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1. Genomic Analysis of the Only Blind Cichlid Reveals Extensive Inactivation in Eye and Pigment Formation Genes

   https://doi.org/10.1093/gbe/evaa144  

   Aardema, Matthew L ; Stiassny, Melanie L ; Alter, S Elizabeth ( August 2020 , Genome Biology and Evolution)

   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. 

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2. Genomic Analysis of the Only Blind Cichlid Reveals Extensive Inactivation in Eye and Pigment Formation Genes

   https://doi.org/doi:10.1093/gbe/evaa144  

   Matthew, L. Aardema ; Melanie, L.J. Stiassny ; S. Elizabeth, Alter ( July 2020 , Genome biology and evolution)

   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. 

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3. Light-induced stress as a primary evolutionary driver of eye origins

   https://doi.org/10.1093/icb/icz064  

   Swafford, Andrew J. M. ; Oakley, Todd H. ( September 2019 , Integrative and Comparative Biology)

   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.

    

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4. Evidence for rapid divergence of sensory systems between Texas populations of the Mexican tetra (Astyanax mexicanus)

   https://doi.org/10.3389/fevo.2023.1085975  

   Enriquez, Maya S. ; Swanson, Nathan ; Putland, Rosalyn L. ; Tait, Ti ; Gluesenkamp, Andrew G. ; McGaugh, Suzanne E. ; Mensinger, Allen F. ( February 2023 , Frontiers in Ecology and Evolution)

   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.

    

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5. Genome-wide analysis of cis-regulatory changes in the metabolic adaptation of cavefish

   https://doi.org/10.1101/2020.08.27.270371  

   Krishnan, Jaya SeidelChris W. Zhang ( August 2020 , bioRxiv)

   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. 

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