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1. A chromosome-level genome of Astyanax mexicanus surface fish for comparing population-specific genetic differences contributing to trait evolution

   https://doi.org/10.1038/s41467-021-21733-z  

   Warren, Wesley C. ; Boggs, Tyler E. ; Borowsky, Richard ; Carlson, Brian M. ; Ferrufino, Estephany ; Gross, Joshua B. ; Hillier, LaDeana ; Hu, Zhilian ; Keene, Alex C. ; Kenzior, Alexander ; et al ( December 2021 , Nature Communications)

   null (Ed.)

   Abstract Identifying the genetic factors that underlie complex traits is central to understanding the mechanistic underpinnings of evolution. Cave-dwelling Astyanax mexicanus populations are well adapted to subterranean life and many populations appear to have evolved troglomorphic traits independently, while the surface-dwelling populations can be used as a proxy for the ancestral form. Here we present a high-resolution, chromosome-level surface fish genome, enabling the first genome-wide comparison between surface fish and cavefish populations. Using this resource, we performed quantitative trait locus (QTL) mapping analyses and found new candidate genes for eye loss such as dusp26 . We used CRISPR gene editing in A. mexicanus to confirm the essential role of a gene within an eye size QTL, rx3 , in eye formation. We also generated the first genome-wide evaluation of deletion variability across cavefish populations to gain insight into this potential source of cave adaptation. The surface fish genome reference now provides a more complete resource for comparative, functional and genetic studies of drastic trait differences within a species. 

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2. Selection-driven trait loss in independently evolved cavefish populations

   https://doi.org/10.1038/s41467-023-37909-8  

   Moran, Rachel L. ; Richards, Emilie J. ; Ornelas-García, Claudia Patricia ; Gross, Joshua B. ; Donny, Alexandra ; Wiese, Jonathan ; Keene, Alex C. ; Kowalko, Johanna E. ; Rohner, Nicolas ; McGaugh, Suzanne E. ( May 2023 , Nature Communications)

   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.

    

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3. Trait Loss in Evolution: What Cavefish Have Taught Us about Mechanisms Underlying Eye Regression

   https://doi.org/10.1093/icb/icad032  

   Sifuentes-Romero, Itzel ; Aviles, Ari_M ; Carter, Joseph_L ; Chan-Pong, Allen ; Clarke, Anik ; Crotty, Patrick ; Engstrom, David ; Meka, Pranav ; Perez, Alexandra ; Perez, Riley ; et al ( May 2023 , Integrative And Comparative Biology)

   Reduction or complete loss of traits is a common occurrence throughout evolutionary history. In spite of this, numerous questions remain about why and how trait loss has occurred. Cave animals are an excellent system in which these questions can be answered, as multiple traits, including eyes and pigmentation, have been repeatedly reduced or lost across populations of cave species. This review focuses on how the blind Mexican cavefish, Astyanax mexicanus, has been used as a model system for examining the developmental, genetic, and evolutionary mechanisms that underlie eye regression in cave animals. We focus on multiple aspects of how eye regression evolved in A. mexicanus, including the developmental and genetic pathways that contribute to eye regression, the effects of the evolution of eye regression on other traits that have also evolved in A. mexicanus, and the evolutionary forces contributing to eye regression. We also discuss what is known about the repeated evolution of eye regression, both across populations of A. mexicanus cavefish and across cave animals more generally. Finally, we offer perspectives on how cavefish can be used in the future to further elucidate mechanisms underlying trait loss using tools and resources that have recently become available.

    

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4. Transcriptomic analysis of the Brazilian blind characid, Stygichthys typhlops, reveals convergent selection with Astyanax mexicanus and other cavefishes

   https://doi.org/10.3389/fevo.2023.1076756  

   Arcila, Dahiana ; Rincon-Sandoval, Melissa ; Hanson, William ; Hart, Pamela B. ; González, Vanessa L. ; Betancur-R, Ricardo ; Bichuette, Maria E. ( May 2023 , Frontiers in Ecology and Evolution)

   Molecular studies have shown that Neotropical fishes of the order Characiformes have undergone two independent events of cave colonization. Among these fishes are the Mexican blind cavefish ( Astyanax mexicanus ), a well-studied model system for cave adaptation, and the lesser-known Brazilian blind characid ( Stygichthys typhlops ). Although various genomic and transcriptomic approaches have been used to identify genes responsible for cave adaptation in A. mexicanus , these genetic factors have not been explored in an evolutionary comparative framework in cave-adapted characiforms. To address this gap, we assembled a de novo transcriptome for the Brazilian blind characid, identifying 27,845 assembled unigenes, of which 22,580 were assigned as putative one-to-one orthologs to the Mexican cavefish. We then used the package RELAX to analyze 789 genes in cavefishes, identifying 311 genes under intensified or relaxed selection. Our analysis revealed 26 genes with signatures of convergent, relaxed selection linked to vision, circadian cycles, pigmentation, and hematopoiesis processes. Additionally, we conducted differential gene expression analyzes between the snout region and a control tissue sample (muscle), identifying 96 differentially expressed genes associated with cell-surface-bound and calcium-binding proteins. Our study offers insights into the genetic mechanisms underlying cave adaptation in characiform fishes, particularly the Brazilian blind characid. Moreover, our transcriptome dataset and list of genes under convergent, relaxed, and intensified selection serve as a valuable resource for future functional studies of genes involved in cave adaptation. Our work highlights the importance of examining genetic adaptations in multiple independent lineages to better understand the evolutionary processes underlying cave adaptation. 

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5. Comparative transcriptome analysis of wild and lab populations of Astyanax mexicanus uncovers differential effects of environment and morphotype on gene expression

   https://doi.org/10.1002/jez.b.22933  

   Krishnan, Jaya ; Persons, Jenna L. ; Peuß, Robert ; Hassan, Huzaifa ; Kenzior, Alexander ; Xiong, Shaolei ; Olsen, Luke ; Maldonado, Ernesto ; Kowalko, Johanna E. ; Rohner, Nicolas ( February 2020 , Journal of Experimental Zoology Part B: Molecular and Developmental Evolution)

   Studying how different genotypes respond to environmental variation is essential to understand the genetic basis of adaptation. The Mexican tetra,Astyanax mexicanus, has cave and surface‐dwelling morphotypes that have adapted to entirely different environments in the wild, and are now successfully maintained in lab conditions. While this has enabled the identification of genetic adaptations underlying a variety of physiological processes, few studies have directly compared morphotypes between lab‐reared and natural populations. Such comparative approaches could help dissect the varying effects of environment and morphotype, and determine the extent to which phenomena observed in the lab are generalizable to conditions in the field. To this end, we take a transcriptomic approach to compare the Pachón cavefish and their surface fish counterparts in their natural habitats and the lab environment. We identify key changes in expression of genes implicated in metabolism and physiology between groups of fish, suggesting that morphotype (surface or cave) and environment (natural or lab) both alter gene expression. We find gene expression differences between cave and surface fish in their natural habitats are much larger than differences in expression between morphotypes in the lab environment. However, lab‐raised cave and surface fish still exhibit numerous gene expression changes, supporting genetically encoded changes in livers of this species. From this, we conclude that a controlled laboratory environment may serve as an ideal setting to study the genetic underpinnings of metabolic and physiological differences between the cavefish and surface fish.

    

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