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Evolutionary analysis of gene expression in hybrid sculpins


Czypionka,  Till
Research Group Evolutionary Genetics of Fishes, Department Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, Max Planck Society;

Tautz,  Diethard
Department Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Czypionka, T. (2013). Evolutionary analysis of gene expression in hybrid sculpins. PhD Thesis, Christian-Albrechts-Universität, Kiel.

European freshwater sculpins of the genus Cottus receive attention as a model for studying the initial steps of a homoploid hybrid speciation. An invasive lineage of Cottus, which originated from the hybridization between Cottus rhenanus and Cottus perifretum, was able to invade a new habitat and occupy a new ecological niche not available to its parent species. In this thesis several aspects of this process are studied at the transcriptome level. To this means, a Cottus specific oligonucleotide microarray was designed based on transcriptome sequencing. The binding behavior of the probes on the microarray was experimentally determined, revealing large variation in binding behavior between probes. A newly developed normalization approach was applied, to remove artifacts resulting from this variation. As a first step, the phenotypic differentiation between invasive Cottus and its parent species was assessed. Expression level differentiation indicates that the invasive Cottus phenotype is overall intermediate between its parent species in agreement with its hybrid origin. However, invasive Cottus are characterized through a set genes with unique expression distinguishing it from its parent species. These are mainly genes with transgressive expression patterns, i.e. expression patterns outside the expression range observed in the parent species. Genes which are transgressively overexpressed in invasive Cottus are functionally correlated as evidenced through Gene Ontology term enrichment. These genes represent candidates for the adaptive phenotypic change which enabled the colonization of the new habitat by invasive Cottus. Some of the transgressive expression patterns were already observed in F2 crosses between the parent species, which were analyzed as a proxy of the initial stages of hybrid speciation. This observation suggests that initial hybridization played a role in the formation of the unique invasive phenotype. Importantly, a large fraction of transgressive patterns of over expression were not observed in the in F2 crosses and thus must have been acquired when invasive Cottus evolved after the initial hybridization. Overall these results are in line with an evolutionary process where natural selection acts on hybridization-induced increased phenotypic diversity to shape the new invasive phenotype, thus leading to ecological and spatial segregation from the parent species. As a second aspect, the role of phenotypic plasticity in promoting adaptation and diversification was assessed. Evolutionary mechanisms involving phenotypic plasticity do apply particularly in situations involving the adaptation to a new environment. This is the case for invasive Cottus, which colonized a new habitat with a different thermal regime. Temperature is a key factor structuring ecological communities along the fluvial ecosystems inhabited by Cottus. Thus, thermal plasticity was assessed by measuring temperature specific gene expression profiles over a temperature range from 14°C to 25°C. This temperature range reflects conditions in the originally occupied and the newly invaded habitat during summer when temperature differences between the two habitats are most pronounced. Expression profile differentiation between the invasive Cottus and the parent species was most pronounced at the lower half of the analyzed temperature range (i.e. < 21°C). This is surprising, given that these temperatures are not an exclusive property of the newly invaded habitat but are commonly observed both in original and newly invaded habitats. Comparative analysis of gene expression changes over temperatures revealed plastic responses shared by all the species of Cottus in analysis as well as changes in plasticity between parent species and invasive Cottus. In particular the augmentation of pre-existing plastic responses was shown to contribute to the phenotypic differentiation of invasive Cottus, which is in line with the prediction that plastic traits contribute to early steps of adaptive evolution. For the temperatures < 21°C, the augmentation of a plastic response was found in a mitochondrion related phenotype of potential adaptive value. In summary, this thesis provides evidence in support of proposed modes of hybrid speciation as well as for proposed modes of adaptive evolution through the modification of plastic phenotypes. Furthermore, this thesis constitutes the first systematic phenotypic analysis of the Cottus study system and therefore is an important step towards the identification of the adaptive changes underlying the diversification process.