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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.
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Cascading indirect genetic effects in a clonal vertebrate
Understanding how individual differences arise and how their effects propagate through groups are fundamental issues in biology. Individual differences can arise from indirect genetic effects (IGE): genetically based variation in the conspecifics with which an individual interacts. Using a clonal species, the Amazon molly ( Poecilia formosa ), we test the hypothesis that IGE can propagate to influence phenotypes of the individuals that do not experience them firsthand. We tested this by exposing genetically identical Amazon mollies to conspecific social partners of different clonal lineages, and then moving these focal individuals to new social groups in which they were the only member to have experienced the IGE. We found that genetically different social environments resulted in the focal animals experiencing different levels of aggression, and that these IGE carried over into new social groups to influence the behaviour of naive individuals. These data reveal that IGE can cascade beyond the individuals that experience them. Opportunity for cascading IGE is ubiquitous, especially in species with long-distance dispersal or fission–fusion group dynamics. Cascades could amplify (or mitigate) the effects of IGE on trait variation and on evolutionary trajectories. Expansion of the IGE framework to include cascading and other types of carry-over effects will therefore improve understanding of individual variation and social evolution and allow more accurate prediction of population response to changing environments.
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- Award ID(s):
- 1740466
- PAR ID:
- 10406959
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 289
- Issue:
- 1978
- ISSN:
- 0962-8452
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2022.0731
