Biology subjects

Duboue, E. R.

Publications and source records attributed to Duboue, E. R..

At least 19 recordsLinked to original sources

bioRxiv2026

A comparative brain atlas of Mexican cavefish identifies naturally-occurring changes in cellular composition and gene expression

Understanding how naturally occurring genetic variation shapes human health and disease is critical for improving diagnosis and treatment strategies. The Mexican cavefish, Astyanax mexicanus, represents a powerful system for evolutionary medicine, enabling investigation of naturally evolved mechanisms of resilience to disease-related traits including diabetes, obesity, insomnia, and eye loss. Larval A. mexicanus, like zebrafish, are transparent, allowing whole-brain imaging, circuit mapping, and the generation of computationally derived atlases that precisely quantify neuroanatomical differences between surface and cave populations. Developing a molecular map of brain cell types provides a foundation for identifying evolved differences in neural circuits and physiology. Here, we present a single-cell atlas of the larval cavefish brain that reveals widespread divergence in the abundance and molecular signatures of neurons and glia. Our cell type map validates known neuroanatomical differences, including a reduction of the optic tectum and expansion of the pineal gland in cavefish. We uncover substantial changes in multiple glial cell classes that are linked to neural regulation of behavior, including microglia. Analysis of differential gene expression between surface and cavefish microglia revealed enhanced genes associated with synaptic pruning and clearance of neural debris, suggesting cavefish increased microglia activity to shape brain development. We also analyzed cell types that did not classify as canonical neurons or glia and identified notable divergence in transcriptomes and cell composition, including reduced meningeal fibroblasts in cavefish and substantial transcriptional changes related to phototransduction in non-visual photoreceptors within the pineal gland. Together, these findings provide a comprehensive atlas of cell type-specific gene expression differences between A. mexicanus surface and cavefish, establishing a platform for dissecting the molecular and cellular basis of evolved disease resilience in cavefish

evolutionary biology↗

bioRxiv2026

Evolved differences in microglial cell biology between surface and cave populations of Astyanax mexicanus

Microglia govern multiple aspects of brain architecture and function by eliminating dying cells, stimulating neurogenesis, refining neural connections, and orchestrating immune responses. The Mexican tetra, Astyanax mexicanus, is a powerful model system for investigating the evolution of brain function, yet microglia have not been investigated in this system. A. mexicanus exists as surface-dwelling and cave morphotypes with prominent behavioral and physiological differences. Notably, these evolved behavioral and physiological changes in cavefish, including diminished immune response, sleep, circadian rhythms, and sensory processing, are directly linked to known microglial functions. These observations suggest that evolved differences in microglia may shape brain circuitry adaptations in cavefish. Here we develop an experimental toolbox to examine microglial specification, dynamics, and function in A. mexicanus to perform comparative analysis of microglial cell biology between the surface and cave morphotypes. We find that the cave populations show increased numbers of microglia over developmental time relative to their surface counterparts. Microglia in Astyanax rapidly expand in response to inflammatory cues, distinct from microglial responses in the related teleost, zebrafish. Furthermore, lysosomal compartments of microglia in the cave populations exhibit increased enhanced proteolytic activity and reduced pH relative to surface morphotypes. Together, our observations reveal evolved differences in microglial cell biology between surface and cave populations of A. mexicanus and provide a framework to uncover novel neuroimmune mechanisms underlying the remarkable adaptations of A. mexicanus.

evolutionary biology↗

bioRxiv2025

CRISPR screening reveals genetic regulators associated with the evolution of eye degeneration

