents Summary ............................................................................... 2 Zusammenfassung ............................................................... 5 General introduction ............................................................ 8 Chapter 1 Gamete production patterns, ploidy and population genetics reveal evolutionary significant units in hybrid water frogs (Pelophylax esculentus) (Later version published in Ecology and Evolution 2013, doi:10.1002/ece3.687) ........................................ 23 Chapter 2 Genetic diversity and distribution patterns of diploid and polyploid water frogs (Pelophylax esculentus) across a large area of Europe ........................................................... 60 Chapter 3 Unisexual paternal lineage of triploid water frogs (Pelophylax esculentus) from Central Europe ............................................................... 117 Chapter 4 Genotype-temperature interactions on larval performance shape population structure in hybridogenetic water frogs (Pelophylax esculentus complex) (Functional Ecology 27, 2013, pp.459-471) .............................................. 154 Chapter 5 Genetic and cytogenetic characteristics of pentaploidy in water frogs (Herpetologica 69, 2013, pp.36-45) .................................................. 190 Acknowledgements .............................................................. 227 Curriculum Vitae ................................................................... 229 2 Summary Summary The European water frog Pelophylax esculentus (genome LR) is a natural hybrid between P. lessonae (LL) and P. ridibundus (RR). It presents a peculiar quasi-sexual reproductive mode known as hybridogenesis: the hybrid excludes one of the parental species’ genomes at a pre-meiotic stage of gametogenesis, thus producing gametes containing clonal copies of the other parental genome. By mating with the parental species whose genome has been excluded it re-establishes hybridity at each generation. Moreover, because of its hybrid nature and resulting problems of chromosome pairing at gametogenesis, P. esculentus also produces diploid gametes from time to time. These gametes often lead to the generation of triploid frogs which will allow, under certain ecological conditions, the establishment of all hybrid populations which are maintained without the genetic contribution of either parental species. Over the past decade, such populations have been well studied in the north-western part of Europe, but the presence of triploid water frogs has also been reported for various areas in Central Europe. However, for those localities details on the breeding system, i.e. the genetic contribution of the various frog types, are usually lacking. The major goals of this thesis were to (a) investigate the Central European populations more closely, (b) to compare the breeding systems there with that in all-hybrid populations from Northern Europe and (c) find out whether triploid water frogs in different areas are of mono- or polyphyletic origin. In chapter one I used microsatellite DNA analyses and crossing experiments to compare five populations (one in Poland, two in Germany and two in Slovakia) presenting different population structures. Indices of heterozygosity and of genetic differentiation allowed to depict the genetic interactions between the different type of frogs (LL, LLR, LR, LRR and RR). I was then able to define and differentiate the breeding systems occurring in each of them and to propose an evolutionary scenario for the appearance and maintenance of the all-hybrid populations. Summary 3 Chapter two presents a collaborative study with Alexandra Hoffmann. Here we enlarged our survey to populations distributed all over Europe and used microsatellite DNA and mitochondrial DNA (mtDNA) analyses to find patterns of genetic structure among different breeding system types. We found that genetic diversity among hybrid populations is influenced by geographic location (latitude, longitude) and by the proportions of parental genotypes in the hybrid population. Furthermore, we identified genetic clusters from both microsatellites and mtDNA, which indicate that there are at least two separate polyploid hybrid clades existing today: one in Northern and East- Central Europe and one in Eastern Europe (Eastern Ukraine). In chapter three I focused on eight Czech and Slovak populations. Using microsatellite DNA analyses, flow cytometry and crossing experiments I was able to enlighten and describe a new breeding system type of hybrid water frog populations, the “modified LE-system”. It is characterized by a triploid lineage consisting of males only. Chapter four takes a more ecological approach where I was looking for fitness differences in larval life history traits between the three hybrid types (diploid LR and two type of triploids LLR and LRR) and their parental species (LL and RR) when raised under two temperature regimes. Diploid and triploid hybrids performed better than their parental species under colder conditions. This finding helps to explain why all hybrid populations dominate in the colder northern part of the species distribution. Chapter five also presents a collaborative study
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