Genetic architecture underlying changes in carotenoid accumulation during the evolution of the blind Mexican cavefish, Astyanax mexicanus.
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ABSTRACT:
SUBMITTER: Riddle MR
PROVIDER: S-EPMC7708440 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Astyanax mexicanus, a teleost fish that exists in a river-dwelling surface form and multiple cave-dwelling forms, is an excellent system for studying the genetic basis of evolution. Cavefish populations, which independently evolved from surface fish ancestors multiple times, have evolved a number of morphological and behavioral traits. Quantitative trait loci (QTL) analyses have been performed to identify the genetic basis of many of these traits. These studies, combined with recent sequencing of the genome, provide a unique opportunity to identify candidate genes for these cave-specific traits. However, tools to test the requirement of these genes must be established to evaluate the role of candidate genes in generating cave-specific traits. To address this need, we designed transcription activator-like effector nucleases (TALENs) to target two genes that contain coding changes in cavefish relative to surface fish and map to the same location as QTL for pigmentation, oculocutaneous albinism 2 (oca2) and melanocortin 1 receptor (mc1r). We found that surface fish genes can be mutated using this method. TALEN-induced mutations in oca2 result in mosaic loss of melanin pigmentation visible as albino patches in F0 founder fish, suggesting biallelic gene mutations in F0s and allowing us to evaluate the role of this gene in pigmentation. The pigment cells in the albino patches can produce melanin upon treatment with L-DOPA, behaving similarly to pigment cells in albino cavefish and providing additional evidence that oca2 is the gene within the QTL responsible for albinism in cavefish. This technology has the potential to introduce a powerful tool for studying the role of candidate genes responsible for the evolution of cavefish traits.
| S-EPMC4361574 | biostudies-literature
Project description:Distinct populations of Astyanax mexicanus cavefish offer striking examples of repeatable convergence or parallelism in their independent evolutions from surface to cave phenotypes. However, the extent to which the repeatability of evolution occurred at the genetic level remains poorly understood. To address this, we first characterized the genetic diversity of 518 single-nucleotide polymorphisms (SNPs), obtained through RAD tag sequencing and distributed throughout the genome, in seven cave and three groups of surface populations. The cave populations represented two distinct lineages (old and new). Thirty-one SNPs were significantly differentiated between surface and old cave populations, two SNPs were differentiated between surface and new cave populations, and 44 SNPs were significantly differentiated in both old and new cave populations. In addition, we determined whether these SNPs map to the same locations of previously described quantitative trait loci (QTL) between surface and cave populations. A total of 25 differentiated SNPs co-map with several QTL, such as one containing a fibroblast growth factor gene (Fgf8) involved in eye development and lens size. Further, the identity of many SNPs that co-mapped with QTL was the same in independently derived cave populations. These conclusions were further confirmed by haplotype analyses of SNPs within QTL regions. Our findings indicate that the repeatability of evolution at the genetic level is substantial, suggesting that ancestral standing genetic variation significantly contributed to the population genetic variability used in adaptation to the cave environment.
| S-EPMC3808867 | biostudies-other
Project description:BackgroundCave animals converge evolutionarily on a suite of troglomorphic traits, the best known of which are eyelessness and depigmentation. We studied 11 cave and 10 surface populations of Astyanax mexicanus in order to better understand the evolutionary origins of the cave forms, the basic genetic structuring of both cave and surface populations, and the degree to which present day migration among them affects their genetic divergence.ResultsTo assess the genetic structure within populations and the relationships among them we genotyped individuals at 26 microsatellite loci. We found that surface populations are similar to one another, despite their relatively large geographic separation, whereas the cave populations are better differentiated. The cave populations we studied span the full range of the cave forms in three separate geographic regions and have at least five separate evolutionary origins. Cave populations had lower genetic diversity than surface populations, correlated with their smaller effective population sizes, probably the result of food and space limitations. Some of the cave populations receive migrants from the surface and exchange migrants with one another, especially when geographically close. This admixture results in significant heterozygote deficiencies at numerous loci due to Wahlund effects. Cave populations receiving migrants from the surface contain small numbers of individuals that are intermediate in both phenotype and genotype, affirming at least limited gene flow from the surface.ConclusionsCave populations of this species are derived from two different surface stocks denoted "old" and "new." The old stock colonized caves at least three times independently while the new stock colonized caves at least twice independently. Thus, the similar cave phenotypes found in these caves are the result of repeated convergences. These phenotypic convergences have occurred in spite of gene flow from surface populations suggesting either strong natural or sexual selection for alleles responsible for the cave phenotype in the cave environment.
