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


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, Max Planck Institute for Evolutionary Biology, Plön.

Cite as: https://hdl.handle.net/21.11116/0000-0002-9C20-A
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
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.