Kinematic analysis deconstructs the evolved loss of schooling behavior in 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.