Born this way: individuality is seeded before birth and robust to environmental stress

James Hayden Gallagher , Ammon Perkes, Chia-Chen Chang, Emma Chirila, Karen Kacevas, Kate Laskowski

Behavioral individuality, or consistent individual differences in behavior, are pervasive across the animal world and have major ecological and evolutionary consequences. Nevertheless, we still have a limited understanding of what drives individuality and how it emerges during ontogeny. Here, we subjected clonal individuals to a ubiquitous yet critical environmental challenge—the threat of predation—to disentangle the developmental mechanisms of individuality. Under such a salient environmental stressor, among-individual differences may collapse or expand depending on whether there is a single or multiple optimal strategies, demonstrating that individuality itself is a developmentally plastic trait. If, however, individuality is determined before birth, we may expect it to be resistant to environmental influences. We continuously tracked the behavior of genetically identical fish (Amazon mollies, Poecilia formosa), reared with or without predation stress, all day, every day, from birth through their first month of life, providing unprecedented insight into the trajectories of behavioral development in response to this key environmental cue. Predation shifted mean-level behaviors, with predator-exposed individuals swimming more slowly and spending more time near their refuges. However, the magnitude of individuality (as evidenced by repeatability) increased similarly over development in both treatments, indicating that individuality crystallizes robustly over time, even under stress and in a vacuum of genetic variation. Predator-reared fish also exhibited greater within-individual variation in refuge use, suggesting decreased behavioral predictability or disrupted developmental canalization in response to stress. Surprisingly, maternal identity, but not maternal behavior, was the strongest contributor to variance in swimming velocity (accounting for two thirds of variation), pointing to maternal effects as a key pre-birth source of behavioral variation. Variance in refuge use however was only negligibly explained by maternal identity, highlighting that fundamental behaviors may have very different developmental mechanisms. Collectively, our results show that individuality persists despite environmental stress and is likely seeded before birth through non-genetic factors. Even in the face of a shared environmental challenge, the behavioral trajectories of individuals are unique.