Subterranean Fishes of the World

6363

2023

A thesis submitted in fulfillment of the requirements for the degree of Doctor of Philosophy in the Departament of Gene regulation and morphogenesis Centro Andaluz de Biología del Desarrollo

Transcriptional regulation is a key mechanism in the complex process of gene regulation. This process makes it possible to control how much gene product each cell expresses, changes, or maintains as needed, thereby affecting cell identity. This tight regulation occurs because of the interplay between transcription factors and cis regulatory elements. Observing how evolution has shaped the elements of gene regulation offers a fascinating view of the mechanisms that have driven adaptation and evolutionary novelty. In this thesis, we used epigenomic and transcriptomic techniques to explore the role of cis regulatory elements in different evolutionary scenarios. In the first scenario, we addressed how gene regulation contributes to the generation of evolutionary novelty in vertebrates. To do so, we used Branchiostoma lanceolatum (amphioxus), which is more similar to the chordate ancestor and compared it to our vertebrate animal model, zebrafish. Vertebrate genomes have undergone two rounds of whole genome duplications, increasing the number of gene copies and contributing to more complex gene regulation. We treated embryos of both species to alter conserved signalling pathways. This alteration revealed that, in vertebrates, developmental genes tend to have more cis regulatory elements, and that these elements integrate more regulatory information, and that this gain of regulatory information increases the interconnectivity of key developmental signalling pathways. This gain of interconnectivity is likely essential for the emergence of vertebrate morphological novelty. In the second scenario, we explored the role of cis regulatory elements during adaptation to a new environment using Astyanax mexicanus as a model organism. This teleost fish has two well-differentiated populations. The surface population lives in the rivers and lakes of Mexico. The cavefish population has conquered cave systems and has undergone several phenotypic adaptations to survive in that environment. They lack eyes and pigmentation and have undergone several metabolic changes, accumulating more fat than the surfacefish. These adaptations occurred in a short evolutionary period and independently in different Astyanax communities. We used epigenomics and transcriptomics to understand how cis regulatory elements have contributed to this rapid adaptation. Using this approach, we discovered that the regulation of key developmental genes is altered in cavefish compared to that in surfacefish, contributing to this adaptation. Furthermore, we found changes in cis regulatory elements that are key to explaining this quick adaptation because they alter specific gene regulatory networks, such as eye developmental networks. Together, our studies demonstrate the importance of gene regulation and how changes in the cis regulatory elements contribute to the generation of evolutionary novelties and adaptation during development. Our understanding of the mechanisms behind these processes provides insight into how biological diversity arises and how organisms use these mechanisms to adapt to their environments.

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