Determining the genetic factors contributing to trait evolution is critical for understanding how and why traits evolve; however, establishing which genes underlie the evolution of complex traits remains challenging. The freshwater fish Astyanax mexicanus, a species that includes blind, cave-dwelling and eyed, surface-dwelling fish, is a powerful model for evolutionary genetics. While genetic mapping studies in this species previously identified genomic regions associated with cave-derived traits, few causative genes and genetic changes have been identified. Here, we develop methods to identify and rapidly functionally assess candidate genes in A. mexicanus, focusing on a defining trait of cave animals, eye loss. Candidate genes were identified based on whether they fell within an eye-related quantitative trait locus, were differentially expressed between surface and cave eyes, and showed evidence of positive selection in cavefish. Single-nucleus RNA-sequencing revealed that these candidate genes were expressed in multiple cell types during development, including those in different tissues of the eye. CRISPR-Cas9-based mutagenesis demonstrated that disruption of nine of these candidate genes in surface fish resulted in altered eye size. Perturbation of one of these genes, fibulin-7 (fbln7), revealed changes in eye size across multiple stages of eye development. Together, this work identified multiple genes associated with the evolution of eye degeneration in A. mexicanus. Further, this study represents a roadmap for rapid identification and functional assessment of candidate genes implicated in the evolution of traits in cavefish that can be applied to other evolutionary genetic models.

genetics↗

bioRxiv2025

Analysis of multi-trait evolution across independently evolved cavefish populations reveals shared and independent evolution of suites of cave-associated traits

Environmental perturbations often lead to the evolution of multiple traits. Determining whether shared genetic factors underlie multi-trait evolution is a central question in evolutionary biology. In the Mexican tetra, Astyanax mexicanus, cave-dwelling populations have repeatedly evolved multiple traits. The repeated evolution of these traits, paired the robust environmental differences between the surface and cave habitats, provide an opportunity to investigate the genetic basis of multi-trait evolution. Here, we investigate the extent to which shared genetic mechanisms underlie the repeated evolution of multiple traits in cavefish. Across cave populations, we find evidence for shared and distinct genetic mechanisms contributing to the evolution of individual traits. Further, multiple traits covary in cave-surface F2 hybrids and many of the same trait correlations are found across independently evolved cave populations. Finally, we assessed traits that differ between pigmented and albino F2 fish in surface fish with mutations in the albinism gene oculocutaneous albinism 2 (oca2). This revealed that mutations in oca2 reduce bottom-dwelling behavior in A. mexicanus. Together, these findings suggest that multi-trait evolution occurs repeatedly through shared genetic factors across A. mexicanus cave populations. These results are consistent with pleiotropy or linkage playing a large role in multi-trait evolution in this species.

evolutionary biology↗

bioRxiv2025

Automated behavioral profiling using neural networks reveals differences in stress-like behavior between cave and surface-dwelling Astyanax mexicanus

Behavioral stress responses allow animals to quickly adapt to local environments and are critical for survival. Stress responses provide an ideal model for investigating the evolution of complex behaviors due to their conservation across species, critical role in survival, and integration of behavioral and physiological components. The Mexican cavefish (Astyanax mexicanus) has evolved dramatically different stress responses compared to river-dwelling surface fish morphs, providing a model to investigate the neural and evolutionary basis of stress-like responses. Surface morphs inhabit predator-rich environments whereas cave-dwelling morphs occupy predator-free habitats. While these key ecological variables may underlie differences in stress responses, the complexity of the behavioral differences has not been thoroughly examined. By leveraging automated pose-tracking and machine learning tools, we quantified a range of behaviors associated with stress, including freezing, bottom-dwelling, and hyperactivity, during a novel tank assay. Surface fish exhibited heightened stress responses characterized by prolonged bottom-dwelling and frequent freezing, while cavefish demonstrated reduced stress behaviors, marked by greater exploration and minimal freezing. Analysis of F2 hybrids revealed that a subset of behaviors, freezing and bottom-dwelling, co-segregated, suggesting shared genetic or physiological underpinnings. Our findings illustrate the power of computational tools for high-throughput behavioral phenotyping, enabling precise quantification of complex traits and revealing the genetic and ecological factors driving their evolution. This study provides a framework for understanding how integrated behavioral and physiological traits evolve, offering broader insights into the mechanisms underlying the diversification of animal behavior in natural systems.

