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Sleep is an evolutionarily ancient behavior, yet multiple cave-dwelling populations of the Mexican tetra, Astyanax mexicanus, have converged on sleep loss compared to surface fish. However, most of the 34 cave populations remain unstudied, and sleep in natural habitats is largely unknown. To address this, we measured sleep and activity in 15 representative populations of surface, cave, and hybrid populations. All cavefish and hybrid populations tested exhibited drastically reduced sleep, including hybrid populations with diverse eye and pigmentation phenotypes. Mapping behavior onto the A. mexicanus phylogeny revealed that reduced sleep and elevated locomotor activity evolved independently multiple times. Field experiments confirmed that wild fish also exhibit sleep loss, paralleling laboratory findings. These results demonstrate deep evolutionary convergence on sleep loss across cavefish lineages and suggest that sleep reduction is a primary trait contributing to adaptation in subterranean environments. 

ABSTRACT The regulation of bone size is a poorly understood and complex developmental process. Evolutionary models can enable insight through interrogation of the developmental and molecular underpinnings of natural variation in bone size and shape. Here, we examine the Mexican tetra (Astyanax mexicanus), a species of teleost fish comprising of an extant river‐dwelling surface fish and obligate cave‐dwelling fish. These divergent morphs have evolved for thousands of years in drastically different habitats, which have led to diverse phenotypic differences. Among many craniofacial aberrations, cavefish harbor a wider gape, an underbite, and larger jaws compared to surface‐dwelling morphs. Morphotypes are inter‐fertile, allowing quantitative genetic analyses in F₂pedigrees derived from surface × cavefish crosses. Here, we used quantitative trait locus (QTL) analysis to determine the genetic basis of jaw size. Strikingly, we discovered a single genomic region associated with several jaw size metrics. Future work identifying genetic lesions that explain differences in jaw development will provide new insight to the mechanisms driving bone size differences across vertebrate taxa. 

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 cluster 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 Astyanax mexicanus and demonstrate how this compiled dataset can facilitate our understanding of the genetic basis of repeated evolution in the Mexican cavefish. 

The trajectory of evolution is impacted by molecular constraints and biases that are difficult to validate experimentally. Repeated evolution of similar traits across the Tree of Life serves as a natural experiment to discern common factors that drive the evolution of these traits. The architecture of genomes in one-dimensional, two-dimensional, and three-dimensional space is emerging as a potential factor that may predict repeated phenotypic evolution. For example, chromatin packaging and the 3D organization of the genome within the nucleus can impose evolutionary constraints by predisposing genomic regions for particular types of mutations, while the evolution of genome sequence can also drive reorganization of chromatin. With the explosion of new library preparation and sequencing technologies that are accessible for non-model species, we envision a great opportunity to understand how genome architecture across phylogenetically disparate species may impact repeated phenotypic evolution. We provide examples of the known and potential avenues of phenotypic convergence at each level of genome architecture and how integration of these data can provide unique insights into the constraints, trajectory, and predictability of evolution. 

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 Laboratory studies have demonstrated that a single phenotype can be produced by many different genotypes; however, in natural systems, it is frequently found that phenotypic convergence is due to parallel genetic changes. This suggests a substantial role for constraint and determinism in evolution and indicates that certain mutations are more likely to contribute to phenotypic evolution. Here we use whole genome resequencing in the Mexican tetra,Astyanax mexicanus, to investigate how selection has shaped the repeated evolution of both trait loss and enhancement across independent cavefish lineages. We show that selection on standing genetic variation and de novo mutations both contribute substantially to repeated adaptation. Our findings provide empirical support for the hypothesis that genes with larger mutational targets are more likely to be the substrate of repeated evolution and indicate that features of the cave environment may impact the rate at which mutations occur. 

Population divergence is often quantified using phenotypic variation. However, because sensory abilities are more difficult to discern, we have little information on the plasticity and rate of sensory change between different environments. The Mexican tetra (Astyanax mexicanus) is a fish distributed throughout Southern Texas and Northern Mexico and has evolved troglomorphic phenotypes, such as vestigial eyes and reduced pigmentation, when surface ancestors invaded caves in the past several hundred thousand years. In the early 1900s, surfaceA. mexicanuswere introduced to the karstic Edwards-Trinity Aquifer in Texas. Subsequent cave colonization of subterranean environments resulted in fish with phenotypic and behavioral divergence from their surface counterparts, allowing examination of how new environments lead to sensory changes. We hypothesized that recently introduced cave populations would be more sensitive to light and sound when compared to their surface counterparts. We quantified divergence using auditory evoked potentials (AEPs) and particle acceleration levels (PALs) to measure differences in sound sensitivity, and electroretinography (ERGs) to measure light sensitivity. We also compared these results to measurements taken from native populations and lab-born individuals of the introduced populations. Honey Creek Cave fish were significantly more sensitive than proximate Honey Creek surface fish to sound pressure levels between 0.6 and 0.8 kHz and particle acceleration levels between 0.4 and 0.8 kHz. Pairwise differences were found between San Antonio Zoo surface and the facultative subterranean San Pedro Springs and Blue Hole populations, which exhibited more sensitivity to particle acceleration levels between 0.5 and 0.7 kHz. Electroretinography results indicate no significant differences between populations, although Honey Creek Cave fish may be trending toward reduced visual sensitivity. Auditory thresholds between wild-caught and lab-raised populations of recently invaded fish show significant differences in sensitivity, suggesting that these traits are plastic. Collectively, while these results may point to the rapid divergence ofA. mexicanusin cave habitats, it also highlights the responsive plasticity ofA. mexicanusauditory system to disparate environments. 

Abstract The growing use of genomics in diverse organisms provides the basis for identifying genomic and transcriptional differences across species and experimental conditions. Databases containing genomic and functional data have played critical roles in the development of numerous genetic models but most emerging models lack such databases. The Mexican tetra, Astyanax mexicanus exists as 2 morphs: surface-dwelling and cave-dwelling. There exist at least 30 cave populations, providing a system to study convergent evolution. We have generated a web-based analysis suite that integrates datasets from different studies to identify how gene transcription and genetic markers of selection differ between populations and across experimental contexts. Results of diverse studies can be analyzed in conjunction with other genetic data (e.g. Gene Ontology information), to enable biological inference from cross-study patterns and identify future avenues of research. Furthermore, the framework that we have built for A. mexicanus can be adapted for other emerging model systems. 

Variation in complex traits is the result of contributions from many loci of small effect. Based on this principle, genomic prediction methods are used to make predictions of breeding value for an individual using genome-wide molecular markers. In breeding, genomic prediction models have been used in plant and animal breeding for almost two decades to increase rates of genetic improvement and reduce the length of artificial selection experiments. However, evolutionary genomics studies have been slow to incorporate this technique to select individuals for breeding in a conservation context or to learn more about the genetic architecture of traits, the genetic value of missing individuals or microevolution of breeding values. Here, we outline the utility of genomic prediction and provide an overview of the methodology. We highlight opportunities to apply genomic prediction in evolutionary genetics of wild populations and the best practices when using these methods on field-collected phenotypes.