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

   https://doi.org/10.1126/sciadv.aba3126  

   Jaggard, James B. ; Lloyd, Evan ; Yuiska, Anders ; Patch, Adam ; Fily, Yaouen ; Kowalko, Johanna E. ; Appelbaum, Lior ; Duboue, Erik R. ; Keene, Alex C. ( September 2020 , Science Advances)

   null (Ed.)

   Environmental perturbation can drive behavioral evolution and associated changes in brain structure and function. The Mexican fish species, Astyanax mexicanus , includes eyed river-dwelling surface populations and multiple independently evolved populations of blind cavefish. We used whole-brain imaging and neuronal mapping of 684 larval fish to generate neuroanatomical atlases of surface fish and three different cave populations. Analyses of brain region volume and neural circuits associated with cavefish behavior identified evolutionary convergence in hindbrain and hypothalamic expansion, and changes in neurotransmitter systems, including increased numbers of catecholamine and hypocretin/orexin neurons. To define evolutionary changes in brain function, we performed whole-brain activity mapping associated with behavior. Hunting behavior evoked activity in sensory processing centers, while sleep-associated activity differed in the rostral zone of the hypothalamus and tegmentum. These atlases represent a comparative brain-wide study of intraspecies variation in vertebrates and provide a resource for studying the neural basis of behavioral evolution. 

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2. Repeated evolution of eye loss in Mexican cavefish: Evidence of similar developmental mechanisms in independently evolved populations

   https://doi.org/10.1002/jez.b.22977  

   Sifuentes‐Romero, Itzel ; Ferrufino, Estephany ; Thakur, Sunishka ; Laboissonniere, Lauren A. ; Solomon, Michael ; Smith, Courtney L. ; Keene, Alex C. ; Trimarchi, Jeffrey M. ; Kowalko, Johanna E. ( July 2020 , Journal of Experimental Zoology Part B: Molecular and Developmental Evolution)

   Evolution in similar environments often leads to convergence of behavioral and anatomical traits. A classic example of convergent trait evolution is the reduced traits that characterize many cave animals: reduction or loss of pigmentation and eyes. While these traits have evolved many times, relatively little is known about whether these traits repeatedly evolve through the same or different molecular and developmental mechanisms. The small freshwater fish,Astyanax mexicanus, provides an opportunity to investigate the repeated evolution of cave traits.A. mexicanusexists as two forms, a sighted, surface‐dwelling form and at least 29 populations of a blind, cave‐dwelling form that initially develops eyes that subsequently degenerate. We compared eye morphology and the expression of eye regulatory genes in developing surface fish and two independently evolved cavefish populations, Pachón and Molino. We found that many of the previously described molecular and morphological alterations that occur during eye development in Pachón cavefish are also found in Molino cavefish. However, for many of these traits, the Molino cavefish have a less severe phenotype than Pachón cavefish. Further, cave–cave hybrid fish have larger eyes and lenses during early development compared with fish from either parental population, suggesting that some different changes underlie eye loss in these two populations. Together, these data support the hypothesis that these two cavefish populations evolved eye loss independently, yet through some of the same developmental and molecular mechanisms.

    

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3. 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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4. Quantitative trait loci concentrate in specific regions of the Mexican cavefish genome and reveal key candidate genes for cave-associated evolution

   https://doi.org/10.1093/jhered/esae040  

   Wiese, Jonathan ; Richards, Emilie ; Kowalko, Johanna_E ; McGaugh, Suzanne_E ; Andrews, ed., Kim ( July 2024 , Journal of Heredity)

   A major goal of modern biology is connecting phenotype with its underlying genetic basis. The Mexican cavefish (Astyanax mexicanus), a characin fish species comprised of a surface ecotype and a cave-derived ecotype, is well suited as a model to study the genetic mechanisms underlying adaptation to extreme environments. Here, we map 206 previously published quantitative trait loci (QTL) for cave-derived traits in A. mexicanus to the newest version of the surface fish genome assembly, AstMex3. These analyses revealed that QTL clusters in the genome more than expected by chance, and this clustering is not explained by the distribution of genes in the genome. To investigate whether certain characteristics of the genome facilitate phenotypic evolution, we tested whether genomic characteristics associated with increased opportunities for mutation, such as highly mutagenic CpG sites, are reliable predictors of the sites of trait evolution but did not find any significant trends. Finally, we combined the QTL map with previously collected expression and selection data to identify 36 candidate genes that may underlie the repeated evolution of cave phenotypes, including rgrb, which is predicted to be involved in phototransduction. We found this gene has disrupted exons in all non-hybrid cave populations but intact reading frames in surface fish. Overall, our results suggest specific regions of the genome may play significant roles in driving adaptation to the cave environment in A. mexicanus and demonstrate how this compiled dataset can facilitate our understanding of the genetic basis of repeated evolution in the Mexican cavefish.

    

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5. Unique transcriptional signatures of sleep loss across independently evolved cavefish populations

   https://doi.org/10.1002/jez.b.22949  

   McGaugh, Suzanne E. ; Passow, Courtney N. ; Jaggard, James Brian ; Stahl, Bethany A. ; Keene, Alex C. ( April 2020 , Journal of Experimental Zoology Part B: Molecular and Developmental Evolution)

   Animals respond to sleep loss with compensatory rebound sleep, and this is thought to be critical for the maintenance of physiological homeostasis. Sleep duration varies dramatically across animal species, but it is not known whether evolutionary differences in sleep duration are associated with differences in sleep homeostasis. The Mexican cavefish,Astyanax mexicanus, has emerged as a powerful model for studying the evolution of sleep. While eyed surface populations ofA. mexicanussleep approximately 8 hr each day, multiple blind cavefish populations have converged on sleep patterns that total as little as 2 hr each day, providing the opportunity to examine whether the evolution of sleep loss is accompanied by changes in sleep homeostasis. Here, we examine the behavioral and molecular response to sleep deprivation across four independent populations ofA. mexicanus. Our behavioral analysis indicates that surface fish and all three cavefish populations display robust recovery sleep during the day following nighttime sleep deprivation, suggesting sleep homeostasis remains intact in cavefish. We profiled transcriptome‐wide changes associated with sleep deprivation in surface fish and cavefish. While the total number of differentially expressed genes was not greater for the surface population, the surface population exhibited the highest number of uniquely differentially expressed genes than any other population. Strikingly, a majority of the differentially expressed genes are unique to individual cave populations, suggesting unique expression responses are exhibited across independently evolved cavefish populations. Together, these findings suggest sleep homeostasis is intact in cavefish despite a dramatic reduction in overall sleep duration.

    

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