Comparative genomics in teleost fish: Insights into forces driving genome evolution

• Published in: Genome Biology and Evolution
• Main Author: Varadharajan, Srinidhi
• Format: Doctoral or Postdoctoral Thesis
• Language: English
• Published: 2019
• Subjects: Atlantic salmon; Salmo salar
• Online Access: http://hdl.handle.net/10852/68508; http://urn.nb.no/URN:NBN:no-71663

Every genome encodes a story of evolution, the remarkable complexity of life. Today, about five decades after Ohno’s momentous proposition on the genetic redundancy being an important driver for the evolution of genetic novelty, we are still continuing to solve the enigma that is a genome, the genetic code that ‘defines’ us and every other organism. The genomic revolution, fueled by the developments in sequencing technology, has provided an unparalleled opportunity to unravel the intricacies of this story to a fine resolution. These rapid advances coupled with increased feasibility of whole genome sequencing has especially bolstered the field of evolutionary genomics by providing an opportunity to study the molecular basis of evolution in species across the tree of life. Teleost fish are an outstanding model system to study a multitude of questions regarding the evolution of vertebrate genomes. The accruing genomic resource for these species is continuing to enable comparative genomic studies shedding light on vital aspects of genome evolution and the impact of whole genome duplication. This thesis explores into some aspects of genome and chromosome evolution in two important teleost family fish, namely, salmonids and sticklebacks Gene and genome duplication are the primary mode of generation of new genetic material for novelty to evolve. The relatively young whole genome duplication (WGD) in the salmonid lineage (referred to as Ss4R WGD) offers a great opportunity to gain insights into the evolution of gene duplicates consequent to polyploidy. To this end, we sequenced and assembled the draft genome of a representative of the earliest diverging non-anadromous salmonid lineage, Thymallus thymallus. We used this novel genomic resource in a comparative phylogenomic framework to gain insights into the consequences of lineage-specific rediploidization and genome-wide selective constraints on gene expression regulation. The genetic redundancy introduced post polyploidy is associated with rewiring of the regulatory network causing shifts in the gene expression patterns. Extensive divergence of ohnologs is often observed post WGD and is considered vital for retention of duplicates. Our analyses demonstrate that selection is important in the evolution of tissue expression following Ss4R WGD. To address large-scale genome structure evolution in grayling, we further generated a chromosome-level assembly for grayling by using long-read PacBio data and a linkage map. Using this resource, we could investigate the chromosomal rearrangements responsible for the extreme differences in karyotypes between Atlantic salmon (Salmo salar) and European grayling. While the Atlantic salmon karyotype has evolved through a series of Robertsonian translocations and fusions, we confirm that the more primitive looking karyotype of grayling has evolved primarily through inversions. Sticklebacks, particularly the three-spined stickleback (Gasterosteus aculeatus), have been a well-studied system in many realms of evolutionary biology. Yet another notable member of the same family and an emerging model system in ecology and evolutionary biology, is the nine-spined-stickleback (Pungitius pungitius). We generated a high-quality chromosome-scale genome assembly for the nine-spined stickleback using high coverage longread PacBio data and a high-density linkage map. Utilizing this high-quality genome assembly, we provide a comprehensive analysis of repetitive elements including centromeric repeats in the nine-spined stickleback genome. We also describe a recent duplication in the hemoglobin cluster and show that this region could potentially involve frequent copy number variations in closely related populations. Finally, we also identify structural variations potentially explaining the karyotypic variation between the three- and nine-spined sticklebacks. Taken together, this thesis, while providing the genome assembly and annotation valuable for further studies, also demonstrates the utility of comparative genomic analyses among closely related species to elucidate various facets of genome evolution.