Evolutionary convergence of a neural mechanism in the cavefish lateral line system.
Ontology highlight
ABSTRACT:
SUBMITTER: Lunsford ET
PROVIDER: S-EPMC9246366 | biostudies-literature |
REPOSITORIES: biostudies-literature
Similar Datasets
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: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:Environmental perturbation can drive behavioral evolution and associated changes in brain structure and function. The Mexican fish species, Astyanax mexicanus, includes eyed river-dwelling surface populations and multiple independently evolved populations of blind cavefish. We used whole-brain imaging and neuronal mapping of 684 larval fish to generate neuroanatomical atlases of surface fish and three different cave populations. Analyses of brain region volume and neural circuits associated with cavefish behavior identified evolutionary convergence in hindbrain and hypothalamic expansion, and changes in neurotransmitter systems, including increased numbers of catecholamine and hypocretin/orexin neurons. To define evolutionary changes in brain function, we performed whole-brain activity mapping associated with behavior. Hunting behavior evoked activity in sensory processing centers, while sleep-associated activity differed in the rostral zone of the hypothalamus and tegmentum. These atlases represent a comparative brain-wide study of intraspecies variation in vertebrates and provide a resource for studying the neural basis of behavioral evolution.
| S-EPMC7494351 | biostudies-literature
Project description:In a developing nervous system, axonal arbors often undergo complex rearrangements before neural circuits attain their final innervation topology. In the lateral line sensory system of the zebrafish, developing sensory axons reorganize their terminal arborization patterns to establish precise neural microcircuits around the mechanosensory hair cells. However, a quantitative understanding of the changes in the sensory arbor morphology and the regulators behind the microcircuit assembly remain enigmatic. Here, we report that Semaphorin7A (Sema7A) acts as an important mediator of these processes. Utilizing a semi-automated three-dimensional neurite tracing methodology and computational techniques, we have identified and quantitatively analyzed distinct topological features that shape the network in wild-type and Sema7A loss-of-function mutants. In contrast to those of wild-type animals, the sensory axons in Sema7A mutants display aberrant arborizations with disorganized network topology and diminished contacts to hair cells. Moreover, ectopic expression of a secreted form of Sema7A by non-hair cells induces chemotropic guidance of sensory axons. Our findings propose that Sema7A likely functions both as a juxtracrine and as a secreted cue to pattern neural circuitry during sensory organ development.
| S-EPMC11318972 | biostudies-literature
Project description:Coding and non-coding mutations in DNA contribute significantly to phenotypic variability during evolution. However, less is known about the role of epigenetics in this process. Although previous studies have identified eye development genes associated with the loss-of-eyes phenotype in the Pachón blind cave morph of the Mexican tetra Astyanax mexicanus, no inactivating mutations have been found in any of these genes. Here, we show that excess DNA methylation-based epigenetic silencing promotes eye degeneration in blind cave A. mexicanus. By performing parallel analyses in A. mexicanus cave and surface morphs, and in the zebrafish Danio rerio, we have discovered that DNA methylation mediates eye-specific gene repression and globally regulates early eye development. The most significantly hypermethylated and downregulated genes in the cave morph are also linked to human eye disorders, suggesting that the function of these genes is conserved across vertebrates. Our results show that changes in DNA methylation-based gene repression can serve as an important molecular mechanism generating phenotypic diversity during development and evolution.
| S-EPMC6023768 | biostudies-literature
Project description:Collective cell migration plays an important role in development. Here, we study the posterior lateral line primordium (PLLP) a group of about 100 cells, destined to form sensory structures, that migrates from head to tail in the zebrafish embryo. We model mutually inhibitory FGF-Wnt signalling network in the PLLP and link tissue subdivision (Wnt receptor and FGF receptor activity domains) to receptor-ligand parameters. We then use a 3D cell-based simulation with realistic cell-cell adhesion, interaction forces, and chemotaxis. Our model is able to reproduce experimentally observed motility with leading cells migrating up a gradient of CXCL12a, and trailing (FGF receptor active) cells moving actively by chemotaxis towards FGF ligand secreted by the leading cells. The 3D simulation framework, combined with experiments, allows an investigation of the role of cell division, chemotaxis, adhesion, and other parameters on the shape and speed of the PLLP. The 3D model demonstrates reasonable behaviour of control as well as mutant phenotypes.
