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1. Convergence on reduced aggression through shared behavioral traits in multiple populations of Astyanax mexicanus

   https://doi.org/10.1186/s12862-022-02069-8  

   Rodriguez-Morales, Roberto ; Gonzalez-Lerma, Paola ; Yuiska, Anders ; Han, Ji Heon ; Guerra, Yolanda ; Crisostomo, Lina ; Keene, Alex C. ; Duboue, Erik R. ; Kowalko, Johanna E. ( October 2022 , BMC Ecology and Evolution)

   Aggression is observed across the animal kingdom, and benefits animals in a number of ways to increase fitness and promote survival. While aggressive behaviors vary widely across populations and can evolve as an adaptation to a particular environment, the complexity of aggressive behaviors presents a challenge to studying the evolution of aggression. The Mexican tetra,Astyanax mexicanusexists as an aggressive river-dwelling surface form and multiple populations of a blind cave form, some of which exhibit reduced aggression, providing the opportunity to investigate how evolution shapes aggressive behaviors.

   To define how aggressive behaviors evolve, we performed a high-resolution analysis of multiple social behaviors that occur during aggressive interactions inA. mexicanus.We found that many of the aggression-associated behaviors observed in surface-surface aggressive encounters were reduced or lost in Pachón cavefish. Interestingly, one behavior, circling, was observed more often in cavefish, suggesting evolution of a shift in the types of social behaviors exhibited by cavefish. Further, detailed analysis revealed substantive differences in aggression-related sub-behaviors in independently evolved cavefish populations, suggesting independent evolution of reduced aggression between cave populations. We found that many aggressive behaviors are still present when surface fish fight in the dark, suggesting that these reductions in aggression-associated and escape-associated behaviors in cavefish are likely independent of loss of vision in this species. Further, levels of aggression within populations were largely independent of type of opponent (cave vs. surface) or individual stress levels, measured through quantifying stress-like behaviors, suggesting these behaviors are hardwired and not reflective of population-specific changes in other cave-evolved traits.

   These results reveal that loss of aggression in cavefish evolved through the loss of multiple aggression-associated behaviors and raise the possibility that independent genetic mechanisms underlie changes in each behavior within populations and across populations. Taken together, these findings reveal the complexity of evolution of social behaviors and establishA. mexicanusas a model for investigating the evolutionary and genetic basis of aggressive behavior.

    

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2. A chromosome-level genome of Astyanax mexicanus surface fish for comparing population-specific genetic differences contributing to trait evolution

   https://doi.org/10.1038/s41467-021-21733-z  

   Warren, Wesley C. ; Boggs, Tyler E. ; Borowsky, Richard ; Carlson, Brian M. ; Ferrufino, Estephany ; Gross, Joshua B. ; Hillier, LaDeana ; Hu, Zhilian ; Keene, Alex C. ; Kenzior, Alexander ; et al ( December 2021 , Nature Communications)

   null (Ed.)

   Abstract Identifying the genetic factors that underlie complex traits is central to understanding the mechanistic underpinnings of evolution. Cave-dwelling Astyanax mexicanus populations are well adapted to subterranean life and many populations appear to have evolved troglomorphic traits independently, while the surface-dwelling populations can be used as a proxy for the ancestral form. Here we present a high-resolution, chromosome-level surface fish genome, enabling the first genome-wide comparison between surface fish and cavefish populations. Using this resource, we performed quantitative trait locus (QTL) mapping analyses and found new candidate genes for eye loss such as dusp26 . We used CRISPR gene editing in A. mexicanus to confirm the essential role of a gene within an eye size QTL, rx3 , in eye formation. We also generated the first genome-wide evaluation of deletion variability across cavefish populations to gain insight into this potential source of cave adaptation. The surface fish genome reference now provides a more complete resource for comparative, functional and genetic studies of drastic trait differences within a species. 

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3. Kinematic analysis of social interactions deconstructs the evolved loss of schooling behavior in cavefish

   https://doi.org/10.1371/journal.pone.0265894  

   Patch, Adam ; Paz, Alexandra ; Holt, Karla J. ; Duboué, Erik R. ; Keene, Alex C. ; Kowalko, Johanna E. ; Fily, Yaouen ( April 2022 , PLOS ONE)

   Rétaux, Sylvie (Ed.)