evolutionary biology↗

bioRxiv2024

The rx3 gene contributes to the evolution of eye loss in the cavefish Astyanax mexicanus

Uncovering mechanisms by which sensory systems evolve is critical for understanding how organisms adapt to a novel environment. Astyanax mexicanus is a species of fish with populations of surface fish that inhabit rivers and streams and cavefish that have adapted to life within caves. Cavefish have evolved sensory system changes relative to their surface fish counterparts, providing an opportunity to investigate mechanisms underlying sensory system evolution. Here, we report the role of the gene retinal homeobox 3 (rx3) in cavefish eye evolution. We generated surface fish with putative loss-of-function mutations in the rx3 gene using CRISPR-Cas9 to determine the role of this gene in eye development in this species. These rx3 mutant surface fish fail to develop eyes, demonstrating that rx3 is required for surface fish eye development. Further, rx3 mutant surface fish exhibit altered behaviors relative to wild-type surface fish, suggesting that the loss of eyes impacts sensory-dependent behaviors. Finally, eye development is altered in cave-surface hybrid fish that inherit the mutant allele of rx3 from surface fish relative to siblings that inherit a wild-type surface fish rx3 allele, suggesting that cis-regulatory variation at the rx3 locus contributes to eye size evolution in cavefish. Together, these findings demonstrate that, as in other species, rx3 is required for eye development in A. mexicanus. Moreover, they suggest that variation at the rx3 locus plays a role in the evolved reduction of eye size in cavefish, shedding light on the genetic mechanisms underlying sensory system evolution in response to extreme environmental changes.

evolutionary biology↗

bioRxiv2024

Evolution of a central dopamine circuit underlies adaptation of light-evoked sensorimotor response in the blind cavefish, Astyanax mexicanus.

Adaptive behaviors emerge in novel environments through functional changes in neural circuits. While relationships between circuit function and behavior have been well studied, how evolution shapes those circuits and leads to behavioral adpation is poorly understood. The Mexican cavefish, Astyanax mexicanus, provides a unique genetically amendable model system, equipped with above ground eyed surface fish and multiple evolutionarily divergent populations of blind cavefish that have evolved in complete darkness. These differences in environment and vision provide an opprotunity to examine how a neural circuit is functionally influenced by the presence of light. Here, we examine differences in the detection, and behavioral response induced by non visual light reception. Both populations exhibit photokinetic behavior, with surface fish becoming hyperactive following sudden darkness and cavefish becoming hyperactive following sudden illumination. To define these photokinetic neural circuits, we integrated whole brain functional imaging with our Astyanax brain atlas for surface and cavefish responding to light changes. We identified the caudal posterior tuberculum as the central modulator for both light or dark stimulated photokinesis. To unconver how spatiotemporal neuronal activity differed between surface fish and cavefish, we used stable pan-neuronal GCaMP Astyanax transgenics to show that a subpopulation of darkness sensitve neurons in surface fish are now light senstive in cavefish. Further functional analysis revealed that this integrative switch is dependent on dopmane signaling, suggesting a key role for dopamine and a highly conserved dopamine circuit in modulating the evolution of a circuit driving an essential behavior. Together, these data shed light into how neural circuits evolved to adapte to novel settings, and reveal the power of Astyanax as a model to elucidate mechanistic ingiths underlying sensory adaptation. O_FIG O_LINKSMALLFIG WIDTH=173 HEIGHT=200 SRC="FIGDIR/small/605141v1_ufig1.gif" ALT="Figure 1"> View larger version (34K): org.highwire.dtl.DTLVardef@145efeforg.highwire.dtl.DTLVardef@8b41e6org.highwire.dtl.DTLVardef@936979org.highwire.dtl.DTLVardef@1f18c5b_HPS_FORMAT_FIGEXP M_FIG C_FIG

