Genetic Basis of Innovative Anal Fin Pigmentation Patterns in Cichlid Fish

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Genetic Basis of Innovative Anal Fin Pigmentation Patterns in Cichlid Fish Genetic basis of innovative anal fin pigmentation patterns in cichlid fish Inauguraldissertation Zur Erlangung der Würde eines Doktors der Philosophie Vorgelegt der Philosophisch-Naturwissenschaftlichen Fakultät der Universität Basel von Langyu Gu von China Basel, 2016 Originaldokument gespeichert auf dem Dokumentenserver der Universität Basel edoc.unibas.ch Genehmigt von der Philosophisch-Naturwissenschaftlichen Fakultät auf Antrag von Prof. Dr. Walter Salzburger, Prof. Dr. Alistair McGregor Basel, June, 21st, 2016 Prof. Dr. Jörg Schibler The Dean of Faculty Table of Contents Abstract 1 Chapter 1: Introduction 3 Aim of my PhD project 10 Thesis outline 10 References 11 Chapter 2 Comparative transcriptomics of anal fin pigmentation patterns in cichlid fishes 15 BMC Genomics, 2016, 17: 712. Chapter 3 The genetic basis of convergent evolution of two innovative anal fin pigmentation patterns in East African cichlid fish ——haplochromine eggspots and ectodine blotches 35 Abstract 37 Introduction 38 Materials and Methods 41 Results and Discussion 44 Conclusion 62 Acknowledgements 63 References 63 Supplementary information 73 Chapter 4 Gene network rewiring of the repeated evolution of innovative anal fin pigmentation patterns in cichlid fish 95 Abstract 97 Introduction 98 Methods and Materials 102 Results 104 Discussion 108 Conclusion 111 Acknowledgements 112 References 112 Supplementary information 117 Chapter 5 Expansion via duplication of a multiple-ligand transporter related gene family in cluster in teleost fish 147 Abstract 149 Introduction 149 Materials and Methods 152 Results 156 Discussion 163 Conclusion 168 Acknowledgements 169 References 169 Supplementary files 175 Chapter 6 Discussion and further perspectives 189 References 194 Acknowledgements 197 Curriculum Vitae 199 Abstract The origination of novelty is one of the most fascinating questions in evolutionary biology. The repeated evolution of innovative pigmentation patterns on the anal fin in East African cichlid fish is an ideal model to study this question. One pattern is eggspots, the circular pigmentation pattern with a transparent outer ring that emerged once in the most species rich cichlid lineage, the haplochromines, exhibiting large varieties with different numbers, sizes and colours. Eggspots have been suggested to be involved in female attraction, male-male competition and species recognition. While ancestral haplochromine species feature another fin pigment trait in form of blotch, which is reddish with ill-defined boundary. Anal fin pigmentation pattern was also independently evolved in the ectodine lineage, which possesses similar blotch pattern as the haplochromine blotch. The ectodine blotch pattern was also suggested to be involved in female attraction, although less investigated. Unlike haplochromine eggspots, the ectodine blotch shows almost no variation among species. Here, by applying next generation sequencing technology (RNAseq and Ion Torrent sequencing) followed by a series data analysis, we found that haplochromine eggspots and the ectodine blotch share at least parts of a common gene network. Further sequencing data showed that many of the anal fin pigmentation related candidate genes have eggspots specific segregating patterns. While species with the blotch showed similar sequence patterns with species without anal fin pigmentation patterns. This might suggest that eggspots, but not the ectodine blotch, might have a much more independent gene network, which might explain its higher evolvability. Besides, we also described the evolutionary history of apolipoprotein D (ApoD) gene family in teleosts, whose expansion is via gene duplication and are located in two clusters in teleost fish. One member of this gene family was found to be highly expressed in the ectodine blotch. Interestingly, although most genes showed conserved homologous expression pattern in distant related teleosts, duplicated genes with new functions evolved in a lineage specific manner, especially in cichlid fish, and were expressed in two novelties, lower pharyngeal jaw and anal fin pigmentation. By investigating the genetic basis of the innovative anal fin pigmentation patterns in cichlid fish, this doctoral work gives clues about the relationship among evo-devo, novelty and biological diversity. 