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

Abstract

Background 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 mexicanus exists 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. Results To define how aggressive behaviors evolve, we performed a high-resolution analysis of multiple social behaviors that occur during aggressive interactions in A. 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. Conclusion 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 establish A. mexicanus as a model for investigating the evolutionary and genetic basis of aggressive behavior.

Sensing in the dark: Constructive evolution of the lateral line system in blind populations of Astyanax mexicanus

“…Previous work from others and I showed that multiple populations of A. mexicanus cavefish exhibit reductions in aggressive behaviors (Elipot et al, 2013;Espinasa et al, 2022;Rodriguez-Morales et al, 2022). Although one might think that not seeing another individual would eliminate social interactions, in A. mexicanus, surface fish remain aggressive when visually deprived, while blind Molino cavefish conserved aggressive behaviors (Rodriguez-Morales et al, 2022). Previous work in the juvenile Atlantic salmon, Salmo salar, showed an increase in aggression in the dark, providing evidence that light and visual cues are not necessary for the display of aggressive behavior (Valdimarsson & Metcalfe, 2001).…”

“…Another behavior that evolved reductions in blind cavefish populations of the Mexican tetra is aggression (Parzefall & Hausberg, 2001). Previous work from others and I showed that multiple populations of A. mexicanus cavefish exhibit reductions in aggressive behaviors (Elipot et al, 2013;Espinasa et al, 2022;Rodriguez-Morales et al, 2022). Although one might think that not seeing another individual would eliminate social interactions, in A. mexicanus, surface fish remain aggressive when visually deprived, while blind Molino cavefish conserved aggressive behaviors (Rodriguez-Morales et al, 2022).…”

“…This is in stark contrast with schooling, where studies across species show that while the lateral line is not needed for schooling, vision remains indispensable, with fish unable to school efficiently in the dark (Kowalko et al., 2013 ; Tidswell et al., 2023 ). The opposite is happening in aggression, where vision seems to be entirely dispensable for aggressive interactions to ensue among aggressive surface fish or semi‐aggressive Molino cavefish (Rodriguez‐Morales et al., 2022 ). This raises the very likely possibility that other, non‐visual sensory systems are recruited for conspecific detection and reaction during aggression.…”

“…Over the last decade, a myriad of tools were developed to harness the full potential of A. mexicanus as a model for evolutionary biology, developmental biology, genetics, and neurobiology. A fully assembled genome for surface fish and Pachón cavefish (McGaugh et al., 2014 ; Warren et al., 2021 ), methods for transgenesis (Stahl et al., 2019 ), transcriptomic analyses (McGaugh et al., 2020 ), genetic mapping (Riddle et al., 2021 ), robust and reproducible behavioral assays (Chin et al., 2018 ; Duboué et al., 2011 ; Kowalko et al., 2013 ; Rodriguez‐Morales et al., 2022 ), and the application of gene editing with CRISPR/Cas9 (Klaassen et al., 2018 ) have positioned the field in an unprecedented scenario, with limitless possibilities. Now more than ever, we can attempt to understand the mechanisms – genetic or environmental – behind expansion of the lateral line and learn clues from this model that can ultimately inform evolutionary biology and biomedical research altogether.…”

“…(c) Image of an adult Pachón cavefish. et al, 2014;Warren et al, 2021), methods for transgenesis (Stahl et al, 2019), transcriptomic analyses (McGaugh et al, 2020, genetic mapping (Riddle et al, 2021), robust and reproducible behavioral assays (Chin et al, 2018;Duboué et al, 2011;Kowalko et al, 2013;Rodriguez-Morales et al, 2022), and the application of gene editing with CRISPR/Cas9 (Klaassen et al, 2018)…”