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

• Published in: iScience 2023-09, Vol.26 (9), p.107431-107431, Article 107431
• Main Authors: Paz, Alexandra, Holt, Karla J., Clarke, Anik, Aviles, Ari, Abraham, Briana, Keene, Alex C., Duboué, Erik R., Fily, Yaouen, Kowalko, Johanna E.
• Format: Article
• Language: English
• Subjects: Biological sciences; Evolutionary biology; Zoology
• ISSN: 2589-0042; 2589-0042
• DOI: 10.1016/j.isci.2023.107431

Collective motion emerges from individual interactions which produce group-wide 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, Astyanax 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 mediated by changes in the way fish modulate speed and turning relative to neighbors. This transition begins with the tendency to align to neighbors emerging by 28 days post-fertilization and ends with the emergence of robust attraction by 70 days post-fertilization. Cavefish exhibit neither alignment nor attraction at any stage of development. These results reveal how evolution alters local interactions to produce striking differences in collective behavior. [Display omitted] •Schooling behavior emerges over the course of development in Astyanax surface fish•Tendency to align develops prior to attraction in surface fish•Cavefish do not show the transition to alignment or attraction found in surface fish•Reduced turning and speeding relative to neighbors contributes to loss of schooling Biological sciences; Zoology; Evolutionary biology