Stamhuis, E. | Search bioRxiv

bioRxiv2026

Phenotype-dependent schooling behaviour across hierarchical levels in three-spined sticklebacks

Schooling is a widespread behaviour among pelagic fish that reduces locomotion costs of migration and predation risk. It is characterised by coordinated movements, speed and orientation of group members. Although schooling can vary both between populations and among individuals of the same population, these levels of variation are seldom considered together. Here, we investigated whether schooling tendencies in three-spined sticklebacks (Gasterosteus aculeatus) vary between populations and among individuals within-populations depending on their phenotype. We first compared the schooling behaviour of anadromous (migrants) and recently landlocked (residents) populations and tested whether individual sociability explained within-population variation in schooling. We then studied whether schooling behaviour is modulated when migrants and residents are in mixed groups. Migrant groups displayed better schooling performance than residents with higher alignment. Within migrant groups, less social individuals displayed more leadership, were better aligned, swam closer to others and fatigued less than more social fish. These patterns were absent in residents. When the two populations were mixed, overall schooling performance declined, particularly in migrants, with schools exhibiting reduced compaction and alignment, resembling resident groups. Thus, individuals did not modulate their schooling behaviour to the group social composition and phenotype-dependent schooling patterns were disrupted in migrants when mixed. These findings suggest that migration-related behaviours can disappear quickly post-isolation. They also highlight the importance of individual sociability in self-organisation and shaping collective behaviour, especially in populations that retain migratory behaviour. Considering behavioural variation across multiple hierarchical levels is thus key to understanding complex social systems.

animal behavior and cognition↗

bioRxiv2021

Does genetic differentiation underlie behavioral divergence in response tomigration barriers in sticklebacks? A common garden experiment

Water management measures in the 1970s in the Netherlands have produced a large number of resident populations of three-spined sticklebacks that are no longer able to migrate to the sea. This may be viewed as a replicated field experiment, allowing us to study how the resident populations are coping with human-induced barriers to migration. We have previously shown that residents are smaller, bolder, more exploratory, more active, more aggressive, exhibited lower shoaling and lower migratory tendencies compared to their ancestral migrant counterparts. However, it is not clear if these differences in wild-caught residents and migrants reflect genetic differentiation, rather than different developmental conditions. To investigate this, we raised offspring of four crosses (migrant [male] x migrant [female], resident [male] x resident [female], migrant [male] x resident [female], resident [male] x migrant [female]) under similar controlled conditions and tested for differences in morphology and behavior as adults. We found that lab-raised resident sticklebacks exhibited lower shoaling and migratory tendencies as compared to lab-raised migrants, retaining the differences in their wild-caught parents. This indicates genetic differentiation of these traits. For all other traits, the lab-raised sticklebacks of the various crosses did not differ significantly, suggesting that the earlier-found contrast between wild-caught fish reflect differences in their environment. Our study shows that barriers to migration can lead to rapid differentiation in behavioral tendencies over contemporary timescales ([~]50 generations), and that part of these differences reflects genetic differentiation. Significance statementMany organisms face changes to their habitats due to human activities. Much research is therefore dedicated to the question whether and how organisms are able to adapt to novel conditions. We address this question in three-spined sticklebacks, where water management measures cut off some populations, prohibiting their seasonal migration to the North Sea. In a previous study, we showed that wild-caught resident fish exhibited markedly different behavior than migrants. To disentangle whether these differences reflect genetic differentiation or differences in the conditions under which the wild-caught fish grew up, we conducted crosses, raising the F1 offspring under identical conditions. As their wild-caught parents, the F1 of resident x resident crosses exhibited lower migratory and shoaling tendencies than the F1 of migrant x migrant crosses, while the F1 of hybrid crosses were intermediate. This suggests that [~]50 years of isolation are sufficient to induce behaviorally relevant genetic differentiation.

evolutionary biology↗