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

Consistent individual differences in behavior, known as behavioral individuality, 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, the environment does not impact among-individual variation, this suggests that individuality is determined before birth. We continuously tracked the behavior of genetically identical fish (Amazon mollies, Poecilia formosa), reared with or without predation stress, from birth through their first month of life. 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 variability in refuge use, suggesting increased behavioral flexibility or disrupted developmental canalization in response to stress. Surprisingly, maternal identity, but not maternal behavior, was the strongest predictor of swimming speed, pointing to non-behavioral maternal effects as a key pre-birth source of behavioral variation. Refuge use however was not at all predicted by maternal identity, indicating that major fitness-related behaviors can have entirely different developmental mechanisms. Collectively, we show that individuality persists despite environmental stress and is seeded before birth through non-genetic factors. Even in the face of a shared environmental challenge, the behavioral trajectories of individuals are unique.