Developmental genetics of adaptation

For decades after Darwin´s “The origin of species” was published, the prevailing paradigm was that natural selection is the only driving force in evolution that eventually leads, via gradual change, to adaptation and speciation. However, this rather selectionist view failed to explain different observations. Later, evolutionary biologists began to recognize that development could fill these gaps, providing a more comprehensive take on the evolutionary theory. First, important contributions thereof urged to consider the entire ontogeny of an organism when studying evolutionary histories, as during ontogeny the selective pressures change. Second, it was acknowledged that phenotypic change can precede genetic change, i.e. different phenotypes can develop from the same genetic code. Phenotypic plasticity has since been recognized as an important source for evolution and it has become clear that to truly understand how species adapt, we need to understand the entire developmental program of the traits in question. To study adaptations and their underlying developmental genetic mechanisms, cichlid fish offer great opportunities for several reasons: 1.) most adaptive traits have evolved multiple times independently providing natural replicates, 2.) the adaptive value of many traits has been established, and 3.) genomes of multiple species have been sequenced allowing for extensive comparative analyses. The first chapter of this thesis considers phenotypic plasticity in vertebrate teeth with a focus on how phenotypic plasticity could influence evolutionary outcomes. Teeth are still generally regarded as immutable structures that, once developed, do not change anymore. Being crucial for the survival of most vertebrates, teeth need to perform specialized tasks and thereby determine what food items can be consumed. Therefore, it is important that teeth can change in response to fluctuating food sources via phenotypic plasticity. Dental plasticity appears to be more widespread than previously assumed, being observed in different groups of vertebrates, such as fish or mammals. Adaptive phenotypic changes in teeth allow for the rapid and efficient utilization of multiple different food sources and can potentially even lead to fixed adaptations when genetic assimilation occurs. Two chapters of this thesis are dedicated to the question of what are the developmental genetic mechanisms that drive convergence in cichlids. To address this question, I focused on the convergence in mollusc-crushing lower pharyngeal jaw phenotypes. As an adaptation to hard food, such as molluscs, multiple cichlid species independently evolved large teeth and massive lower pharyngeal jaws. Chapter III focuses on identifying genes that are involved in tooth development in cichlids. Tooth development is relatively conserved across vertebrates. However, cichlids have a repertoire of de novo genes that are specific to their family. These genes formed inside a cluster of conserved tooth genes and got incorporated into the developmental genetic networks of odontogenesis, showing convergent associations with mollusc-crushing morphologies. In Chapter IV, I used genome-wide expression analysis to investigate how convergent developmental genetic mechanisms of mollusc-crushing lower pharyngeal jaws are across Neotropical cichlid species. Overall, there is only little convergence in gene expression patterns across all contrasts. However, the degree of convergence depends on the geographic setting of speciation, with character displacement in gene expression (i.e. greater expression differences between sympatric species) being observed in sympatric species. This could constitute a barrier to gene flow under the assumption that hybrid misexpression affects ecological viability. Such character displacement in gene expression could generally contribute to intrinsic barriers to gene flow, even in traits not directly associated with important ecological tasks. With this thesis, I want to contribute to our understanding of developmental genetic mechanisms of a convergent adaptation and highlight the potential role of gene expression in speciation. To conclude, I provide some future directions of research that build on the findings reported here.