1 2 Chapter 1 Introduction 3 4 Chapter 1 Introduction The origination of novelty is one of the most fascinating questions in evolutionary biology; especially since it is challenging in the light of Darwin’s theory with its natural selection centralism (Darwin 1859; Pigliucci and Müller 2010; Laland et al. 2015). Evolutionary novelties, defined as “is a structure that neither homologous to any structure in the ancestral species nor serially homologous to any part of the same organism” (Müller and Wagner 1991) provide the raw material for downstream selection and adaptation. That way, evolutionary novelties may contribute to biodiversity, as examplified by the beak of birds (Bhullar et al. 2015; Bright et al. 2016), eyespots in the family nymphalidae in butterfly (Monteiro 2015), or the neural crest in vertebrates (Green et al. 2015). In spite of being a hot topic for a long period in evolutionary biology, several basic questions regarding the origination of novelty are still unclear (Wagner 2014). For example, what is the mechanism of the origination and evolution of morphological novelty? Why do some novelties result in much higher evolvability, while others are less variable? Recent re-burning of evolutionary developmental biology (evo-devo) theory combining with next generation sequencing technology provide an unprecedented opportunity to answer these questions (Lynch et al. 2011; Wagner 2012; Roux et al. 2015). With this background, therefore, in my PhD thesis, I addressed questions about the origination and evolution of novelty by focusing on the genetic basis of two convergent innovative anal fin pigmentation patterns in East African cichlid fish, haplochromine eggspots and ectodine botches in East African cichlid fish (Fig.1). 5 egg?spots Lake%Victoria blotches Lake%Malawi haplochromini A.#burtoni Tropheini Pseudocrenilabrus Eretmodini Ectodini:%C.#macrops Cyphotilapiini Limnochromini Perissodini Cyprichromini Lamprologini Bathybatini Trematocarini Tilapiini Fig. 1 Convergent evolution of anal fin pigmentation patterns in East African cichlid fish. Schematic molecular phylogeny of the East African cichlid fishes based on combined evidence from Salzburger et al., 2005; Meyer et al., 2015; Takahashi and Sota, 2016 . Triangle symbol represented species richness based on studies from Salzburger et al., 2005 and https://en.wikipedia.org. Names on the right side indicated rivers or tribes. What is a morphological novelty Previously, novelty was defined as “is a structure that neither homologous to any structure in the ancestral species nor serially homologous to any part of the same organism” (Müller and Wagner 1991). Therefore, understanding the concept of homology is the pre-request to understand what is novelty. However, the definition of homology itself is inconclusive (Wake 1994). For example, inference of homology in digit identity in birds and skinks is based on conflicting evidences from character anatomy, phylogenetic distribution and embryological position (Wagner 2005). Based on developmental experimental data, conserved developmental regulatory genes underlying the maintenance of character identity were found across taxa, such as the Hox gene clusters (Carroll 1995). However, most of times, homologous characters could also exhibit a huge diversity across taxa. It seems that many characters themselves have some sort of modularity, and the corresponding gene-gene interactions can be hierarchically structured for the phenotype with the core gene network being conserved among homologous characters (Wagner et al. 2007; Pigliucci and Müller 2010). Wagner (Wagner 2007) proposed that conserved Character Identity Networks (CHINs) maintained by transcription factors (TFs) is the basis of character homology, while the activation of the expression of CHINs, or the effectors that ultimately express CHINs can be flexible, which can explain the divergence of homologous characters. For example, epistatic 6 interactions between TFs FoxD3, SoxE, Snai1/2 and Pax3/7 constitute a very conserved module of neural crest specification (Green et al. 2015); or 5’-HoxD, which plays a ubiquitous role in digit development (Andrey et al. 2013). With this background in mind, novelty is the evolution of a quasi-independent CHINs to integrate signals into a gene expression pattern unique to that organ, so that it can obtain individuality from ancestral character (Wagner 2014). In this case, the study of evolutionary novelties is to explain the origin of the core gene regulatory network, which executes organ-specific gene expression patterns. Whether these networks are modifications from ancestral gene regulatory networks, or are assembled de novo is an open question. Why do we study morphological novelty The origination of novelty is one of the most challenging question of Darwin’s theory, which is centered around natural selection (Darwin 1859; Pigliucci and Müller 2010; Laland et al. 2015). However, in the case of the evolution of novel traits, natural selection may only be the downstream force and follows the evolution of “raw phenotypic materials”, while the intrinsic developmental factors themselves should not be ignored. The recently growing field of evolutionary development biology (evo-devo)
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