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Adaptive phenotypic change over the lifetime of an invader - Transcriptomics of a Cottus lineage of hybrid origin

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Iwaszkiewicz-Eggebrecht,  Elzbieta Anna
IMPRS for Evolutionary Biology, Max Planck Institute for Evolutionary Biology, Max Planck Society;
Research Group Evolutionary Genetics of Fishes, Department Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Iwaszkiewicz-Eggebrecht, E. A. (2018). Adaptive phenotypic change over the lifetime of an invader - Transcriptomics of a Cottus lineage of hybrid origin. PhD Thesis, Christian-Albrechts-Universität, Kiel.


Cite as: https://hdl.handle.net/21.11116/0000-0002-9C20-A
Abstract
A central idea about hybrid speciation is that recombination of parental traits can allow hybrids to colonize new ecological niches. However, the connections between ecological context and the genetic traits underlying adaptive evolutionary changes in hybrids remain elusive in most systems. I study a young hybrid lineage of Cottus fish that has invaded an environment where its parent species do not occur. While the parental species are limited to summer-cold headwaters, the hybrid Cottus colonize downstream areas of rivers that are more exposed to sunlight and significantly warmer in the summer. This suggests that invasive Cottus have adapted to a new ecological niche coarsely related to water temperature. I tested temperature preference of the three Cottus lineages in the laboratory conditions during summer and found that invasives, despite living in warmer waters, prefer same water temperature as their parental species when given a choice. Then I proceeded to transcriptome scans in natural habitats in order to understand the nature of adaptation to local environments. I used RNAseq to compare, in an unprecedented detail, transcriptome profiles of wild populations over the course of a complete year. I found that different clusters of genes contribute to the differentiation of hybrids from parental species in different seasons. Gene expression profiles that follow changes in temperature in nature were enriched for metabolism-related GO terms and suggest thermal adaptation in the hybrid lineage. However, the data suggest that much of the differentiation between hybrid Cottus and their parents is not related to temperature. The analysis is complemented by sampling of transcriptomes from fish raised under controlled laboratory conditions, which reveals heritable components of gene expression divergence. Some of these heritable differences distinguish hybrid Cottus from both parents and are likely to be involved in evolutionary novelty after hybridization. Prevailing theory about homoploid hybrid speciation posits that hybridization can give rise to new potentials for adaptation through 8 transgressive segregation. As a result, the phenotype of a hybrid lineage exceeds that of both parental species, which would equip hybrids with the ability to colonize new ecological niches and thus reinforce speciation. I found ecologically relevant transgressive traits in Cottus by comparing expression patterns identified as transgressive in the laboratory with the time-series data from natural habitats. Many of the transgressive genes were connected to metabolic functions suggesting that these genes have altered the metabolism of the invasive lineage relative to the parental species. Another interesting candidate trait shows a transgressive pattern likely due to an increase in copy number and may be involved in the extended red-light vision. This possibly constitutes an adaptation to life in the murky waters of downstream habitats of the invasive Cottus. Overall, I explored Cottus responses to the environment in great depth and traced their genetic basis. The analysis inferred expression phenotypes that constitute worthy avenues for further investigation.