Eye morphogenesis in the blind Mexican cavefish.
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ABSTRACT:
SUBMITTER: Devos L
PROVIDER: S-EPMC8565469 | 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:Responding appropriately to stress is essential for survival, yet in pathological states, these responses can develop into debilitating conditions such as post-traumatic stress disorder and generalized anxiety. While genetic models have provided insight into the neurochemical and neuroanatomical pathways that underlie stress, little is known about how evolutionary processes and naturally occurring variation contribute to the diverse responses to stressful stimuli observed in the animal kingdom. The Mexican cavefish is a powerful system to address how altered genetic and neuronal systems can give rise to altered behaviors. When introduced into a novel tank, surface fish and cavefish display a stereotypic stress response, characterized by reduced exploratory behavior and increased immobility, akin to "freezing". The stress response in cave and surface forms is reduced by pharmacological treatment with the anxiolytic drug, buspirone, fortifying the notion that behavior in the assay represents a conserved stress state. We find that cave populations display reduced behavioral measures of stress compared to surface conspecifics, including increased time in the top half of the tank and fewer periods of immobility. Further, reduced stress responses are observed in multiple independently derived cavefish populations, suggesting convergence on loss of behavioral stress responses in the novel tank assay. These findings provide evidence of a naturally occurring species with two drastically different forms in which a shift in predator-rich ecology to one with few predators corresponds to a reduction in stress behavior.
| S-EPMC6444932 | biostudies-literature
Project description:The development and implementation of a scientific outreach activity comes with a number of challenges. A successful outreach event must match the sophistication of content to the audience, be engaging, expand the knowledge base for participants, and be inclusive for a diverse audience. Ideally, a successful event will also convey the importance of scientific outreach for future scientists and citizens. In this paper, we present a simple, hands-on guide to a scientific outreach event targeted to kindergarten learners. This activity also pursued a second goal: the inclusion of undergraduate students in the development and delivery of the event. We provided a detailed set of four activities, focusing on the blind Mexican cavefish, which were enthusiastically received by kindergarten audiences. The engagement of undergraduate students in the development of this activity encouraged public outreach involvement and fostered new scientific and communication skills. The format of the outreach event we describe is flexible. We provide a set of guidelines and suggestions for adapting this approach to other biological topics. The activity and approach we describe enables the implementation of effective scientific outreach, using active learning approaches, which benefits both elementary school learners and undergraduate students.
| S-EPMC5604892 | biostudies-literature
Project description:Fish reproductive patterns are very diverse in terms of breeding frequency, mating system, sexual dimorphisms and selection, mate choice, spawning site choice, courtship patterns, spawning behaviors and parental care. Here we have compared the breeding behavior of the surface-dwelling and cave-dwelling morphs of the characiform A. mexicanus, with the goals of documenting the spawning behavior in this emerging model organism, its possible evolution after cave colonization, and the sensory modalities involved. Using infrared video recordings, we showed that cave and surface Astyanax spawning behavior is identical, occurs in the dark, and can be divided into 5 rapid phases repeated many times, about once per minute, during spawning sessions which last about one hour and involve one female and several males. Such features may constitute "pre-adaptive traits" which have facilitated fish survival after cave colonization, and may also explain how the two morphs can hybridize in the wild and in the laboratory. Accordingly, cross-breeding experiments involving females of one morphotype and males of the other morphotype showed the same behavior including the same five phases. However, breeding between cavefish females and surface fish males was more frequent than the reverse. Finally, cavefish female pheromonal solution was able to trigger strong behavioral responses in cavefish males-but not on surface fish males. Lastly, egg production seemed higher in surface fish females than in cavefish females. These results are discussed with regards to the sensory modalities involved in triggering reproductive behavior in the two morphs, as well as its possible ongoing evolution.
| S-EPMC6382271 | biostudies-literature
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:Feeding strategies are dependent on multi-modal sensory processing, that integrates visual, chemosensory, and mechanoreceptive cues. In many fish species, local environments and food availability dramatically influence the evolution of sensory and morphological traits that underlie feeding. The Mexican cavefish, Astyanax mexicanus, have developed robust changes in sensory-dependent behaviors, but the impact on prey detection and feeding behavior is not known. In the absence of eyes, cavefish have evolved enhanced sensitivity of the lateral line, comprised of mechanosensory organs that sense water flow and detect prey. Here, we identify evolved differences in prey capture behavior of larval cavefish that are dependent on lateral line sensitivity. Under lighted conditions, cavefish strike Artemia prey at a wider angle than surface fish; however, this difference is diminished under dark conditions. In addition, the strike distance is greater in cavefish than surface fish, revealing an ability to capture, and likely detect, prey at greater distances. Experimental ablation of the lateral line disrupts prey capture in cavefish under both light and dark conditions, while it only impacts surface fish under dark conditions. Together, these findings identify an evolutionary shift towards a dependence on the lateral line for prey capture in cavefish, providing a model for investigating how loss of visual cues impacts multi-modal sensory behaviors.
| S-EPMC6450390 | 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:Although Astyanax mexicanus surface fish regenerate their hearts after injury, their Pachón cave-dwelling counterparts cannot and, instead, form a permanent fibrotic scar, similar to the human heart. Myocardial proliferation peaks at similar levels in both surface fish and Pachón 1 week after injury. However, in Pachón, this peak coincides with a strong scarring and immune response, and ultimately, cavefish cardiomyocytes fail to replace the scar. We identified lrrc10 to be upregulated in surface fish compared with Pachón after injury. Similar to cavefish, knockout of lrrc10 in zebrafish impairs heart regeneration without affecting wound cardiomyocyte proliferation. Furthermore, using quantitative trait locus (QTL) analysis, we have linked the degree of heart regeneration to three loci in the genome, identifying candidate genes fundamental to the difference between scarring and regeneration. Our study provides evidence that successful heart regeneration entails a delicate interplay between cardiomyocyte proliferation and scarring.
| S-EPMC6280125 | biostudies-literature
Project description:The blind cavefish Astyanax mexicanus undergoes bilateral eye degeneration during embryonic development. Despite the absence of light in the cave environment, cavefish have retained a structurally intact pineal eye. We show here that contrary to visual degeneration in the bilateral eyes, the cavefish pineal eye has conserved the ability to detect light. Larvae of two different Astyanax cavefish populations and the con-specific sighted surface-dwelling form (surface fish) respond similarly to light dimming by shading the pineal eye. As a response to shading, cavefish larvae swim upward vertically. This behavior resembles that of amphibian tadpoles rather than other teleost larvae, which react to shadows by swimming downward. The shadow response is highest at 1.5-days post-fertilization (d.p.f.), gradually diminishes, and is virtually undetectable by 7.5 d.p.f. The shadow response was substantially reduced after surgical removal of the pineal gland from surface fish or cavefish larvae, indicating that it is based on pineal function. In contrast, removal of one or both bilateral eye primordia did not affect the shadow response. Consistent with its light detecting capacity, immunocytochemical studies indicate that surface fish and cavefish pineal eyes express a rhodopsin-like antigen, which is undetectable in the degenerating bilateral eyes of cavefish larvae. We conclude that light detection by the pineal eye has been conserved in cavefish despite a million or more years of evolution in complete darkness.
| S-EPMC3584714 | biostudies-literature