Subterranean Fishes of the World

7001

2025

Dissertation presented to the Faculty of the Graduate School of The University of Texas at Austin in partial fulfillment of the requirements for the Degree of Doctor of Philosophy The University of Texas at Austin May 2025

Lineages that invade subterranean environments often evolve convergent adaptations to life in darkness, including sensory tradeoffs and morphological reduction. In central Texas, the Eurycea salamander radiation provides a unique system to investigate repeated evolution, with multiple independent transitions into karstic groundwater habitats. These invasions have led to parallel phenotypic changes, including eye reduction, limb elongation, and expansion of non-visual sensory systems. We integrated developmental, morphological, and transcriptomic analyses across six Eurycea lineages—both surface and subterranean—to examine the molecular basis of eye regression and sensory shifts. Using 3′ tag-based RNA sequencing and a de novo transcriptome assembly, we analyzed gene expression in eye tissue across developmental stages (1–5 months post-oviposition and adult). Expression patterns clustered strongly by ecotype and correlated with eye volume, reflecting the convergence of gene expression trajectories during eye reduction. Subterranean species exhibited heterochronic compression of gene expression, with early onset and truncation of key eye developmental genes, including cryga, RP1, and prox1. These shifts were consistent across both interspecific and intraspecific comparisons and aligned with reduced eye volume. Notably, surface species maintained prolonged expression of lens- and photoreceptor-related genes, while subterranean lineages showed abbreviated expression profiles, reflecting relaxed selection on vision. We also observed compensation between optic and the mechanosensory systems. Subterranean lineages showed increased numbers of anterior neuromast organs, along with sustained expression of PAX6 in lateral line tissues. In contrast, surface species showed reduced PAX6 labeling in adult neuromasts, suggesting a reallocation of developmental resources between vision and mechanosensation. Together, our results demonstrate that parallel eye regression in subterranean Eurycea is underpinned by predictable changes in gene expression and developmental timing. These findings highlight how ecological transitions can reshape developmental trajectories and drive parallel evolution at molecular and morphological levels. More broadly, this work offers a comparative framework for investigating the moelcular basis of adaptation and may inform our understanding of progressive eye disorders in humans

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