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Extreme environments serve as natural laboratories for studying evolutionary processes, with caves offering replicated instances of independent colonizations. The timing, mode and genetic underpinnings underlying cave-obligate organismal evolution remain enigmatic. We integrate phylogenomics, fossils, palaeoclimatic modelling and newly sequenced genomes to elucidate the evolutionary history and adaptive processes of cave colonization in the study group, the North American Amblyopsidae fishes. Amblyopsid fishes present a unique system for investigating cave evolution, encompassing surface, facultative cave-dwelling and cave-obligate (troglomorphic) species. Using 1105 exon markers and total-evidence dating, we reconstructed a robust phylogeny that supports the nested position of eyed, facultative cave-dwelling species within blind cavefishes. We identified three independent cave colonizations, dated to the Early Miocene (18.5 Ma), Late Miocene (10.0 Ma) and Pliocene (3.0 Ma). Evolutionary model testing supported a climate-relict hypothesis, suggesting that global cooling trends since the Early–Middle Eocene may have influenced cave colonization. Comparative genomic analyses of 487 candidate genes revealed both relaxed and intensified selection on troglomorphy-related loci. We found more loci under relaxed selection, supporting neutral mutation as a significant mechanism in cave-obligate evolution. Our findings provide empirical support for climate-driven cave colonization and offer insights into the complex interplay of selective pressures in extreme environments. 

Cave-obligate aquatic organisms are difficult to monitor for conservation due to cryptic diversity, unknown subterranean hydrological connectivity, and accessibility to habitats. Conservation management practices have benefitted from evolutionary data; however, the evolutionary and biogeographic histories of most cave-obligate organisms are unknown. The modes and patterns leading to most cave-obligate organism distributions are also uncertain. The Southern Cavefish (Typhlichthys subterraneus, Amblyopsidae) is the largest ranging cavefish in the world but represents a species complex of which the distribution and relatedness within remains unclear. To explore modes of cave-adaptive evolution, we performed population genomic analyses on a dataset of single nucleotide polymorphisms harvested from ultraconserved elements. We found five to eight strongly delineated genetic clusters. Little to no genetic exchange occurred between clusters, indicating high genetic distinctiveness and low connectivity, a concerning result for the fitness and conservation of these fishes. Genetic clusters did not correspond to caves nor to other geographic boundaries examined. Unfortunately, one of the geographic units most easily communicated for conservation– caves– do not match the biological units of interest. Our results support multiple independent colonization events from a widespread surface ancestor with a small degree of cave connectivity among, but not between, clusters. We suggest whole cave system conservation.