evolutionary biology↗

bioRxiv2024

Postprandial sleep in short-sleeping Mexican cavefish

Interaction between sleep and feeding behaviors are critical for adaptive fitness. Diverse species suppress sleep when food is scarce to increase the time spent foraging. Post-prandial sleep, an increase in sleep time following a feeding event, has been documented in vertebrate and invertebrate animals. While interactions between sleep and feeding appear to be highly conserved, the evolution of postprandial sleep in response to changes in food availability remains poorly understood. Multiple populations of the Mexican cavefish, Astyanax mexicanus, have independently evolved sleep loss and increased food consumption compared to surface-dwelling fish of the same species, providing the opportunity to investigate the evolution of interactions between sleep and feeding. Here, we investigate effects of feeding on sleep in larval and adult surface fish, and two parallelly evolved cave populations of A. mexicanus. Larval surface and cave populations of A. mexicanus increase sleep immediately following a meal, providing the first evidence of postprandial sleep in a fish model. The amount of sleep was not correlated to meal size and occurred independently of feeding time. In contrast to larvae, postprandial sleep was not detected in adult surface or cavefish, that can survive for months without food. Together, these findings reveal that postprandial sleep is present in multiple short-sleeping populations of cavefish, suggesting sleep-feeding interactions are retained despite the evolution of sleep loss. These findings raise the possibility that postprandial sleep is critical for energy conservation and survival in larvae that are highly sensitive to food deprivation.

neuroscience↗

bioRxiv2024

Elevated DNA Damage without signs of aging in the short-sleeping Mexican Cavefish

Dysregulation of sleep has widespread health consequences and represents an enormous health burden. Short-sleeping individuals are predisposed to the effects of neurodegeneration, suggesting a critical role for sleep in the maintenance of neuronal health. While the effects of sleep on cellular function are not completely understood, growing evidence has identified an association between sleep loss and DNA damage, raising the possibility that sleep facilitates efficient DNA repair. The Mexican tetra fish, Astyanax mexicanus provides a model to investigate the evolutionary basis for changes in sleep and the consequences of sleep loss. Multiple cave-adapted populations of these fish have evolved to sleep for substantially less time compared to surface populations of the same species without identifiable impacts on healthspan or longevity. To investigate whether the evolved sleep loss is associated with DNA damage and cellular stress, we compared the DNA Damage Response (DDR) and oxidative stress levels between A. mexicanus populations. We measured markers of chronic sleep loss and discovered elevated levels of the DNA damage marker {gamma}H2AX in the brain, and increased oxidative stress in the gut of cavefish, consistent with chronic sleep deprivation. Notably, we found that acute UV-induced DNA damage elicited an increase in sleep in surface fish but not in cavefish. On a transcriptional level, only the surface fish activated the photoreactivation repair pathway following UV damage. These findings suggest a reduction of the DDR in cavefish compared to surface fish that coincides with elevated DNA damage in cavefish. To examine DDR pathways at a cellular level, we created an embryonic fibroblast cell line from the two populations of A. mexicanus. We observed that both the DDR and DNA repair were diminished in the cavefish cells, corroborating the in vivo findings and suggesting that the acute response to DNA damage is lost in cavefish. To investigate the long-term impact of these changes, we compared the transcriptome in the brain and gut of aged surface fish and cavefish. Strikingly, many genes that are differentially expressed between young and old surface fish do not transcriptionally vary by age in cavefish. Taken together, these findings suggest that cavefish have developed resilience to sleep loss, despite possessing cellular hallmarks of chronic sleep deprivation.

neuroscience↗

bioRxiv2023

Changes in local interaction rules during ontogeny underlie the evolution of collective behavior

Collective motion emerges from individual interactions which produce groupwide patterns in behavior. While adaptive changes to collective motion are observed across animal species, how local interactions change when these collective behaviors evolve is poorly understood. Here, we use the Mexican tetra, A. mexicanus, which exists as a schooling surface form and a non-schooling cave form, to study differences in how fish alter their swimming in response to neighbors across ontogeny and between evolutionarily diverged populations. We find that surface fish undergo a transition to schooling during development that occurs through increases in inter-individual alignment and attraction mediated by changes in the way fish modulate speed and turning relative to neighbors. Cavefish, which have evolved loss of schooling, exhibit neither of these schooling-promoting interactions at any stage of development. These results reveal how evolution alters local interaction rules to produce striking differences in collective behavior.

