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

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

10.1101/805804 ◽

2019 ◽

Author(s):

Li Ma ◽

Aniket V. Gore ◽

Daniel Castranova ◽

Janet Shi ◽

Mandy Ng ◽

...

Keyword(s):

Oxygen Deficiency ◽

Circulatory System ◽

Astyanax Mexicanus ◽

Transsulfuration Pathway ◽

Key Enzyme ◽

Surface Dwelling ◽

Blind Cave ◽

Different Populations ◽

Key Indicators ◽

Blind Cavefish

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 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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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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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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Faculty Opinions recommendation of The population genomics of repeated evolution in the blind cavefish Astyanax mexicanus.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718063419.793481845 ◽

2013 ◽

Author(s):

Ary Hoffmann

Keyword(s):

Population Genomics ◽

Astyanax Mexicanus ◽

Repeated Evolution ◽

Blind Cavefish

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Catecholaminergic neurons in the brain-stem and sleep apnea in SIDS victims

Pathophysiology ◽

10.1016/j.pathophys.2004.01.006 ◽

2004 ◽

Vol 10 (3-4) ◽

pp. 173-178 ◽

Cited By ~ 1

Author(s):

Toshiko Sawaguchi ◽

Yuri Ozawa ◽

Patricia Franco ◽

Hazim Kadhim ◽

Jose Groswasser ◽

...

Keyword(s):

Sleep Apnea ◽

Brain Stem ◽

Catecholaminergic Neurons ◽

The Brain

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The brain of the tree pangolin (Manis tricuspis ). II. The olfactory system

The Journal of Comparative Neurology ◽

10.1002/cne.24510 ◽

2018 ◽

Vol 526 (16) ◽

pp. 2548-2569 ◽

Cited By ~ 6

Author(s):

Aminu Imam ◽

Adhil Bhagwandin ◽

Moyosore S. Ajao ◽

Muhammed A. Spocter ◽

Amadi O. Ihunwo ◽

...

Keyword(s):

Olfactory System ◽

The Brain

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Long-term modulation of tyrosine hydroxylase activity and expression by endothelin-1 and -3 in the rat anterior and posterior hypothalamus

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.00555.2007 ◽

2008 ◽

Vol 294 (3) ◽

pp. R905-R914 ◽

Cited By ~ 12

Author(s):

Guadalupe Perfume ◽

Sabrina L. Nabhen ◽

Karla Riquelme Barrera ◽

María G. Otero ◽

Liliana G. Bianciotti ◽

...

Keyword(s):

Tyrosine Hydroxylase ◽

Cardiovascular Effects ◽

Receptor Activation ◽

Catecholaminergic Neurons ◽

Endothelin System ◽

Catecholaminergic Transmission ◽

Underlying Mechanisms ◽

G Protein Coupled ◽

The Brain

Brain catecholamines are involved in the regulation of biological functions, including cardiovascular activity. The hypothalamus presents areas with high density of catecholaminergic neurons and the endothelin system. Two hypothalamic regions intimately related with the cardiovascular control are distinguished: the anterior (AHR) and posterior (PHR) hypothalamus, considered to be sympathoinhibitory and sympathoexcitatory regions, respectively. We previously reported that endothelins (ETs) are involved in the short-term tyrosine hydroxylase (TH) regulation in both the AHR and PHR. TH is crucial for catecholaminergic transmission and is tightly regulated by well-characterized mechanisms. In the present study, we sought to establish the effects and underlying mechanisms of ET-1 and ET-3 on TH long-term modulation. Results showed that in the AHR, ETs decreased TH activity through ETB receptor activation coupled to the nitric oxide, phosphoinositide, and CaMK-II pathways. They also reduced total TH level and TH phosphorylated forms (Ser 19 and 40). Conversely, in the PHR, ETs increased TH activity through a G protein-coupled receptor, likely an atypical ET receptor or the ETC receptor, which stimulated the phosphoinositide and adenylyl cyclase pathways, as well as CaMK-II. ETs also increased total TH level and the Ser 19, 31, and 40 phosphorylated sites of the enzyme. These findings support that ETs are involved in the long-term regulation of TH activity, leading to reduced sympathoinhibition in the AHR and increased sympathoexcitation in the PHR. Present and previous studies may partially explain the cardiovascular effects produced by ETs when applied to the brain.

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The cell biology of smell

The Journal of Cell Biology ◽

10.1083/jcb.201008163 ◽

2010 ◽

Vol 191 (3) ◽

pp. 443-452 ◽

Cited By ~ 90

Author(s):

Shannon DeMaria ◽

John Ngai

Keyword(s):

Olfactory System ◽

Cell Biology ◽

Odorant Receptor ◽

Large Family ◽

G Protein Coupled Receptors ◽

Odorant Receptors ◽

Chemical Structures ◽

Wide Range ◽

G Protein Coupled ◽

The Brain

The olfactory system detects and discriminates myriad chemical structures across a wide range of concentrations. To meet this task, the system utilizes a large family of G protein–coupled receptors—the odorant receptors—which are the chemical sensors underlying the perception of smell. Interestingly, the odorant receptors are also involved in a number of developmental decisions, including the regulation of their own expression and the patterning of the olfactory sensory neurons' synaptic connections in the brain. This review will focus on the diverse roles of the odorant receptor in the function and development of the olfactory system.

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