Abstract
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, and more aggressive and 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 ♂ × migrant ♀, resident ♂ × resident ♀, migrant ♂ × resident ♀, resident ♂ × migrant ♀) 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 reflects 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 × resident crosses exhibited lower migratory and shoaling tendencies than the F1 of migrant × 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.
Highlights
Habitat fragmentation resulting from human activities is considered to be a major threat for many animal populations (Foley et al 2005; Fischer and Lindenmayer 2007)
Behavioral Ecology and Sociobiology (2021) 75: 161 habitat size, habitat loss, and loss of habitat connectivity (Fahrig 2003). This poses a threat to animal populations, especially for migratory species which rely on connectivity between functional habitats for reproduction and survival (Legrand et al 2017)
We further found that shoaling and migratory tendencies varied significantly and consistently between RR and MM crosses in the same direction, with RR crosses exhibiting lower shoaling and migratory tendencies than MM crosses (Fig. 3c, e; Table 1; overall effect of crosses on shoaling: χ2 = 17.91, df = 3, p < 0.01, on migratory tendency: χ2 = 14.37, df = 3, p < 0.01)
Summary
Habitat fragmentation resulting from human activities is considered to be a major threat for many animal populations (Foley et al 2005; Fischer and Lindenmayer 2007). Behavioral Ecology and Sociobiology (2021) 75: 161 habitat size, habitat loss, and loss of habitat connectivity (Fahrig 2003) This poses a threat to animal populations, especially for migratory species which rely on connectivity between functional habitats for reproduction and survival (Legrand et al 2017). Plasticity, defined as the ability of a genotype to exhibit different phenotypes in response to the environment (Via et al 1995; Pigliucci 2005), can provide a rapid mechanism to respond to environmental changes (Ghalambor et al 2007). Selection may favor genotypes with varying levels of plasticity (Scheiner 1993; Nussey et al 2007), implying that the mentioned mechanisms are intertwined (Edelaar et al 2017) and that observed population divergence could reflect genetic differentiation and/or differences in the environments under which individuals grow up. In the case where migrants are no longer able to migrate (forced “residents”), we expect selection to act on either the traits themselves or on the degree of plasticity
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