Convergence on reduced stress behavior in the Mexican blind cavefish

Chin, Jacqueline S. R.; Gassant, Claude E.; Amaral, Paloma M.; Lloyd, Evan; Stahl, Bethany A.; Jaggard, James B.; Keene, Alex C.; Duboué, Erik R.

doi:10.1016/j.ydbio.2018.05.009

Cited by 46 publications

(71 citation statements)

References 85 publications

(112 reference statements)

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“…In addition, understanding stress and its effects in the long term on growth, cardiovasculature, metabolism, and musculature is important in aquaculture (Sadoul and Vijayan, 2016). We have previously demonstrated that adult A. mexicanus have diminished stress responses (Chin et al, 2018), and these data extend this to larval forms. We expect that future work using powerful approaches unique to larvae, such as whole brain functional imaging and tracing of neural circuits that modulate stress, together with genotype-phenotype associations between genes and stress responses will shed significant light into genetic pre-disposition to stress disorders.…”

Section: Future Directionssupporting

confidence: 70%

Analysis of stress responses inAstyanaxlarvae reveals heterogeneity among different populations

Chin

Loomis

Albert

et al. 2020

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Research Highlight:• Cavefish populations of A. mexicanus have reduced stress relative to surface conspecific at larval stages • We show that a glucocorticoid receptor, a negative regulator of the neuroendocrine stress axis, is upregulated in stress-resistant cavefish • There exists much ontological heterogeneity between different cavefish populations. AbstractStress responses are conserved physiological and behavioral outcomes as a result of facing potentially harmful stimuli, yet in pathological states, stress becomes debilitating. Stress responses vary considerably throughout the animal kingdom, but how these responses are shaped evolutionarily is unknown. The Mexican cavefish has emerged as a powerful system for examining genetic principles underlying behavioral evolution. Here, we demonstrate that cave Astyanax have reduced behavioral and physiological measures of stress when examined at larval stages. We also find increased expression of the glucocorticoid receptor, a repressible element of the neuroendocrine stress pathway. Additionally, we examine stress in three different cave populations, and find that some, but not all, show reduced stress measures. Together, these results reveal a mechanistic system by which cave-dwelling fish reduced stress, presumably to compensate for a predator poor environment.

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Section: Future Directionssupporting

confidence: 70%

Analysis of stress responses inAstyanaxlarvae reveals heterogeneity among different populations

Chin

Loomis

Albert

et al. 2020

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“…The volume of the pineal gland, a region associated with secretion of sleep-promoting melatonin, was significantly reduced in all three populations of cavefish (Fig 1K, Fig S4), raising the possibility that these changes are associated with loss of sleep and circadian regulation of activity in cavefish [39, 43]. In addition, volume of the habenular nuclei that regulate stress were reduced in all three cavefish populations, demonstrating a potential neuroanatomical mechanism underlying blunted response to stress in cavefish (Fig 1K, Fig S4) [44]. While many of the evolved changes in brain anatomy we identified were shared between cave populations, we also observed differences between individuals from different cave populations.…”

Section: Resultsmentioning

confidence: 99%

“…Therefore, to directly compare brain activity in sleeping surface fish and cavefish, we pharmacologically induced sleep in all populations of cavefish. Previously, we showed that moderate concentrations of β-adrenergic antagonist propranolol and HCRT receptor inhibitor EMPA restore sleep to Pachón cavefish without affecting sleep in surface fish, suggesting enhanced sensitivity to inhibitors of β-adrenergic and HCRT signaling [44, 51]. The effects of these agents on neural activity and in additional cave populations is unknown.…”

Section: Resultsmentioning

confidence: 99%

Cavefish brain atlases reveal functional and anatomical convergence across independently evolved populations

