A Hypomorphic Cystathionine ß-Synthase Gene Contributes to Cavefish Eye Loss by Disrupting Optic Vasculature

AbstractVestigial structures are key indicators of evolutionary descent but the mechanisms underlying their development are poorly understood. This study examines vestigial eye formation in the teleost Astyanax mexicanus, which consists of a sighted surface-dwelling morph and different populations of blind cave morphs. Cavefish embryos initially develop optic primordia but vestigial eyes are formed during larval development. Multiple genetic factors are involved in cavefish eye loss but none of the mutated genes have been identified. Here we identify cystathionine ß-synthase (cbsa), which encodes the key enzyme of the transsulfuration pathway, as a mutated gene responsible for eye degeneration in multiple cavefish populations. The inactivation of cbsa affects eye development by inducing accumulation of the transsulfuration intermediate homocysteine and defects in optic vasculature, including aneurysms and eye hemorrhages, leading to oxygen deficiency. Our findings suggest that localized modifications in the circulatory system and hypoxia had important roles in the evolution of vestigial eyes in blind cavefish.

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A hypomorphic cystathionine ß-synthase gene contributes to cavefish eye loss by disrupting optic vasculature

Nature Communications ◽

10.1038/s41467-020-16497-x ◽

2020 ◽

Vol 11 (1) ◽

Cited By ~ 1

Author(s):

Li Ma ◽

Aniket V. Gore ◽

Daniel Castranova ◽

Janet Shi ◽

Mandy Ng ◽

...

Keyword(s):

Circulatory System ◽

Astyanax Mexicanus ◽

Transsulfuration Pathway ◽

Key Enzyme ◽

Surface Dwelling ◽

Blind Cave ◽

Vestigial Structures ◽

Key Indicators ◽

Evolutionary Descent ◽

Eye Formation

Abstract Vestigial structures are key indicators of evolutionary descent, but the mechanisms underlying their development are poorly understood. This study examines vestigial eye formation in the teleost Astyanax mexicanus, which consists of a sighted surface-dwelling morph and multiple populations of blind cave morphs. Cavefish embryos initially develop eyes, but they subsequently degenerate and become vestigial structures embedded in the head. The mutated genes involved in cavefish vestigial eye formation have not been characterized. Here we identify cystathionine ß-synthase a (cbsa), which encodes the key enzyme of the transsulfuration pathway, as one of the mutated genes responsible for eye degeneration in multiple cavefish populations. The inactivation of cbsa affects eye development by increasing the transsulfuration intermediate homocysteine and inducing defects in optic vasculature, which result in aneurysms and eye hemorrhages. Our findings suggest that localized modifications in the circulatory system may have contributed to the evolution of vestigial eyes in cavefish.

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Innervation of the lateral line system in the blind cavefish Astyanax mexicanus (Characidae) and comparisons with the eyed surface-dwelling form

Ichthyological Research ◽

10.1007/s10228-015-0458-7 ◽

2015 ◽

Vol 62 (4) ◽

pp. 420-430 ◽

Cited By ~ 5

Author(s):

Keina Sumi ◽

Ryu Asaoka ◽

Masanori Nakae ◽

Kunio Sasaki

Keyword(s):

Lateral Line ◽

Lateral Line System ◽

Line System ◽

Astyanax Mexicanus ◽

Surface Dwelling ◽

Blind Cavefish

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A mutation in monoamine oxidase (MAO) affects the evolution of stress behavior in the blind cavefish Astyanax mexicanus

Journal of Experimental Biology ◽

10.1242/jeb.226092 ◽

2020 ◽

Vol 223 (18) ◽

pp. jeb226092 ◽

Cited By ~ 2

Author(s):

Constance Pierre ◽

Naomie Pradère ◽

Cynthia Froc ◽

Patricia Ornelas-García ◽

Jacques Callebert ◽

...

