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Exploring Reticulate Evolution and Its Consequences for Phylogenetic Reconstruction

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Exploring Reticulate Evolution and Its Consequences for Phylogenetic Reconstruction phylogenetworks EXPLORING RETICULATE EVOLUTION AND ITS CONSEQUENCES FOR PHYLOGENETIC RECONSTRUCTION Bastienne Vriesendorp Promotor: Prof. dr. M.S.M. Sosef Hoogleraar Biosystematiek Wageningen Universiteit Co-promotoren: Dr. F.T. Bakker Universitair Docent, leerstoelgroep Biosystematiek Wageningen Universiteit Dr. R.G. van den Berg Universitair Hoofddocent, leerstoelgroep Biosystematiek Wageningen Universiteit Promotiecommissie: Prof. dr. J.A.M. Leunissen (Wageningen Universiteit) Prof. dr. E.F. Smets (Universiteit Leiden) Prof. dr. P.H. van Tienderen (Universiteit van Amsterdam) Dr. P.H. Hovenkamp (Universiteit Leiden) Dit onderzoek is uitgevoerd binnen de onderzoekschool Biodiversiteit phylogenetworks EXPLORING RETICULATE EVOLUTION AND ITS CONSEQUENCES FOR PHYLOGENETIC RECONSTRUCTION Bastienne Vriesendorp Proefschrift ter verkrijging van de graad van doctor op gezag van de rector magnificus van Wageningen Universiteit Prof. dr. M.J. Kropff in het openbaar te verdedigen op woensdag 12 september 2007 des namiddags te vier uur in de Aula Bastienne Vriesendorp (2007) Phylogenetworks: Exploring reticulate evolution and its consequences for phylogenetic reconstruction PhD thesis Wageningen University, The Netherlands With references – with summaries in English and Dutch ISBN 978-90-8504-703-2 aan mijn ouders CONTENTS chapter 1 General Introduction 9 chapter 2 Hybridization: History, terminology and evolutionary significance 15 chapter 3 Reconstructing patterns of reticulate evolution in angiosperms: what can we do? 41 chapter 4 Mosaic DNA sequences and their effect on phylogenetic tree reconstruction: simulations involving recombination and hybridization 57 chapter 5 Exploring network methods performance using angiosperm species-level DNA sequence data sets 83 chapter 6 AFLPs and hybrid detection – a case study of Solanum 103 chapter 7 Towards species trees 127 chapter 8 General discussion 143 literature cited 151 summary 173 samenvatting 175 nawoord 179 curriculum vitae 181 Chapter 1 Reticulate evolution is the collective name for processes such as hybridization, recombination or other events involving gene transfer between individual organisms or lineages. This thesis is about reticulate evolution and its implications for phylogenetic reconstruction. Reticulate evolution comes from the Latin reticulum, a diminutive for net. So, literally it means net-like evolution, which describes evolutionary events where independent lineages exchange genetic information, causing branches in an evolutionary tree to come together, i.e. forming a “net” (or network). This is in contrast with bifurcating evolution, where branches in an evolutionary tree split into new lineages and evolve independently from another. Reticulation, hence the exchange of genetic information, can occur at multiple levels: chromosomal level (meiotic recombination), organism level, population level and species level, but the focus in this work is on reticulation at species-level. Evolution at species-level is normally seen as the accumulation of mutational changes within evolutionary lineages (i.e. substitutions, deletions, insertions, etc.) that are passed on to the new generation leading to a bifurcating evolutionary pattern. However, reticulate evolution implies genetic changes that may also arise from gene transfer between different lineages. The most obvious reticulate processes that may occur at species-level are related to hybridization (such as hybrid speciation, introgression, introgressive hybridization) and horizontal gene transfer (the exchange of genetic material via an external vector such as a virus). Other evolutionary processes can mimic species-level reticulation and will produce the same signature, such as incomplete lineage sorting of ancestral alleles and recombination (i.e. reticulation at lower levels). Whereas a large body of literature has been published to build up insights in the evolutionary and ecological significance of hybrids, the same cannot be said for the general phenomenon of reticulate evolution. Naturally, underlying processes are often discussed in terms of hybridization and throughout this thesis most data sets are based on studies that include putative hybrid species. However, when reticulate phylogenetic patterns are discussed and evaluated in this thesis, this relates to the general case of reticulate evolution and not solely to underlying hybridization events. While many studies focus on processes, e.g. study the frequency and mechanisms of hybrid speciation, others focus on the resulting character patterns. Also, in phylogenetic reconstruction it can be important to recognize these patterns either before or after an analysis. 