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The evolution of plasticity in the transcriptome of the Trinidadian guppy


Phenotypic plasticity is a ubiquitous feature of all living systems, and there is much interest in how plasticity influences long term evolutionary trajectories. One of the major complications with modeling evolutionary trajectories is that plasticity itself is known to evolve. The evolution of plasticity has mainly been focused on at the level of the whole organism, and it is unclear if plasticity at all levels of biological organization evolve. Models that assume no generational change in plasticity may be overly simplistic; a more nuanced approach could incorporate the evolution of plasticity into the modeling. A first step towards this end is to determine what levels of biological organization plasticity evolves, and then to determine if there are predictable patterns of evolved plasticity. RNA is an intermediate to DNA and protein, that can undergo changes in response to environmental conditions, thereby modifying the genetic information passed on to non-coding RNAs, functional RNAs, and proteins. Responses to environment include both changes in abundance of RNAs, as well as changes to the composition of the molecules. This dissertation focuses on the evolution of plasticity within the transcriptome of Poecilia reticulata (Trinidadian guppy). One of the major known regulators of transcript abundance are small RNAs (sRNAs). Micro RNAs (miRNAs), are a specific type of sRNA that bind transcripts, typically leading to translational silencing. We investigated two forms of plasticity, an abundance measure of plasticity (miRNA differential expression), and a compositional measure of plasticity (A-to-I RNA editing). A-to-I RNA editing is the chemical nucleotide change from adenosine to inosine, catalyzed by the enzyme ADAR. We first produced a set of miRNAs in guppies, and confirmed the presence of key biogenesis pathway components, i.e. argonaute proteins in the genome. Tissue-specific miRNA expression patterns were identified for three tissues in Poecilia reticulata (Trinidadian guppy), brain, ovary and testis. We found most discovered miRNAs were located in intergenic regions of the genome. Some miRNAs matched known miRBase sequences, while others were considered novel guppy miRNAs. We observed miRNAs expressed from tandem clusters and analyzed piRNA distribution in ovary samples. This study provides important insights into guppy small RNA expression, laying the groundwork for future investigations into their regulatory roles. The 3rd chapter of this dissertation revealed many miRNAs with differential expression (DE), including population main effects, rearing condition, and their interactions. Population DE miRNAs showed a wide range of expression levels. Rearing condition main effects were (slightly) less common. We identified miRNAs with evolved expression plasticity, distributed across four categories: reversed, evolved plastic, assimilated, and accommodated. Both populations showed similar numbers of miRNAs exhibiting plasticity. In the final chapter of this dissertation we characterized the "editome" of guppies. The majority of the edits were consistent with A-to-I editing, with a smaller proportion of C-to-U edits. The intragenic edits were distributed among a number of genes. However, there were no significant differences in editing between populations, rearing conditions, or their interaction. This dissertation revealed significant miRNA expression differences and provided insights into A-to-I editing patterns in guppies.


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gene expression
phenotypic plasticity


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