evolutionary biology↗

bioRxiv2023

Thalamic neurons drive distinct forms of motor asymmetry that are conserved in teleost and dependent on visual evolution

Brain laterality is a prominent feature in Bilateria, where neural functions are favored in a single brain hemisphere. These hemispheric specializations are thought to improve behavioral performance and are commonly observed as sensory or motor asymmetries, such as handedness in humans. Despite its prevalence, our understanding of the neural and molecular substrates instructing functional lateralization is limited. Moreover, how functional lateralization is selected for or modulated throughout evolution is poorly understood. While comparative approaches offer a powerful tool for addressing this question, a major obstacle has been the lack of a conserved asymmetric behavior in genetically tractable organisms. Previously, we described a robust motor asymmetry in larval zebrafish. Following the loss of illumination, individuals show a persistent turning bias that is associated with search pattern behavior with underlying functional lateralization in the thalamus. This behavior permits a simple yet robust assay that can be used to address fundamental principles underlying lateralization in the brain across taxa. Here, we take a comparative approach and show that motor asymmetry is conserved across diverse larval teleost species, which have diverged over the past 200 million years. Using a combination of transgenic tools, ablation, and enucleation, we show that teleosts exhibit two distinct forms of motor asymmetry, vision-dependent and - independent. These asymmetries are directionally uncorrelated, yet dependent on the same subset of thalamic neurons. Lastly, we leverage Astyanax sighted and blind morphs, which show that fish with evolutionarily derived blindness lack both retinal-dependent and -independent motor asymmetries, while their sighted surface conspecifics retained both forms. Our data implicate that overlapping sensory systems and neuronal substrates drive functional lateralization in a vertebrate brain that are likely targets for selective modulation during evolution.

neuroscience↗

bioRxiv2022

Novel husbandry practices result in rapid rates of growth and sexual maturation without impacting adult behavior in the blind Mexican cavefish.

The development of animal model systems is dependent on the standardization of husbandry protocols that increase fecundity and reduce generation time. The blind Mexican tetra, Astyanax mexicanus, is an emerging genetic vertebrate model for evolution and biomedical research. Surface and cave populations of A. mexicanus have independently evolved, providing a model system for studying the genetic basis of divergent biological traits. While a rapid increase in the use of A. mexicanus has led to the generation of genetic tools including gene-editing and transgenesis, a slow and inconsistent growth rate remains a major limitation to the expanded application of A. mexicanus. The optimization of husbandry protocols that maximizes high-nutrient feed, smaller tank densities and larger tank sizes across development, would facilitate faster growth and expand the use of this model. Here, we describe standardized husbandry practices that optimize growth through a high protein diet, increased feeding, growth sorting of larvae and juveniles, and tank size transitions based on standard length. These changes to husbandry had a significant effect on growth rates and decreased the age of sexual maturity in comparison to our previous protocols. To determine whether our nutritional change and increased feeding impacted behavior, we tested fish in exploration and schooling assays. We found that a change in diet had no effect on the behaviors we tested, suggesting that increased feeding and rapid growth will not impact the natural variation in behavioral traits. Taken together, this standardized husbandry protocol will accelerate the development of A. mexicanus as a genetic model.

