On the genetic basis of phenotypic diversity in teleost fish

Abstract

The origin of phenotypic diversity in closely related species remains one of the great mysteries of biology. Exploring the genetic mechanisms underlying this phenotypic diversity is one of the main endeavors of evolutionary biology. The recent advances in sequencing technologies allow the investigation of the genetic basis of phenotypic diversity in a wide range of organisms. The infraclass of teleosts is a lineage that gave rise to a multitude of adaptive radiations, of which many represent great model systems to study the genetic basis of morphology and behavior. In this thesis, I combined a number of different sequencing approaches to investigate the genetic basis of different morphological features and behaviors using two different teleost species radiations: the haplochromine cichlids of East African Great Malawi and the South-East Asian fighting fishes. In chapter 1, we investigated the genetic basis of the two most common melanic patterns found in African cichlids: horizontal stripes and vertical bars. Using a hybrid cross between the striped species Pseudotropheus cyaneorhabdos and the barred species Chindongo demasoni, we conducted quantitative trait locus (QTL) mapping, to identify genomic locations underlying the formation of the two color patterns. The distribution of phenotypes in our hybrid cross showed, that bars and stripes are inherited as independent modules. The results of the QLT analysis revealed, that in Lake Malawi cichlids one large effect QTL encompassing the gene agrp2 affects the formation of horizontal stripes next to a number of smaller effect QTL. While most parts of the horizontal stripe pattern share a common genetic basis, a few of the identified QTL are only responsible for the formation of specific parts of the stripe pattern. The analysis of vertical bars revealed a high number of small effect QTL underlying the formation of the color pattern. We discuss the role of hybridization in the diversification of melanic color patterns in Lake Malawi cichlids regarding the modularity of stripes and bars and the independent inheritance of some parts of the horizontal stripe patterns. Our work in chapter 2 focuses on the genetic basis of aggressive behavior in two fighting fish species of the genus Betta. Using brain transcriptomes of the highly aggressive species B. splendens and the less aggressive species B. simplex, we investigated the species-specific transcriptional responses to an aggressive interaction, to detect expressional differences that might underlie the behavioral differences of the two studied species. Differential gene expression analysis revealed a much stronger transcriptional response in the aggressive species B. splendens when compared to B. simplex. The transcriptional response was strongest in the diencephalon and telencephalon of B. splendens. A closer look at the functions of the genes showed, that B. splendens showed differential expression of genes involved in hormonal regulation and regulation of the carbohydrate metabolism, indicating changes in the short-term regulation of aggressive behavior in this species. Both species showed differential expression of genes that may have functions in the long-term regulation of aggressive behavior by the formation of new neurons and neuronal connections. Weighted correlation network analysis revealed that genes involved in long-term regulation of social behavior were integrated into new co-expression networks in the telencephalon of both species. Our results indicate a more fine-tuned short-term regulation of aggressive behavior in the aggressive species B. splendens, highlighting the importance of regulation of behavior in an aggressive environment. In Chapter 3, we investigated the visual system of the Siamese fighting fish B. splendens with a focus on the cone opsin gene lws of which five copies were found in the genome of B. splendens. Using whole genome sequences of nine different anabantoid species we explored the evolutionary history of cone opsins in the Anabantiformes. Our analysis shows, that only species of the genus Betta have five copies of lws and that at least two duplication events in the Betta lineage lead to the expansion of this cone opsin class. The analysis of the amino acid sequences of the different lws paralogs revealed functional differentiation between the different paralogs within Betta. Using eye transcriptomes of B. splendens, we demonstrated expression shifts between paralogs of all cone opsin classes throughout ontogeny. Expression of lws showed patterns of temporal collinearity, which might have facilitated the expansion and functional diversification of lws genes in Betta. The three chapters emphasize the importance of using a variation of approaches to investigate the genetic basis of different phenotypes in different teleost model systems in order to get a comprehensive understanding of the fast evolution of phenotypic diversity.