| S-EPMC5393887 | biostudies-literature
Project description:Coding and non-coding mutations in DNA contribute significantly to phenotypic variability during evolution. However, less is known about the role of epigenetics in this process. Although previous studies have identified eye development genes associated with the loss of eyes phenotype in the Pachón blind cave morph of the Mexican tetra Astyanax mexicanus1-6, no inactivating mutations have been found in any of these genes2,3,7-10. Here we show that excess DNA methylation-based epigenetic silencing promotes eye degeneration in blind cave Astyanax mexicanus. By performing parallel analyses in Astyanax mexicanus cave and surface morphs and in the zebrafish Danio rerio, we have discovered that DNA methylation mediates eye-specific gene repression and globally regulates early eye development. The most significantly hypermethylated and down-regulated genes in the cave morph are also linked to human eye disorders, suggesting the function of these genes is conserved across the vertebrates. Our results show that changes in DNA methylation-based gene repression can serve as an important molecular mechanism generating phenotypic diversity during development and evolution.
2018-05-01 | GSE109006 | GEO
Project description:The mechanosensory lateral line system is used by fishes to sense hydrodynamic stimuli in their environment. It provides information about flow regimes, proximity to substrate, and the presence and identity of prey and predators and represents a means of receiving communication signals from other fish. Thus we may expect lateral line system structures to be under strong divergent selection during adaptive radiation. Here, we used X-ray micro-computed tomography scans to quantify variation in cranial lateral line canal morphology within the adaptive radiation of Lake Malawi cichlids. We report that cranial lateral line canal morphology is strongly correlated with diet and other aspects of craniofacial morphology, including the shape of oral jaws. These results indicate an adaptive role for the lateral line system in prey detection and suggest that diversification of this system has taken an important role in the spectacular evolution of Lake Malawi's cichlid fish diversity.
| S-EPMC6542376 | biostudies-literature
Project description:Model microbial systems provide opportunity to understand the genetic bases of ecological traits, their evolution, regulation and fitness contributions. Experimental populations of Pseudomonas fluorescens rapidly diverge in spatially structured microcosms producing a range of surface-colonising forms. Despite divergent molecular routes, wrinkly spreader (WS) niche specialist types overproduce a cellulosic polymer allowing mat formation at the air-liquid interface and access to oxygen. Given the range of ways by which cells can form mats, such phenotypic parallelism is unexpected. We deleted the cellulose-encoding genes from the ancestral genotype and asked whether this mutant could converge on an alternate phenotypic solution. Two new traits were discovered. The first involved an exopolysaccharide encoded by pgaABCD that functions as cell-cell glue similar to cellulose. The second involved an activator of an amidase (nlpD) that when defective causes cell chaining. Both types form mats, but were less fit in competition with cellulose-based WS types. Surprisingly, diguanylate cyclases linked to cellulose overexpression underpinned evolution of poly-beta-1,6-N-acetyl-d-glucosamine (PGA)-based mats. This prompted genetic analyses of the relationships between the diguanylate cyclases WspR, AwsR and MwsR, and both cellulose and PGA. Our results suggest that c-di-GMP regulatory networks may have been shaped by evolution to accommodate loss and gain of exopolysaccharide modules facilitating adaptation to new environments.
| S-EPMC5322309 | biostudies-literature
Project description:The resurrection of ancestral enzymes of now-extinct organisms (paleogenetics) is a developing field that allows the study of evolutionary hypotheses otherwise impossible to be tested. In the present study, we target fungal peroxidases that play a key role in lignin degradation, an essential process in the carbon cycle and often a limiting step in biobased industries. Ligninolytic peroxidases are secreted by wood-rotting fungi, the origin of which was recently established in the Carboniferous period associated with the appearance of these enzymes. These first peroxidases were not able to degrade lignin directly and used diffusible metal cations to attack its phenolic moiety. The phylogenetic analysis of the peroxidases of Polyporales, the order in which most extant wood-rotting fungi are included, suggests that later in evolution these enzymes would have acquired the ability to degrade nonphenolic lignin using a tryptophanyl radical interacting with the bulky polymer at the surface of the enzyme. Here, we track this powerful strategy for lignin degradation as a phenotypic trait in fungi and show that it is not an isolated event in the evolution of Polyporales. Using ancestral enzyme resurrection, we study the molecular changes that led to the appearance of the same surface oxidation site in two distant peroxidase lineages. By characterization of the resurrected enzymes, we demonstrate convergent evolution at the amino acid level during the evolution of these fungi and track the different changes leading to phylogenetically distant ligninolytic peroxidases from ancestors lacking the ability to degrade nonphenolic lignin.
| S-EPMC6016776 | biostudies-literature