Review
doi: 10.1016/j.tig.2023.10.002. Epub 2023 Oct 26.From darkness to discovery: evolutionary, adaptive, and translational genetic insights from cavefish
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- PMID:38707509
- PMCID: PMC11068324
- DOI: 10.1016/j.tig.2023.10.002
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Review
From darkness to discovery: evolutionary, adaptive, and translational genetic insights from cavefish
Amruta Swaminathan et al. Trends Genet.2024 Jan.
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Abstract
How genotype determines phenotype is a well-explored question, but genotype-environment interactions and their heritable impact on phenotype over the course of evolution are not as thoroughly investigated. The fishAstyanax mexicanus, consisting of surface and cave ecotypes, is an ideal emerging model to study the genetic basis of adaptation to new environments. This model has permitted quantitative trait locus mapping and whole-genome comparisons to identify the genetic bases of traits such as albinism and insulin resistance and has helped to better understand fundamental evolutionary mechanisms. In this review, we summarize recent advances inA. mexicanus genetics and discuss their broader impact on the fields of adaptation and evolutionary genetics.
Keywords: Astyanax mexicanus; QTL mapping; adaptation; evolution; population genetics.
Conflict of interest statement
Declaration of Interests The authors declare no competing interests.
Figures
(A) Examples of cave-dwelling and subterranean species, from left to right: olm or cave salamanderProteus anguinus, mysid shrimpSpelaeomysis quinterensis found in the Dinaric Karst of the western Balkans, Tumbling Creek cavesnailAntrobia culveri found in Missouri, USA, and golden-line fishSinocyclocheilus anatirostris found in karst areas of southwest China. (B) The Mexican tetraAstyanax mexicanus: a widely used troglomorphic species to study adaptation. This species consists of a sighted river-dwelling surface ecotype (top) and blind cave ecotype (bottom), depicted here alongside their contrasting natural habitats. (C) Map showing the locations of several populations of the cave and surface ecotypes ofAstyanax mexicanus distributed in northeastern Mexico. Image sources: (A) olm cropped from [74] figure 1B, licensed under CC BY-NC-ND 4.0; mysid shrimp cropped from [75] figure 1B; cavesnail from Wikimedia Commons public domain; golden-line fish cropped from [76] figure 1B; (B)Astyanax natural habitat photographs courtesy of Riley Kellermeyer; (C) map ofAstyanax populations cropped from [9], figure 1B. Images licensed under CC BY 4.0 unless stated otherwise.
Abbreviation: SF, surface fish; CF, cavefish; ot, optic tectum; ol, olfactory lobe; DASPEI, (2-(4-(Dimethylamino)styryl)-N-ethylpyridinium iodide); microCT, micro-computed tomography ; H&E, hematoxylin and eosin. (A) The head regions of adult fish show the reduced eye size and pigmentation in cavefish. (B) DASPEI staining of the surface fish and cavefish larvae show increased superficial neuromasts in cavefish. (C) microCT images of dorsal cranium show the asymmetry in adult cavefish. (D) Different size and morphology shown by the dissected brains from surface fish and cavefish. (E) Left, the increased amount of visceral adipose tissue in cavefish shown by dissection and H&E staining. Right, H&E staining images of adult fish trunk show the reduced amount of muscle and increased amount of fat in cavefish. Image sources: (B, D) modified with the author’s permission from [6] figure 2F and figure 2C. (C) cropped from [77] figure 4A, 4D and 4E. (E) obtained from [78] figure 1A and [49] figure 1C, with permission from Elsevier. Images licensed under CC BY 4.0 unless stated otherwise.
(A) An illustration of QTL mapping and analysis. Phenotypically and genetically different surface fish (F0, left) and cavefish (F0, right) are crossed to generate F1 hybrids. F1 hybrid fish phenotypically resemble the parental surface fish. The F1 hybrids are intercrossed to generate F2 hybrids, which exhibit a wide range of phenotypes and genotypes. The whole genome is divided into linkage groups by molecular markers. The linkage probabilities (logarithm of the odds score, LOD score) between the quantitative trait and molecular markers are plotted in the linkage groups (bottom) for the F2 generation. Loci with LOD score above the statistical threshold (blue) are considered significantly associated with the trait. Fish illustrations modified from original by Mark Miller. (B) the workflow of candidate gene approaches.
Astyanax multi-species-coalescent phylogenetic tree cropped from [9], figure 1C, licensed under CC BY 4.0. Numbers at nodes indicate bootstrap node support values. Lineage 1 and Lineage 2 (new and old lineage, respectively, in older publications) are cave lineages from different ancestral surface fish stocks. Population names are color-coded according to lineage. As shown in the simplified map graphic on the left, lineage is correlated with geographical proximity of populations. Since surface and cave populations are interspersed in the tree, cave populations do not form a monophyletic clade and have multiple origins. The Subterráneo population (Micos region) is thought to have arisen from a Lineage 2 surface population but now extensively hybridized with Lineage 1 surface fish in the Micos region [9].
References
- Soares D and Niemiller ML (2020) Extreme adaptation in caves. Anat Rec (Hoboken) 303, 15–23 - PubMed
- Borowsky R. (2018) Cavefishes. Curr Biol 28, R60–R64 - PubMed
- Culver DC and Pipan T (2019) The biology of caves and other subterranean habitats. Oxford University Press
- Mitchell RW, et al. (1977) Mexican eyeless Characin fishes, genus Astyanax: environment, distribution, and evolution. KIP Monographs 17
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