10 General introduction When reticulation has occurred, one may expect specific character patterns in the involved species. The “signature” of reticulate evolution may be an “average” of its parents as expected for morphological characters (e.g. pink flowers from a white- and red-flowered parent or sparsely hairy plants from a glabrous and a hairy one), where probably several different genes are involved in the expression of the character. However, characters may also reveal a conflicting signal, when an organism has obtained some characters from one and some from the other parent. Alternatively, additive patterns can be observed, e.g. multiple copies of nrDNA genes may result in the identification of polymorphic sites that represent the base positions of either parent. Also, markers such as AFLPs are expected to reveal an additive pattern, where both unique band positions of the parents might be observed in the hybrid. Therefore, it seems good to concentrate on what patterns may evolve from reticulate evolution and how to properly interpret them given the data. The main focus in this thesis is on data incongruence as representation for an underlying reticulate pattern, using different parts of DNA sequence alignments that are incompatible with each other. A reticulate pattern does of course not necessarily implicate underlying reticulate historical processes. Different sources of data error or random noise may cause the same pattern of incongruence, such as taxonomic and character sampling artefacts, random error in site readings, compositional bias, etc. Based on the variety of reticulate patterns and their causes, a range of different methods exist to detect and/or represent reticulation. In phylogenetic reconstruction at species-level, hybrids are often left out of the analysis, because they are considered to disrupt the reconstruction of (bifurcating) phylogenetic trees that do not allow for reticulate patterns. However, specific network methods have been developed that may detect reticulation between lineages and may represent the (reticulate) evolutionary relationships in a graphical way. These methods allow conflicting phylogenetic signals to be displayed in a network and are mainly based on the incongruence between different molecular markers. While most of these network methods were originally applied at population-level to simplify the non-hierarchical relationships, they can also be applied to species-level to represent the reticulate phylogenetic patterns. This thesis is aimed at describing the different aspects of reticulate evolution, the patterns in the data and the resulting phylogeny that may emerge from it, and its consequences for phylogeny reconstruction in general. 11 Chapter 1 In plant systematics, reticulate evolution usually involves hybridization. To first clarify the possible confusion in terminology related to hybrids and hybridization processes, the first part of the introductory Chapter 2 presents an overview of the terminology. The second part provides a brief history on studies related to hybrids and describes the different views on the evolutionary significance of plant hybridization. The rest of the thesis is outlined as follows: the third chapter treats the implications of plant hybrids for systematics and phylogeny reconstruction, describing the treatment of hybrids in recent phylogenetic studies, possible problems, and providing a conceptual framework for hybrid terminology. Testing of the actual influence of hybrid terminals (represented by mosaic terminals) on phylogenetic analysis is performed in Chapter 4, while Chapter 5 involves testing of the performance of a selection of network methods. In the following Chapter 6 the behaviour and suitability of AFLPs in hybrid studies is explored using an ancient hybrid species of Solanum plus its re-synthesized F1 hybrid. Chapter 7 explores the possibilities of methods that reconcile gene trees into a species tree to contribute to the representation of organisms instead of character-level networks. Finally, Chapter 8 provides a summary of the most important conclusions and describes the consequences of reticulate evolution for taxonomy and classification. 12 General introduction 13 Chapter 2 INTRODUCTION Hybrids are being studied in various contexts, such as speciation processes, population genetics, molecular evolution of characters in hybrids, occurrence of hybrids in phylogenies, or within crossing experiments, with applications across many different fields of expertise (i.e. genetics, ecology and systematics). Accordingly, it is not surprising that the concepts and terminology relating to hybrids is not uniform across these fields and therefore not always straightforward. Here I will first give an overview of the wealth of definitions and concepts that are used to describe hybrids or implicitly implied in studies
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