Subterranean Fishes of the World

7095

2025

108 pages

A dissertation submitted to the faculty of the University of Minnesota In partial fulfillment of the requirements for the degree of Doctor of Philosophy. Copyright Emma Yvette Roback 2025

Adaptation is often framed as a process that results in the proliferation of novel traits or enhancement of existing functions in a population. However, the Mexican tetra (Astyanax mexicanus) offers a contrasting case study: cavefish populations with repeated loss of traits whose functions are dispensable—or even detrimental—in perpetual darkness. Independent lineages of Mexican cavefish exhibit a striking loss of traits present in their surface fish counterparts such as eyes, pigment, sleep, and aggression. Yet, since the time of Darwin, evolutionary biologists have argued about whether this trait loss was an adaptive process driven by natural selection. In On the Origin of the Species (1859) Darwin remarks: “As it is difficult to imagine that eyes, though useless, could in any way be injurious to animals living in darkness, I attribute their loss solely to disuse.” Likewise, trait loss in cavefish was often attributed to mutation accumulation and genetic drift, with little role of selection. Here, I explore an alternate hypothesis. Perhaps trait loss is produced through genetic variation that eliminates or reduces the function of genes underlying ancestral traits, and further, the extremes of cave life may create a selective environment where that loss is beneficial. This is the hypothesis of addition by subtraction. This work explores the population genomics of adaptation through loss by identifying loss-offunction variants across independently evolved populations of cavefish and investigating the demographic histories of unique cave systems with novel environmental pressures. In Chapter 1, investigation of premature termination codons (PTCs) illustrated how genetic drift has indeed been a prominent force in the evolutionary history of cavefish. The environmental shift from surface to cave has likely resulted in relaxed constraint that has allowed loss-of-function variants to persist and rise in frequency. In addition, genes with PTCs are consistently disrupted in other subterrean-dwelling taxa, suggesting that degradation of certain genes has occurred in a repeated manner across dark-adapted organisms. In Chapter 2 we generated a pangenome graph for the Mexican tetra, one of the first pangenomes for a wild vertebrate. Our pangenome enabled comprehensive discovery of structural variation that revealed repeated deletion events likely contributing to the recurrent evolution of cave-derived phenotypes in independent cavefish lineages. We found instances of the same gene harboring unique high-frequency deletions between lineages. These genes have strong evidence of selection, suggesting that that the presence of different deletions in the same gene in each lineage is not due to chance or relaxed constraint simply allowing these variants to persist, but repeated selection favoring independent mutations in specific genes in caves. Finally, in Chapter 3, we untangle the demographic history of a curious cave where the trait of eyesight seems to have re-appeared after light entered the cave. In sum, this work highlights loss-of-function variants as underexplored contributors to adaptive evolution and identifies patterns of genetic convergence underlying how organisms cope with similar environmental challenges

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