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Abstract Loss-of-function alleles are a pertinent source of genetic variation with the potential to contribute to adaptation. Cave-adapted organisms exhibit striking loss of ancestral traits such as eyes and pigment, suggesting that loss-of-function alleles may play an outsized role in these systems. Here, we leverage 141 whole genome sequences to evaluate the evolutionary history and adaptive potential of single nucleotide premature termination codons (PTCs) in Mexican tetra. We find that cave populations contain significantly more PTCs at high frequency than surface populations. We also find that PTCs occur more frequently in genes with inherent relaxed evolutionary constraint relative to the rest of the genome. Using SLiM to simulate PTC evolution in a cavefish population, we show that the smaller population size and increased genetic drift is sufficient to account for the observed increase in PTC frequency in cave populations without positive selection. Using CRISPR-Cas9, we show that mutation of one of these genes, pde6c, produces phenotypes in surface Mexican tetra that mimic cave-derived traits. Finally, we identify a small subset of candidate genes that contain high-frequency PTCs in cave populations, occur within selective sweeps, and may contribute to beneficial traits such as reduced energy expenditure, suggesting that a handful of PTCs may be adaptive. Overall, our work provides a rare characterization of PTCs across wild populations and finds that they may have an important role in loss-of-function phenotypes, contributing to a growing body of literature showing genome evolution through relaxed constraint in subterranean organisms. 

Abstract A major goal of modern biology is connecting phenotype with its underlying genetic basis. The Mexican cavefish (Astyanax mexicanus), a characin fish species comprised of a surface ecotype and a cave-derived ecotype, is well suited as a model to study the genetic mechanisms underlying adaptation to extreme environments. Here, we map 206 previously published quantitative trait loci (QTL) for cave-derived traits in A. mexicanus to the newest version of the surface fish genome assembly, AstMex3. These analyses revealed that QTL clusters in the genome more than expected by chance, and this clustering is not explained by the distribution of genes in the genome. To investigate whether certain characteristics of the genome facilitate phenotypic evolution, we tested whether genomic characteristics associated with increased opportunities for mutation, such as highly mutagenic CpG sites, are reliable predictors of the sites of trait evolution but did not find any significant trends. Finally, we combined the QTL map with previously collected expression and selection data to identify 36 candidate genes that may underlie the repeated evolution of cave phenotypes, including rgrb, which is predicted to be involved in phototransduction. We found this gene has disrupted exons in all non-hybrid cave populations but intact reading frames in surface fish. Overall, our results suggest specific regions of the genome may play significant roles in driving adaptation to the cave environment in A. mexicanus and demonstrate how this compiled dataset can facilitate our understanding of the genetic basis of repeated evolution in the Mexican cavefish. 

Abstract Animal genitalia evolve rapidly because of coevolution between male and female traits. However, how the ecological context in which mating occurs might modulate the evolution of genital traits remains poorly understood. We investigated how a change in the sensory environment (the absence of light upon cave colonization) impacted the expression of genital traits in a live-bearing fish, Poecilia mexicana (Poeciliidae), with populations in adjacent cave and surface habitats. Quantifying characteristics of the female urogenital aperture and the male gonopodium (a modified anal fin used for copulation), we found significant differences in genital traits of both sexes. Females from cave populations exhibited larger and more rounded genitalia. Males from cave populations exhibited a significantly enlarged palp, a fleshy gonopodial appendage that has been hypothesized to have sensory functions. Our results suggest that genital traits can diverge rapidly among closely related populations exposed to different environmental conditions. The absence of light could impact genital evolution directly, if some genital structures have sensory functions that compensate for the lack of visual information during copulation, or indirectly, if the absence of light impacts dynamics of sexual conflict or cryptic female choice that arise through the interaction between the sexes.