| S-EPMC3282648 | biostudies-literature
Project description:Organisms living in the subterranean biome evolve extreme characteristics including vision loss and sensory expansion. Despite prior work linking certain genes to Mendelian traits, the genetic basis for complex cave-associated traits remains unknown. Moreover, it is unclear if certain forms of genetic variation (e.g., indels, copy number variants) are more common in regressive evolution. Progress in this area has been limited by a lack of suitable natural model systems and genomic resources. In recent years, the Mexican tetra, Astyanax mexicanus, has advanced as a model for cave biology and regressive evolution. Here, we present the results of a genome-wide screen for in-frame indels using alignments of RNA-sequencing reads to the draft cavefish genome. Mutations were discovered in three genes associated with blood physiology (mlf1, plg, and wdr1), two genes associated with growth factor signaling (ghrb, rnf126), one gene linked to collagen defects (mia3), and one gene which may have a global epigenetic impact on gene expression (mki67). With one exception, polymorphisms were shared between Pachón and Tinaja cavefish lineages, and different from the surface-dwelling lineage. We confirmed the presence of mutations using direct Sanger sequencing and discovered remarkably similar developmental expression in both morphs despite substantial coding sequence alterations. Further, three mutated genes mapped near previously established quantitative trait loci associated with jaw size, condition factor, lens size, and neuromast variation. This work reveals previously unappreciated traits evolving in this species under environmental pressures (e.g., blood physiology) and provides insight to genetic changes underlying convergence of organisms evolving in complete darkness.
| S-EPMC6751357 | biostudies-literature
Project description:As a consequence of adaptation to the cave environment, the blind Mexican cavefish, Astyanax mexicanus, has evolved several cranial aberrations including changes to bone sizes, shapes and presence of numerous lateral asymmetries. Prior studies of cranial asymmetry in cavefish focused strictly on adult specimens. Thus, the extent to which these asymmetries emerge in adulthood, or earlier in the life history of cavefish, was unknown. We performed a geometric morphometric analysis of shape variation in the chondrocranium and osteocranium across life history in two distinct cavefish populations and surface-dwelling fish. The cartilaginous skull in juveniles was bilaterally symmetric and chondrocranial shape was conserved in all three populations. In contrast, bony skull shapes segregated into significantly distinct groups in adults. Cavefish demonstrated significant asymmetry for the bones surrounding the collapsed eye orbit, and the opercle bone posterior to the eye orbit. Interestingly, we discovered that cavefish also exhibit directional "bends" in skull shape, almost always biased to the left. In sum, this work reveals that asymmetric craniofacial aberrations emerge later in the cavefish life history. These abnormalities may mirror asymmetries in the lateral line sensory system, reflect a 'handedness' in cavefish swimming behavior, or evolve through neutral processes.
