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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.
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Population Genomics of Premature Termination Codons in Cavefish With Substantial Trait Loss
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.
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- PAR ID:
- 10570407
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Molecular Biology and Evolution
- Volume:
- 42
- Issue:
- 2
- ISSN:
- 0737-4038
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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