   Fish display a remarkable diversity of social behaviors, both within and between species. 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. Here we use motion tracking and analysis of swimming kinematics to quantify social swimming in four Astyanax mexicanus populations. In the light, surface fish school, maintaining both close proximity and alignment with each other. In the dark, surface fish no longer form coherent schools, however, they still show evidence of an attempt to align and maintain proximity when they find themselves near another fish. In contrast, cavefish from three independently-evolved populations (Pachón, Molino, Tinaja) show little preference for proximity or alignment, instead exhibiting behaviors that suggest active avoidance of each other. Two of the three cave populations we studied also slow down when more fish are present in the tank, a behavior which is not observed in surface fish in light or the dark, suggesting divergent responses to conspecifics. Using data-driven computer simulations, we show that the observed reduction in swimming speed is sufficient to alter the way fish explore their environment: it can increase time spent exploring away from the walls. Thus, the absence of schooling in cavefish is not merely a consequence of their inability to see, but may rather be a genuine behavioral adaptation that impacts the way they explore their environment. 

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4. Dark‐rearing uncovers novel gene expression patterns in an obligate cave‐dwelling fish

   https://doi.org/10.1002/jez.b.22947  

   Sears, Connor R. ; Boggs, Tyler E. ; Gross, Joshua B. ( May 2020 , Journal of Experimental Zoology Part B: Molecular and Developmental Evolution)

   Extreme environments often result in the evolution of dramatic adaptive features. The Mexican tetra,Astyanax mexicanus, includes 30 different populations of cave‐dwelling forms that live in perpetual darkness. As a consequence, many populations have evolved eye loss, reduced pigmentation, and amplification of nonvisual sensory systems. Closely‐related surface‐dwelling morphs demonstrate typical vision, pigmentation, and sensation. Transcriptomic assessments in this system have revealed important developmental changes associated with the cave morph, however, they have not accounted for photic rearing conditions. Prior studies reared individuals under a 12:12 hr light/dark (LD) cycle. Here, we reared cavefish under constant darkness (DD) for 5+ years. From these experimental individuals, we performed mRNA sequencing and compared gene expression of surface fish reared under LD conditions to cavefish reared under DD conditions to identify photic‐dependent gene expression differences. Gene Ontology enrichment analyses revealed a number of previously underappreciated cave‐associated changes impacting blood physiology and olfaction. We further evaluated the position of differentially expressed genes relative to QTL positions from prior studies and found several candidate genes associated with these ecologically relevant lighting conditions. In sum, this work highlights photic conditions as a key environmental factor impacting gene expression patterns in blind cave‐dwelling fish.

    

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5. Trait Loss in Evolution: What Cavefish Have Taught Us about Mechanisms Underlying Eye Regression

   https://doi.org/10.1093/icb/icad032  

   Sifuentes-Romero, Itzel ; Aviles, Ari M. ; Carter, Joseph L. ; Chan-Pong, Allen ; Clarke, Anik ; Crotty, Patrick ; Engstrom, David ; Meka, Pranav ; Perez, Alexandra ; Perez, Riley ; et al ( May 2023 , Integrative And Comparative Biology)

   Reduction or complete loss of traits is a common occurrence throughout evolutionary history. In spite of this, numerous questions remain about why and how trait loss has occurred. Cave animals are an excellent system in which these questions can be answered, as multiple traits, including eyes and pigmentation, have been repeatedly reduced or lost across populations of cave species. This review focuses on how the blind Mexican cavefish, Astyanax mexicanus, has been used as a model system for examining the developmental, genetic, and evolutionary mechanisms that underlie eye regression in cave animals. We focus on multiple aspects of how eye regression evolved in A. mexicanus, including the developmental and genetic pathways that contribute to eye regression, the effects of the evolution of eye regression on other traits that have also evolved in A. mexicanus, and the evolutionary forces contributing to eye regression. We also discuss what is known about the repeated evolution of eye regression, both across populations of A. mexicanus cavefish and across cave animals more generally. Finally, we offer perspectives on how cavefish can be used in the future to further elucidate mechanisms underlying trait loss using tools and resources that have recently become available.

    

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