| S-EPMC5423691 | biostudies-literature
Project description:The retina is the light-sensitive tissue of the eye that facilitates vision. Mutations within genes affecting eye development and retinal function cause a host of degenerative visual diseases, including retinitis pigmentosa and anophthalmia/microphthalmia. The characin fish Astyanax mexicanus includes both eyed (surface fish) and eyeless (cavefish) morphs that initially develop eyes with normal retina; however, early in development, the eyes of cavefish degenerate. Since both surface and cave morphs are members of the same species, they serve as excellent evolutionary mutant models with which to identify genes causing retinal degeneration. In this study, we crossed the eyed and eyeless forms of A. mexicanus and quantified the thickness of individual retinal layers among 115 F(2) hybrid progeny. We used next generation sequencing (RAD-seq) and microsatellite mapping to construct a dense genetic map of the Astyanax genome, scan for quantitative trait loci (QTL) affecting retinal thickness, and identify candidate genes within these QTL regions. The map we constructed for Astyanax includes nearly 700 markers assembled into 25 linkage groups. Based on our scans with this map, we identified four QTL, one each associated with the thickness of the ganglion, inner nuclear, outer plexiform, and outer nuclear layers of the retina. For all but one QTL, cavefish alleles resulted in a clear reduction in the thickness of the affected layer. Comparative mapping of genetic markers within each QTL revealed that each QTL corresponds to an approximately 35 Mb region of the zebrafish genome. Within each region, we identified several candidate genes associated with the function of each affected retinal layer. Our study is the first to examine Astyanax retinal degeneration in the context of QTL mapping. The regions we identify serve as a starting point for future studies on the genetics of retinal degeneration and eye disease using the evolutionary mutant model Astyanax.
| S-EPMC3577753 | biostudies-literature
Project description:The evolutionary forces driving the reduction of eyes and pigmentation in cave-adapted animals are unknown; Darwin famously questioned the role of natural selection in eye loss in cave fishes: "As it is difficult to imagine that eyes, although useless, could be in any way injurious to animals living in darkness, I attribute their loss wholly to disuse"[1]. We studied the genetics of eye and pigmentation regression in the Mexican cave tetra, Astyanax mexicanus, by mapping and quantitative trait loci (QTL) analysis. We also mapped QTL for the putatively constructive traits of jaw size, tooth number, and numbers of taste buds. The data suggest that eyes and pigmentation regressed through different mechanisms. Cave alleles at every eye or lens QTL we detected caused size reductions, consistent with evolution by natural selection but not with drift. QTL polarities for melanophore number were mixed, however, consistent with genetic drift. Arguments against a role for selection in the regression of cave-fish eyes cited the insignificant cost of their development [2, 3], but we argue that the energetic cost of their maintenance is sufficiently high for eyes to be detrimental in the cave environment. Regression can be caused either by selection or drift.
| S-EPMC2570642 | biostudies-literature
Project description:BACKGROUND:Cavefish populations belonging to the Mexican tetra species Astyanax mexicanus are outstanding models to study the tempo and mode of adaptation to a radical environmental change. They are currently assigned to two main groups, the so-called "old" and "new" lineages, which would have populated several caves independently and at different times. However, we do not have yet accurate estimations of the time frames of evolution of these populations. RESULTS:We reanalyzed the geographic distribution of mitochondrial and nuclear DNA polymorphisms and we found that these data do not support the existence of two cavefish lineages. Using IMa2, a program that allows dating population divergence in addition to demographic parameters, we found that microsatellite polymorphism strongly supports a very recent origin of cave populations (<?20,000 years). We identified a large number of single-nucleotide polymorphisms (SNPs) in transcript sequences of pools of embryos (Pool-seq) belonging to Pachón cave population and a surface population from Texas. Based on summary statistics that can be computed with this SNP data set together with simulations of evolution of SNP polymorphisms in two recently isolated populations, we looked for sets of demographic parameters that allow the computation of summary statistics with simulated populations that are similar to the ones with the sampled populations. In most simulations for which we could find a good fit between the summary statistics of observed and simulated data, the best fit occurred when the divergence between simulated populations was less than 30,000 years. CONCLUSIONS:Although it is often assumed that some cave populations have a very ancient origin, a recent origin of these populations is strongly supported by our analyses of independent sets of nuclear DNA polymorphism. Moreover, the observation of two divergent haplogroups of mitochondrial and nuclear genes with different geographic distributions support a recent admixture of two divergent surface populations, before the isolation of cave populations. If cave populations are indeed only several thousand years old, many phenotypic changes observed in cavefish would thus have mainly involved the fixation of genetic variants present in surface fish populations and within a very short period of time.
