Eyes are quintessential complex traits and our understanding of their evolution guides models of trait evolution in general. A long-standing account of eye evolution argues natural selection favors morphological variations that allow increased functionality for sensing light. While certainly true in part, this focus on visual performance does not entirely explain why diffuse photosensitivity persists even after eyes evolve, or why eyes evolved many times, each time using similar building blocks. Here, we briefly review a vast literature indicating most genetic components of eyes historically responded to stress caused directly by light, including ultraviolet damage of DNA, oxidative stress, and production of aldehydes. We propose light-induced stress had a direct and prominent role in the evolution of eyes by bringing together genes to repair and prevent damage from light-stress, both before and during the evolution of eyes themselves. Stress-repair and stress-prevention genes were perhaps originally deployed as plastic responses to light and/or as beneficial mutations genetically driving expression where light was prominent. These stress-response genes sense, shield, and refract light but only as reactions to ongoing light stress. Once under regulatory-genetic control, they could be expressed before light stress appeared, evolve as a module, and be influenced by natural selection to increase functionality for sensing light, ultimately leading to complex eyes and behaviors. Recognizing the potentially prominent role of stress in eye evolution invites discussions of plasticity and assimilation and provides a hypothesis for why similar genes are repeatedly used in convergent eyes. Broadening the drivers of eye evolution encourages consideration of multi-faceted mechanisms of plasticity/assimilation and mutation/selection for complex novelties and innovations in general.
Throughout the evolutionary tree, there are gains and losses of morphological features, physiological processes, and behavioral patterns. Losses are perhaps nowhere so prominent as for subterranean organisms, which typically show reductions or losses of eyes and pigment. These losses seem easy to explain without recourse to natural selection. Its most modern form is the accumulation of selectively neutral, structurally reducing mutations. Selectionist explanations include direct selection, often involving metabolic efficiency in resource poor subterranean environments, and pleiotropy, where genes affecting eyes and pigment have other effects, such as increasing extra-optic sensory structures. This dichotomy echoes the debate in evolutionary biology in general about the sufficiency of natural selection as an explanation of evolution, e.g., Kimura’s neutral mutation theory. Tests of the two hypotheses have largely been one-sided, with data supporting that one or the other processes is occurring. While these tests have utilized a variety of subterranean organisms, the Mexican cavefish,
- NSF-PAR ID:
- 10471616
- Publisher / Repository:
- Frontiers
- Date Published:
- Journal Name:
- Frontiers in Ecology and Evolution
- Volume:
- 11
- ISSN:
- 2296-701X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Barluenga, Marta (Ed.)Abstract Trait loss represents an intriguing evolutionary problem, particularly when it occurs across independent lineages. Fishes in light-poor environments often evolve “troglomorphic” traits, including reduction or loss of both pigment and eyes. Here, we investigate the genomic basis of trait loss in a blind and depigmented African cichlid, Lamprologus lethops, and explore evolutionary forces (selection and drift) that may have contributed to these losses. This species, the only known blind cichlid, is endemic to the lower Congo River. Available evidence suggests that it inhabits deep, low-light habitats. Using genome sequencing, we show that genes related to eye formation and pigmentation, as well as other traits associated with troglomorphism, accumulated inactivating mutations rapidly after speciation. A number of the genes affected in L. lethops are also implicated in troglomorphic phenotypes in Mexican cavefish (Astyanax mexicanus) and other species. Analysis of heterozygosity patterns across the genome indicates that L. lethops underwent a significant population bottleneck roughly 1 Ma, after which effective population sizes remained low. Branch-length tests on a subset of genes with inactivating mutations show little evidence of directional selection; however, low overall heterozygosity may reduce statistical power to detect such signals. Overall, genome-wide patterns suggest that accelerated genetic drift from a severe bottleneck, perhaps aided by directional selection for the loss of physiologically expensive traits, caused inactivating mutations to fix rapidly in this species.more » « less
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Trait loss represents an intriguing evolutionary problem, particularly when it occurs across independent lineages. Fishes in light-poor environments often evolve “troglomorphic” traits, including reduction or loss of both pigment and eyes. Here, we investigate the genomic basis of trait loss in a blind and depigmented African cichlid, Lamprologus lethops, and explore evolutionary forces (selection and drift) that may have contributed to these losses. This species, the only known blind cichlid, is endemic to the lower Congo River. Available evidence suggests that it inhabits deep, low-light habitats. Using genome sequencing, we show that genes related to eye formation and pigmentation, as well as other traits associated with troglomorphism, accumulated inactivating mutations rapidly after speciation. A number of the genes affected in L. lethops are also implicated in troglomorphic phenotypes in Mexican cavefish(Astyanax mexicanus) and other species. Analysis of heterozygosity patterns across the genome indicates that L. lethops underwent significant population bottleneck roughly 1Ma, after which effective population sizes remained low. Branch-length tests on a subset of genes with inactivating mutations show little evidence of directional selection; however, low overall heterozygosity may reduce statistical power to detect such signals. Overall, genome-wide patterns suggest that accelerated genetic drift from a severe bottleneck, perhaps aided by directional selection for the loss of physiologically expensive traits, caused inactivating mutations to fix rapidly in this species.more » « less
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null (Ed.)Changes in cis-regulatory elements play important roles in adaptation and phenotypic evolution. However, their contribution to metabolic adaptation of organisms is less understood. Here we have utilized a unique vertebrate model, Astyanax mexicanus, different morphotypes of which survive in nutrient-rich surface and nutrient-deprived cave water to uncover gene regulatory networks in metabolic adaptation. We performed genome-wide epigenetic profiling in the liver tissue of one surface and two independently derived cave populations. We find that many cis-regulatory elements differ in their epigenetic status/chromatin accessibility between surface fish and cavefish, while the two independently derived cave populations have evolved remarkably similar regulatory signatures. These differentially accessible regions are associated with genes of key pathways related to lipid metabolism, circadian rhythm and immune system that are known to be altered in cavefish. Using in vitro and in vivo functional testing of the candidate cis-regulatory elements, we find that genetic changes within them cause quantitative expression differences. We characterized one cis-regulatory element in the hpdb gene and found a genomic deletion in cavefish that abolishes binding of the transcriptional repressor IRF2 in vitro and derepresses enhancer activity in reporter assays. Genetic experiments further validated a cis-mediated role of the enhancer and suggest a role of this deletion in the upregulation of hpdb in wild cavefish populations. Selection of this mutation in multiple independent cave populations supports its importance in the adaptation to the cave environment, providing novel molecular insights into the evolutionary trade-off between loss of pigmentation and adaptation to a food-deprived cave environment.more » « less
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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.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fevo.2023.1080503