Keyword(s):

Monoamine Oxidase ◽

Anatomical Variations ◽

Loss Of Function ◽

Partial Loss ◽

Astyanax Mexicanus ◽

Excellent Candidate ◽

Cave Environment ◽

Blind Cave ◽

Blind Cavefish ◽

Subterranean Environment

ABSTRACTThe neurotransmitter serotonin controls a variety of physiological and behavioral processes. In humans, mutations affecting monoamine oxidase (MAO), the serotonin-degrading enzyme, are highly deleterious. Yet, blind cavefish of the species Astyanax mexicanus carry a partial loss-of-function mutation in MAO (P106L) and thrive in their subterranean environment. Here, we established four fish lines, corresponding to the blind cave-dwelling and the sighted river-dwelling morphs of this species, with or without the mutation, in order to decipher the exact contribution of mao P106L in the evolution of cavefish neurobehavioral traits. Unexpectedly, although mao P106L appeared to be an excellent candidate for the genetic determinism of the loss of aggressive and schooling behaviors in cavefish, we demonstrated that it was not the case. Similarly, the anatomical variations in monoaminergic systems observed between cavefish and surface fish brains were independent from mao P106L, and rather due to other, morph-dependent developmental processes. However, we found that mao P106L strongly affected anxiety-like behaviors. Cortisol measurements showed lower basal levels and an increased amplitude of stress response after a change of environment in fish carrying the mutation. Finally, we studied the distribution of the P106L mao allele in wild populations of cave and river A. mexicanus, and discovered that the mutant allele was present – and sometimes fixed – in all populations inhabiting caves of the Sierra de El Abra. The possibility that this partial loss-of-function mao allele evolves under a selective or a neutral regime in the particular cave environment is discussed.

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Evolutionary increases in catecholamine signaling may underlie the emergence of adaptive traits and behaviors in the blind cavefish, Astyanax mexicanus

10.1101/724179 ◽

2019 ◽

Author(s):

Kathryn Gallman ◽

Daihana Rivera ◽

Daphne Soares

Keyword(s):

Olfactory System ◽

Adaptive Traits ◽

Astyanax Mexicanus ◽

Catecholaminergic Neurons ◽

Defensive Responses ◽

Evolutionary Changes ◽

Blind Cave ◽

Food Seeking ◽

Blind Cavefish ◽

The Brain

AbstractEvolutionary changes in catecholamine neurotransmitters such as dopamine and noradrenaline can lead to habitat specific behaviors. We used tyrosine hydroxylase, a conserved precursor to the biosynthesis of dopamine and noradrenaline, to compare catecholaminergic neurons in the brain of a species undergoing allopatric speciation. The teleost fish Astyanax mexicanus is extant in two readily available forms, an ancestral river dwelling form (surface) and various derived blind cave forms (cavefish). Adaptation to nutrient poor cave life without predation has led to marked differences in the behavior of this species. The cavefish has lost defensive responses, such as stimulus aversion, found in the ancestral surface fish and instead displays enhanced food seeking behaviors. This is reflected by an increase in catecholamine immunoreactivity in the cavefish brain in regions associated with non-visual sensory perception, motor control pathways, attention, and endocrine release. These neuroanatomical regions include the olfactory system, the basal telencephalon, the preoptic nuclei, the posterior tuberculum, caudal hypothalamus, and isthmus. These results indicate that the evolutionary shift from aversive defensive responses to attractive exploratory behaviors was driven by increases in the size and/or quantity of catecholaminergic neurons in the cavefish brain.

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Evolution of acoustic communication in blind cavefish

Nature Communications ◽

10.1038/s41467-019-12078-9 ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 11

Author(s):

Carole Hyacinthe ◽

Joël Attia ◽

Sylvie Rétaux

Keyword(s):

Environmental Change ◽

Acoustic Communication ◽

Sound Production ◽

Social Contexts ◽

Behavioral Changes ◽

Astyanax Mexicanus ◽

The Social ◽

In The Wild ◽

Blind Cave ◽

Blind Cavefish

Abstract Acoustic communication allows the exchange of information within specific contexts and during specific behaviors. The blind, cave-adapted and the sighted, river-dwelling morphs of the species Astyanax mexicanus have evolved in markedly different environments. During their evolution in darkness, cavefish underwent a series of morphological, physiological and behavioral changes, allowing the study of adaptation to drastic environmental change. Here we discover that Astyanax is a sonic species, in the laboratory and in the wild, with sound production depending on the social contexts and the type of morph. We characterize one sound, the “Sharp Click”, as a visually-triggered sound produced by dominant surface fish during agonistic behaviors and as a chemosensory-, food odor-triggered sound produced by cavefish during foraging. Sharp Clicks also elicit different reactions in the two morphs in play-back experiments. Our results demonstrate that acoustic communication does exist and has evolved in cavefish, accompanying the evolution of its behaviors.