| S-EPMC5905186 | biostudies-literature
Project description:BackgroundThe Mexican tetra (Astyanax mexicanus) has emerged as a good animal model to study the constructive and regressive changes associated with living in cave environments, as both the ancestral sighted morph and the cave dwelling morph are extant. The cave dwelling morphs lack eyes and body pigmentation, but have well developed oral and sensory systems that are essential for survival in dark environments. The cave forms and surface forms are interfertile and give rise to F1 hybrids progeny known as intermediates. In cavefish, degeneration of the lens is one of the key events leading to eye regression. We have previously shown that surgical lens removal in surface fish embryos has an effect on the craniofacial skeleton. Surprisingly, lens removal was also found to have an effect on the caudal teeth in the lower jaw. In order to understand this result, we analyzed the lower jaw and upper jaw dentitions of surface, cavefish and F1 hybrids of surface and cavefish and compared our findings with surface fish that underwent lens removal. We also investigated the upper jaw (premaxillae and maxillae) dentition in these fish.ResultsOur tooth analyses shows that cavefish have the highest numbers of teeth in the mandible and maxillae, surface forms have the lowest numbers and F1 hybrids are between these groups. These differences are not observed in the premaxillae. A wide diversity of cuspal morphology can also be found in these fish. Jaw size also differs amongst the groups, with the mandible exhibiting the greatest differences. Interestingly, tooth number in surgery fish is different only in the caudal region of the mandible; this is the region that is constrained in size in all morphs.ConclusionOur data provides the first detailed description of the jaw dentitions of two morphs of Astyanax mexicanus, as well as in F1 hybrids. Tooth number, patterning and cuspal morphology are enhanced in cavefish in all jaws. This is in contrast to the increase in tooth number previously observed on the lens ablated side of the surgery fish. These findings indicate that the mechanisms which govern the constructive traits in cavefish are different to the mechanisms causing an increase tooth number in surgery fish.
| S-EPMC3852964 | biostudies-literature
Project description:Adaptive behaviors emerge in novel environments through functional changes in neural circuits. While relationships between circuit function and behavior have been well studied, how evolution shapes those circuits and leads to behavioral adpation is poorly understood. The Mexican cavefish, Astyanax mexicanus, provides a unique genetically amendable model system, equipped with above ground eyed surface fish and multiple evolutionarily divergent populations of blind cavefish that have evolved in complete darkness. These differences in environment and vision provide an opprotunity to examine how a neural circuit is functionally influenced by the presence of light. Here, we examine differences in the detection, and behavioral response induced by non visual light reception. Both populations exhibit photokinetic behavior, with surface fish becoming hyperactive following sudden darkness and cavefish becoming hyperactive following sudden illumination. To define these photokinetic neural circuits, we integrated whole brain functional imaging with our Astyanax brain atlas for surface and cavefish responding to light changes. We identified the caudal posterior tuberculum as the central modulator for both light or dark stimulated photokinesis. To unconver how spatiotemporal neuronal activity differed between surface fish and cavefish, we used stable pan-neuronal GCaMP Astyanax transgenics to show that a subpopulation of darkness sensitve neurons in surface fish are now light senstive in cavefish. Further functional analysis revealed that this integrative switch is dependent on dopmane signaling, suggesting a key role for dopamine and a highly conserved dopamine circuit in modulating the evolution of a circuit driving an essential behavior. Together, these data shed light into how neural circuits evolved to adapte to novel settings, and reveal the power of Astyanax as a model to elucidate mechanistic ingiths underlying sensory adaptation.
| S-EPMC11291158 | biostudies-literature