The quantitative genetic architecture of the bold-shy continuum in zebrafish, Danio rerio

Abstract

In studies of consistent individual differences (personality) along the bold-shy continuum, a pattern of behavioral correlations frequently emerges: individuals towards the bold end of the continuum are more likely to utilize risky habitat, approach potential predators, and feed under risky conditions. Here, we address the hypothesis that observed phenotypic correlations among component behaviors of the bold-shy continuum are a result of underlying genetic correlations (quantitative genetic architecture). We used a replicated three-generation pedigree of zebrafish (Danio rerio) to study three putative components of the bold-shy continuum: horizontal position, swim level, and feeding latency. We detected significant narrow-sense heritabilities as well as significant genetic and phenotypic correlations among all three behaviors, such that fish selected for swimming at the front of the tank swam closer to the observer, swam higher in the water column, and fed more quickly than fish selected for swimming at the back of the tank. Further, the lines varied in their initial open field behavior (swim level and activity level). The quantitative genetic architecture of the bold-shy continuum indicates that the multivariate behavioral phenotype characteristic of a "bold" personality type may be a result of correlated evolution via underlying genetic correlations.

Figure 1. Response to two generations of selection on horizontal position (time near observer) in zebrafish.

A: Replicate 1, B: Replicate 2. x-axis generations: P = unselected parental generation (gray circle), 1 = first generation progeny from selected parents, 2 = second generation progeny from selected first generation parents. Black diamonds with a solid line represent means ± SE of High line fish, open squares with a dashed line represent means ± SE of Low line fish. “*” indicate significant (p<0.05) differences between lines within a generation using a mixed-model ANOVA.

Figure 2. Response of Swim Level and Feeding Latency to selection on horizontal position in zebrafish.

Replicate 1 (A & C), Replicate 2 (B & D). P = unselected parental generation (gray circle), 1 = first generation progeny from selected parents, 2 = second generation progeny from selected parents. Black diamonds with a solid line represent means ± SE of High line fish, open squares with a dashed line represent means ± SE of Low line fish. “*” indicate significant (p<0.05) differences between lines within a generation using a mixed-model ANOVA.

Figure 3. Behavior of second-generation selected lines of zebrafish in an open field environment during two periods.

Initial time period is during the introduction to the 19-L aquaria, and Acclimated is after one hour in the aquaria. Proportion of time on the bottom (A) proportion of time at the surface of the tank (B), activity level (C), and proportion of time on the side with cover (D). Filled bars represent means ± SE of the High line, while open bars represent means ±SE of the low line. ‘*’ indicates a significant difference between the lines within a time period using a mixed-model ANOVA.