Jaggard

Lloyd

Yuiska

et al. 2019

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18Environmental perturbation can drive the evolution of behavior and associated changes in 19 brain structure and function. The generation of computationally-derived whole-brain 20 atlases have provided insight into neural connectivity associated with behavior in many 21 model systems. However, these approaches have not been used to study the evolution of 22 brain structure in vertebrates. The Mexican tetra, A. mexicanus, comprises river-dwelling 23 surface fish and multiple independently evolved populations of blind cavefish, providing a 24 unique opportunity to identify neuroanatomical and functional differences associated with 25 behavioral evolution. We employed intact brain imaging and image registration on 684 26 larval fish to generate neuroanatomical atlases of surface fish and three different cave 27 populations. Analyses of brain regions and neural circuits associated with behavioral 28 regulation identified convergence on hypothalamic expansion, as well as changes in 29 transmitter systems including elevated numbers of catecholamine and hypocretin neurons 30 in cavefish populations. To define evolutionarily-derived changes in brain function, we 31 performed whole brain activity mapping associated with feeding and sleep. Feeding 32 evoked neural activity in different sensory processing centers in surface and cavefish. We 33 also identified multiple brain regions with sleep-associated activity across all four 34 populations, including the rostral zone of the hypothalamus and tegmentum. Together, 35 these atlases represent the first comparative brain-wide study of intraspecies variation in 36 a vertebrate model, and provide a resource for studying the neural basis underlying 37 behavioral evolution. 39 Introduction 40Brain function and behavior are influenced by evolutionary history and ecological 41 environment [1,2]. Robust differences in gross anatomy, neural connectivity, and gene 42 expression have been associated with the evolution of behavaior in closely related species 43 [3][4][5]. Most studies employing comparative anatomy have focused on a small number of 44 brain regions, limiting insight into large-scale changes in brain structure and function. The 45 recent generation of computationally-derived whole brain atlases and connectomes has 46 provided an increased understanding of how neural circuits function [6][7][8]. These 47 resources have largely been limited to a select number of genetically accessible model 48 organisms, and have not been applied to a diverse set of models commonly used to study 49 trait evolution. The generation of whole-brain atlases in closely related species, or even 50 independent populations of the same species has potential to provide insight into the 51 principles governing the evolution of brain structure and neural circuit connectivity 52 associated with behavioral diversity. 54The Mexican tetra, Astyanax mexicanus, comprises eyed surface fish that inhabit rivers 55 throughout Mexico and at least 29 populations of cavefish in the San Luis Potosi region of 56 north...

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“…However, the presence or absence of other fish can also affect a fish's overall swimming behavior, whether or not it is near another fish. For example, surface fish exhibit a stress response to isolation which makes them seek the bottom of their tank [6]. Although depth is not significant in our shallow tank, changes in the mean speed or turning statistics are.…”

Section: Group Size Affects Speed Regulation and The Nature Of Turnsmentioning

confidence: 90%

Kinematic analysis deconstructs the evolved loss of schooling behavior in cavefish

Patch

Paz

Holt

et al. 2020

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Fish display a remarkable diversity in social behavior that ranges from highly social to largely solitary. While social behaviors are critical for survival and under stringent selection, surprisingly little is understood about how environmental pressures shape differences in collective behavior. The Mexican tetra, Astyanax mexicanus, is a model for studying the evolution of social behaviors. These fish exist as multiple blind cave populations in the Sierra de El Abra and extant ancestral surface fish populations that inhabit rivers and lakes throughout Mexico. Cavefish populations have converged upon many different morphological, physiological, and behavioral traits including reduced social behavior. Dynamically, groups of surface fish maintain close proximity, persistently shoaling or schooling, while their dark-cave-evolved counterparts swim independently, surveying walls and floors for food. To more carefully study evolved changes in individual and social behavior, we track free-swimming individuals in a large circular tank, varying group size and fish type. We find that group size and isolation impact swimming dynamics of cave and surface fish very differently, underscoring the mechanics of their distinct social dynamics. Highly-social surface fish respond to isolation by becoming more inactive while cavefish swimming becomes less persistent in the presence of others. In stark contrast, we find that cavefish actively evade each other upon encounter and respond to increased social density by slowing down. For abstract consideration of evasive interactions, we consider emergent effects of local evasive interactions by constructing and simulating a minimal active matter model and show how this behavior can generate group dynamics that may uniquely benefit exploration of confined environments in the absence of long-range sensory cues provided by vision. These findings reveal the convergent evolution of avoidance behavior in cavefish and support the use of A. mexicanus as a model for studying the evolution of social behavior.

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Convergence on reduced stress behavior in the Mexican blind cavefish

Cited by 46 publications

References 85 publications

Analysis of stress responses inAstyanaxlarvae reveals heterogeneity among different populations

Analysis of stress responses inAstyanaxlarvae reveals heterogeneity among different populations

Cavefish brain atlases reveal functional and anatomical convergence across independently evolved populations

Kinematic analysis deconstructs the evolved loss of schooling behavior in cavefish

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