evolutionary biology↗

bioRxiv2021

Characterizing the genetic basis of trait evolution in the Mexican cavefish

Evolution in response to a change in ecology often coincides with various morphological, physiological, and behavioral traits. For most organisms little is known about the genetic and functional relationship between evolutionarily derived traits, representing a critical gap in our understanding of adaptation The Mexican tetra, Astyanax mexicanus, consists of largely independent populations of fish that inhabit at least 30 caves in Northeast Mexico, and a surface fish population, that inhabits the rivers of Mexico and Southern Texas. The recent application of molecular genetic approaches combined with behavioral phenotyping have established A. mexicanus as a model for studying the evolution of complex traits. Cave populations of A. mexicanus are interfertile with surface populations and have evolved numerous traits including eye degeneration, insomnia, albinism and enhanced mechanosensory function. The interfertility of different populations from the same species provides a unique opportunity to define the genetic relationship between evolved traits and assess the co-evolution of behavioral and morphological traits with one another. To define the relationships between morphological and behavioral traits, we developed a pipeline to test individual fish for multiple traits. This pipeline confirmed differences in locomotor activity, prey capture, and startle reflex between surface and cavefish populations. To measure the relationship between traits, individual F2 hybrid fish were characterized for locomotor behavior, prey-capture behavior, startle reflex and morphological attributes. Analysis revealed an association between body length and slower escape reflex, suggesting a trade-off between increased size and predator avoidance in cavefish. Overall, there were few associations between individual behavioral traits, or behavioral and morphological traits, suggesting independent genetic changes underlie the evolution of behavioral and morphological traits. Taken together, this approach provides a novel system to identify genes that underlie naturally occurring genetic variation in morphological and behavioral traits.

evolutionary biology↗

bioRxiv2021

Blind cavefish retain functional connectivity in the tectum despite loss of retinal input

Sensory systems display remarkable plasticity and are under strong evolutionary selection. The Mexican cavefish, Astyanax mexicanus, consists of eyed river-dwelling surface populations, and multiple independent cave populations which have converged on eye loss, providing the opportunity to examine the evolution of sensory circuits in response to environmental perturbation. Functional analysis across multiple transgenic populations expressing GCaMP6s showed that functional connectivity of the optic tectum largely did not differ between populations, except for the selective loss of negatively correlated activity within the cavefish tectum, suggesting positively correlated neural activity is resistant to an evolved loss of input from the retina. Further, analysis of surface-cave hybrid fish reveals that changes in the tectum are genetically distinct from those encoding eye-loss. Together, these findings uncover the independent evolution of multiple components of the visual system and establish the use of functional imaging in A. mexicanus to study neural circuit evolution.

neuroscience↗

bioRxiv2021

Long lasting anxiety following early life stress is dependent on glucocorticoid signaling in zebrafish

Chronic adversity in early childhood is associated with increased anxiety and a propensity for substance abuse later in adulthood, yet the effects of early life stress (ELS) on brain development remains poorly understood. The zebrafish, Danio rerio, is a powerful model for studying neurodevelopment and stress. Here, we describe a zebrafish model of ELS and identify a role for glucocorticoid signaling during a critical window in development that leads to long-term changes in brain function. Larval fish subjected to chronic stress in early development exhibited increased anxiety-like behavior and elevated glucocorticoid levels later in life. Increased stress-like behavior was only observed when fish were subjected to ELS within a precise time window in early development, revealing a temporal critical window of sensitivity. Moreover, enhanced anxiety-like behavior only emerges after two months post-ELS, revealing a developmentally specified delay in the effects of ELS. ELS leads to increased levels of baseline cortisol, and resulted in a dysregulation of cortisol receptors, suggesting long-term effects on cortisol signaling. Together, these findings reveal a critical window for ELS to affect developmental reprogramming of the glucocorticoid receptor pathway, resulting in chronic elevated stress.

neuroscience↗

bioRxiv2020

Pleiotropic function of the oca2 gene underlies the evolution of sleep loss and albinism in cavefish

