The role of ecology and phenotypic plasticity in lake-stream divergence in an East African haplochromine cichlid fish

Understanding the “origin of species” has been one of the major topics in biology ever since Charles Darwin’s famous publication (Darwin 1859). One and a half centuries later speciation still remains the “mystery of mysteries” (Pennisi 2005). While we have learned a lot from traditional laboratory model organisms, we now realize that many questions in speciation research can only be answered by studying how organisms adapt, behave and diversify in their natural environment (Nosil et al. 2017). Some of the main questions in speciation research at the moment are: “Which barriers contribute to reproductive isolation?”, “What are the genomic patterns of reproductive isolation?”, “What is the role of plasticity? ”, and “What is the role of changes in gene expression” (Butlin et al. 2012). With this thesis I aim to provide part of the answers to these questions by studying one of the best model systems for speciation research: the East African cichlid fishes (Kocher 2004).
Astatotilapia burtoni is a haplochromine cichlid that inhabits both Lake Tanganyika and affluent rivers. Lake and river populations of A. burtoni represent an emerging model system for studying early phases of adaptive divergence. In my thesis, I investigate the degree of reproductive isolation between different populations and the mechanisms that drive the lake-stream divergence. More specifically, I characterize the reproductive barriers contributing to reproductive isolation and investigate the roles of local adaptation, adaptive phenotypic plasticity, parasites, immune system response, and gene expression in lake-stream divergence.
The main body of work includes four chapters on East-African haplochromine cichlid fishes as a model for studying early phases of adaptive divergence.
In Chapter 1, I investigate the relative contributions of adaptive phenotypic plasticity versus local adaptation to fitness of A. burtoni populations from Lake Tanganyika and nearby rivers. Adaptive phenotypic plasticity has previously been proposed to play a key role in the impressive radiations of cichlids. However, mostly due to logistic difficulties, field-experiments are scarce in this system. By performing two transplant experiments in Lake Tanganyika, using both wild caught and common garden raised F1 individuals, I provide one of the first field-based experiments to assess direct fitness consequences of morphological and genetic divergence between lake and stream cichlids in nature.
In Chapter 2, I further investigate the correlation between genetic divergence between populations and the level of reproductive isolation between populations by performing a mesocosm mating experiment in a semi-natural setting at Lake Tanganyika. I assessed reproductive isolation in the presence of male-male competition by analysing survival and growth rates of introduced adults and their reproductive success from genetic parentage of surviving offspring. I provide one of the first field-based experiments to assess multiple environment dependent (extrinsic) components of reproductive isolation in cichlids.
In Chapter 3, I investigate the role of ecotype-specific parasites, the immune response of hosts, and gene expression in the lake-stream divergence. By performing parasitological screening, immune response measurements, and RNA-sequencing of immune-related organs of fish from natural habitats as well as a lake-like pond setup I reveal the mechanisms underlying phenotypic plasticity in this system.
In Chapter 4, three other haplochromine cichlid species that co-exist with A. burtoni in Lake Tanganyika and surrounding drainage systems were used to uncover commonalities and differences in adaptation to the river/lake habitat. We sequenced whole genomes of multiple lake- stream population pairs of A. burtoni and Ctenochromis horei, Haplochromis stappersi, and Pseudocrenilabrus philander. These natural replicates offered a unique possibility to test whether the same patterns and processes are involved in the adaptation to the lake-stream transition in four haplochromine species. I performed landmark-based geometric morphometric analysis on digital images of fishes of the four species to capture disparity in body shape and compare it with genomic disparity.