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Regressive Evolution of Pigmentation in the Cavefish Astyanax

Israel Journal of Ecology and Evolution ◽

10.1560/ijee_52_3-4_405 ◽

2006 ◽

Vol 52 (3-4) ◽

pp. 405-422 ◽

Cited By ~ 9

Author(s):

William R. Jeffery

Keyword(s):

Neural Crest ◽

Single Gene ◽

Pigment Cells ◽

Loss Of Function ◽

Coding Region ◽

Protein Coding ◽

Regressive Evolution ◽

Astyanax Mexicanus ◽

Key Enzyme ◽

Surface Dwelling

Many cave animals are colorless due to loss of pigment cells. Here, we review recent progress on how and why pigmentation has disappeared in Astyanax mexicanus, a single teleost species with conspecific surface-dwelling (surface fish) and many different cave-dwelling (cavefish) forms. During surface fish development, migratory neural crest cells form three types of pigment cells: silver iridophores, orange xanthophores, and black melanophores. Cavefish have eliminated or substantially reduced their complement of melanophores and exhibit albinism, loss of the capacity to synthesize melanin. Cell tracing, immunolocalization, and neural tube explant cultures show that cavefish have retained a colorless pre-melanophore (melanoblast) lineage derived from the neural crest. Thus, the cavefish neural crest produces melanoblasts that migrate normally but are blocked in differentiation and show defective melanogenesis. Cavefish melanoblasts can convert exogenous L-DOPA into melanin and therefore have active tyrosinase, the key enzyme in melanogenesis. In contrast, cavefish melanoblasts are unable to convert L-tyrosine to L-DOPA (and melanin), although this reaction is also catalyzed by tyrosinase. Thus, cavefish are tyrosinase-positive albinos that have a deficiency in L-tyrosine transport or utilization within the melanosome, the organelle in which melanin is synthesized. At least five different types of Astyanax cavefish show the same defect in melanogenesis. Genetic analysis shows that cavefish albinism is caused by loss of function mutations in a single gene, p/oca2, which encodes a large protein that probably spans the melanosome membrane. Different deletions in the p/oca2 protein-coding region are responsible for loss of function in at least two different cavefish populations, suggesting that albinism evolved by convergence. Based on current understanding of the genetic basis of albinism, we discuss potential mechanisms for regressive evolution of cavefish pigmentation.

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A mutation in monoamine oxidase (MAO) affects the evolution of stress behavior in the blind cavefish Astyanax mexicanus

10.1101/2020.04.09.033266 ◽

2020 ◽

Cited By ~ 1

Author(s):

Constance Pierre ◽

Naomie Pradère ◽

Cynthia Froc ◽

Patricia Ornelas-García ◽

Jacques Callebert ◽

...

Keyword(s):

Monoamine Oxidase ◽

Anatomical Variations ◽

Loss Of Function ◽

Partial Loss ◽

Astyanax Mexicanus ◽

Behavioral Traits ◽

Cave Environment ◽

Blind Cave ◽

Blind Cavefish ◽

Subterranean Environment

AbstractThe neurotransmitter serotonin controls a great variety of physiological and behavioral processes. In humans, mutations affecting the monoamine oxidase or MAO, the serotonin-degrading enzyme, are highly deleterious. Yet, blind cavefish of the species A. mexicanus carry a partial loss-of-function mutation in MAO (P106L) and seem to thrive in their subterranean environment. Here, we established 4 fish lines, corresponding to the blind cave-dwelling and the sighted river-dwelling morphs of this species, with or without the mutation, in order to decipher the exact contribution of mao P106L in the evolution of cavefish neuro-behavioral traits. Unexpectedly, although mao P106L appeared as an excellent candidate for the genetic determinism of the loss of aggressive and schooling behaviors in cavefish, we demonstrated that it was not the case. Similarly, the anatomical variations in monoaminergic systems observed between cavefish and surface fish brains were independent from mao P106L, and rather due other, morph-dependent developmental processes. On the other hand, we found that mao P106L strongly affected anxiety-like behaviors. Cortisol measurements showed lower basal levels and an increased amplitude of stress response after a change of environment in fish carrying the mutation. Finally, we studied the distribution of the P106L mao allele in wild populations of cave and river A. mexicanus, and discovered that the mutant allele was present - and sometimes fixed - in all populations inhabiting caves of the Sierra de El Abra. The possibility that this partial loss-of-function mao allele evolves under a selective or a genetic drift regime in the particular cave environment is discussed.

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