Adaptation to novel environments often involves the evolution of multiple morphological, physiological and behavioral traits. One striking example of multi-trait evolution is the suite of traits that has evolved repeatedly in cave animals, including regression of eyes, loss of pigmentation, and enhancement of non-visual sensory systems [1,3]. The Mexican tetra, Astyanax mexicanus, consists of fish that inhabit at least 30 caves in Northeast Mexico and ancestral-like surface fish which inhabit the rivers of Mexico and Southern Texas [6]. Cave A. mexicanus are interfertile with surface fish and have evolved a number of traits that are common to cave animals throughout the world, including albinism, eye loss, and alterations to behavior [8-10]. To define relationships between different cave-evolved traits, we phenotyped 208 surface-cave F2 hybrid fish for numerous morphological and behavioral traits. We found significant differences in sleep between pigmented and albino hybrid fish, raising the possibility that these traits share a genetic basis. In cavefish and many other species, mutations in oculocutaneous albinism 2 (oca2) cause albinism [11-15]. Surface fish with CRISPR-induced mutations in oca2 displayed both albinism and reduced sleep. Further, this mutation in oca2 fails to complement sleep loss when surface fish harboring this engineered mutation are crossed to different, independently evolved populations of albino cavefish with naturally occurring mutations in oca2, confirming that oca2 contributes to sleep loss. Finally, analysis of the oca2 locus in wild caught cave and surface fish suggests that oca2 is under positive selection in at least three cave populations. Taken together, these findings identify oca2 as a novel regulator of sleep and suggest that a pleiotropic function of oca2 underlies the adaptive evolution of both of albinism and sleep loss.

evolutionary biology↗

bioRxiv2020

Analysis of stress responses in Astyanax larvae reveals heterogeneity among different populations

Stress 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. Research HighlightO_LICavefish populations of A. mexicanus have reduced stress relative to surface conspecific at larval stages C_LIO_LIWe show that a glucocorticoid receptor, a negative regulator of the neuroendocrine stress axis, is upregulated in stress-resistant cavefish C_LIO_LIThere exists much ontological heterogeneity between different cavefish populations. C_LI

neuroscience↗

bioRxiv2020

Analysis of social swimming dynamics in the Mexican cavefish

Fish display a remarkable diversity of social behaviors, from highly social to largely solitary. While social behaviors are likely critical for survival, surprisingly little is known about how they evolve in response to changing environmental pressures. With its highly social surface form and multiple populations of a largely asocial, blind, cave-dwelling form, the Mexican tetra, Astyanax mexicanus, provides a powerful model to study the evolution of social behavior. Given numerous morphological and behavioral differences between the surface and cave forms, a primary impediment to understanding how this behavior evolved is a lack of computational and statistical approaches that can precisely identify independent aspects of social behavior. Here, we use motion tracking and kinematic analysis to quantify social swimming patterns and argue that the absence of schooling in cavefish is not merely a consequence of their inability to see but rather a genuine behavioral adaptation that impacts the way they explore their cave environment. Surface fish school, maintaining both close proximity and alignment with each other. In the dark, surface fish no longer school, but we show that they still attempt to align and maintain proximity when they find themselves near another fish. Conversely, cavefish exhibit little preference for proximity or alignment, instead actively avoiding each other. Cavefish also slow down when more fish are present in the tank, which neither surface fish in the light or in the dark do. Using data-driven computer simulations, we show that those two traits - active avoidance and collective slowdown - are sufficient to shift the exploration strategy of cavefish from mostly-following-the-walls to exploring-the-entire-tank. Finally, we find that those differences in collective swimming patterns are largely consistent across independently-evolved cave populations, revealing an evolutionary convergence on this emergent social behavior. Author SummaryThe Mexican tetra fish offers a fascinating window into the evolution of schooling behavior. Its ancestral-like surface form is found in the rivers and lakes of Mexico and Texas and is highly social. Over the last million years, A. mexicanus repeatedly evolved a second, largely asocial cave form after colonizing a series of dark, underground caves. Here we use motion tracking technology to compare the collective displacement patterns of four populations and present evidence that the loss of schooling in cave populations (i) is a genuine example of parallel behavioral evolution rather than a mere consequence of not being able to see in the dark and (ii) could constitute a cave-specific exploration strategy.

animal behavior and cognition↗