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Genetic Structure and Dynamics of All-Hybrid Edible Frog Populations ______ Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2010 Genetic structure and function of all-hybrid edible frog populations Christiansen, Ditte Guldager Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-24569 Dissertation Published Version Originally published at: Christiansen, Ditte Guldager. Genetic structure and function of all-hybrid edible frog populations. 2010, University of Zurich, Faculty of Science. Genetic Structure and Dynamics of All-hybrid Edible Frog Populations ______________________________________________ Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Ditte Guldager Christiansen aus Dänemark Promotionskomitee Prof. Dr. Heinz-Ulrich Reyer (Vorsitz und Leitung) Prof. Dr. Lukas Keller Prof. Dr. Trevor J. C Beebee Zürich 2010 Genetic structure and function of all-hybrid edible frog populations by Ditte Guldager Christiansen PhD thesis at Ecology, Zoological Institute University of Zurich, Switzerland October 2009 Supervisors / examiners: Heinz-Ulrich Reyer Lukas Keller Trevor J. C. Beebee Leo Beukeboom Contents 1 Contents Summary…… ............................................................................................................................ 2 Zusammenfassung...................................................................................................................... 5 General introduction................................................................................................................... 9 Chapter 1: From clonal to sexual hybrids: genetic recombination via triploids in all-hybrid populations of water frogs. ............................................................................... 15 (Evolution 2009, vol 63, pages 1754-1768) ..................................................... 16 Chapter 2: Gamete types, sex determination and stable equilibria of all-hybrid populations of diploid and triploid edible frogs (Pelophylax esculentus)............................ 15 (BMC Evolutionary Biology 2009, vol 9, article 135) ..................................... 48 Chapter 3: Coexistence of diploid and triploid hybrid water frogs: population differences persist in the apparent absence of differential survival. ................................... 15 (Later version published in BMC Ecology 2010, vol 10, article 14)................ 83 Chapter 4: The effects of geographic distance, sea barriers and ecology on the genetic structure and diversity of all-hybrid water frog populations. ........................... 15 (Later version published in Heredity, doi:10.1038/hdy.2010.37) .................. 112 Curriculum vitae..................................................................................................................... 139 Summary 2 Summary Hybridization is quantitatively important on an evolutionary scale and has several consequences. One consequence is the formation of new taxa. Most hybrid plant taxa are sexual species formed by tetraploidization, whereas many animal hybrid taxa have some form of clonal reproduction and are therefore considered evolutionary dead ends. The European hybrid edible frog, Pelophylax esculentus, is a biologically unique hybrid, because it forms three different breeding systems. In two of the breeding systems, the hybrids reproduce clonally with one or the other parental species. In contrast, the third breeding system consists of all-hybrid populations where the hybrids are 1) reproductively independent and 2) might have sexual reproduction with genetic recombination. These two points represent two important steps towards speciation. P. esculentus is a hybrid between the pool frog, P. lessonae (genotype LL), and the marsh frog, P. ridibundus (genotype RR). In the all-hybrid populations, hybrids are either diploid, LR, or triploid, LLR or LRR. LR frogs make LR and/or R gametes, LLR frogs make L gametes and LRR frogs make R gametes. Frogs of different genotypes are thus dependent on mating with each other for reproduction. The present PhD thesis comprises four independent chapters, about all-hybrid populations, all aiming to increase our understanding of the structure and dynamics of all-hybrid populations of P. esculentus. In chapter 1 it is demonstrated that all-hybrid populations of diploid (LR) and triploid (LLR and LRR) P. esculentus have indeed acquired sexual reproduction. This is of evolutionary importance for the hybrids, because clonal reproduction comes at the expense of genetic diversity and the ability to purge deleterious mutations. First, microsatellite marker analysis on parents and offspring from a crossing experiment showed that triploid hybrids of both sexes and genotypes (LLR and LRR) recombined their homospecific genomes. Second, the great majority of natural populations investigated had low multilocus linkage disequilibrium, indicating a high recombination rate. As predicted from mating system models, the L genome had constant, low levels of linkage disequilibrium, whereas linkage disequilibrium in the R genome showed a significant reduction with increasing proportion of recombining triploids. This direct evidence of sexual reproduction in P. esculentus calls for a change of the conventional view of hybridogens as clonally reproducing diploids. Rather, hybridogens can be independent sexually reproducing units with an evolutionary potential. Chapter 2 provides data and interpretations on gamete types and sex determination that are essential for understanding the function and evolutionary potential of and the threats to Summary 3 this intriguing system. Gamete patterns in hybrids are generally interesting, because triploid individuals often play a key role in speciation by hybridization. An understanding of the gamete types (ploidy and genomic content) and stability of hybrid populations with triploid individuals is therefore of importance for exploring the role of hybridization in evolution. Dissection of metamorphs from a crossing experiment confirmed that sex determination in the all-hybrid populations is an XX-XY system with the Y confined to the L genome. From microsatellite analysis of the crossed parents and their offspring, gamete frequencies could be deduced: Triploids of both sexes mostly made haploid gametes with the genome they had in double dose, however LLR females also made approximately 10% LL gametes by automixis. LR frogs showed much variation in their gamete production: In LRR-rich populations, their LR sperm production was sufficiently high (22%) to explain the observed proportion of LRR males, the formation of which has not previously been understood. This suggests that all- hybrid populations constitute not one, but several intrinsically different breeding systems. A model was constructed to calculate equilibrium genotype proportions for different population types on the basis of the gamete proportions found. These equilibria agreed well with empirical literature data. The model also predicted that tetraploidization could occur if the survival or fertility of both males and females increased. Whether introduction of hybrid or parental species individuals with new genetic variation would threaten the all-hybrid populations by promoting the survival of non-hybrids cannot be predicted without further knowledge about the mechanisms behind non-hybrid inviability. However, at least R genomes with Y factor are predicted to be invasive, if introduced, and would burden the all-hybrid populations with increased mortality from non-hybrid production. Chapter 3 aims to asses the importance of selection in structuring all-hybrid Pelophylax esculentus populations. The role of differential selection in determining the geographic distribution of genotypes in hybrid systems has long been discussed, but not settled. With data from 12 Swedish ponds, it is first shown that - in spite of significant genotype proportion changes over time - the most extreme ponds retained their differences over a six years’ study period. The predominance of different genotypes in different ponds could be a consequence of differential selection varying between ponds (selection hypothesis), or, alternatively, of different gamete production patterns among ponds (gamete pattern hypothesis). The selection hypothesis was tested in adults by a mark-recapture study in the 12 ponds. As the relative survival and proportion of LLR, LR and LRR did not correlate within ponds, this study provided no evidence for the selection hypothesis in adults. Then, both hypotheses were tested simultaneously in juvenile stages (eggs, tadpoles, Summary 4 metamorphs and one-year old froglets) in three of the ponds. A gradual approach to adult genotype proportions through successive stages would support the selection hypotheses, whereas the presence of adult genotype proportions already at the egg stage would support the gamete pattern hypothesis. The result was a weak preference for the gamete pattern hypothesis. These results thus suggest that selection is of little importance for shaping genotype distributions of all-hybrid populations of P. esculentus, but that further studies are needed for a confirmation. Moreover, the study provided valuable data on genotype-specific body lengths, adult survival and sex ratios. Chapter 4 analyzes the genetic structure and diversity of P. esculentus in the Danish archipelago and adjacent
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