Individual learning phenotypes drive collective behavior

Abstract

Individual differences in learning can influence how animals respond to and communicate about their environment, which may nonlinearly shape how a social group accomplishes a collective task. There are few empirical examples of how differences in collective dynamics emerge from variation among individuals in cognition. Here, we use a naturally variable and heritable learning behavior called latent inhibition (LI) to show that interactions among individuals that differ in this cognitive ability drive collective foraging behavior in honey bee colonies. We artificially selected two distinct phenotypes: high-LI bees that ignore previously familiar stimuli in favor of novel ones and low-LI bees that learn familiar and novel stimuli equally well. We then provided colonies differentially composed of different ratios of these phenotypes with a choice between familiar and novel feeders. Colonies of predominantly high-LI individuals preferred to visit familiar food locations, while low-LI colonies visited novel and familiar food locations equally. Interestingly, in colonies of mixed learning phenotypes, the low-LI individuals showed a preference to visiting familiar feeders, which contrasts with their behavior when in a uniform low-LI group. We show that the shift in feeder preference of low-LI bees is driven by foragers of the high-LI phenotype dancing more intensely and attracting more followers. Our results reveal that cognitive abilities of individuals and their social interactions, which we argue relate to differences in attention, drive emergent collective outcomes.

Keywords: cognition; collective behavior; honey bee; latent inhibition; learning.

Fig. 1.

Social environment does not alter expression of heritable latent inhibition. LI scores of individuals from high-LI lines that spent their adult life either in high-LI-only colonies (red, n = 36) or in a control colony with a variety of LI phenotypes from an open mated queen (red with gray vertical lines, n = 18); individuals from low LI lines that spent their adult life either in low-LI-only colonies (yellow, n = 52) or in control colonies (yellow with gray vertical lines, n = 10). LI score is calculated by dividing the number of responses to the novel odor (A) + 1 by the number of responses to the familiar odor (X) + 1. An LI score closer to 1 indicates similar responses to novel and familiar odors and qualifies a bee as low-LI, while an LI score over 1.33 qualifies a bee as high LI, having fewer responses to familiar odor and more responses to the novel odor. Here, high-LI bees had a median LI score of 2 in both treatments, and low-LI bees had a median of 1.25 when in low-LI colonies and 1.29 in control colonies. Different letters above violins indicate statistically significant differences according to a post hoc Tukey test. In this and subsequent figures, the large black dot is the median, the white box is the interquartile range (IQR), whiskers extend to 1.5*IQR, and the small points beyond the whiskers are outliers. The violin shapes show the distribution of the data. Here, and in all following figures, yellow indicates low-LI colonies and individuals, gray indicates control colonies and individuals, and red indicates high-LI colonies and individuals.

Fig. 2.

Colonies constructed from different genetic lines selected for high or low latent inhibition exhibited differences in collective foraging behavior. (A) The experimental setup illustrating the location of feeders in relation to the location of the colony (Center, white) within the experimental flight cage arena (represented here as a large rectangle that encompasses the feeder and colony diagram). The familiar feeder F (red) was provided on day 1 and on all subsequent days. Novel feeder X (blue) was presented on day 2, novel feeder Y (purple) on day 3, and novel feeder Z (orange) on day 4. See SI Appendix, Table S2, for associated odors. Visits to all novel feeders were combined for statistical analysis. (B) Cumulative number of visits of bees to all feeders over time by colony type. Different letters to the right of the lines indicate statistically significant differences according to a post hoc Tukey test. For further illustration of visitation by each colony on each day, see SI Appendix, Fig. S1. (C) Percentage of revisits out of the total number of visits to all feeders by colony type. Here and in all following panels, different letters above boxes indicate statistically significant differences according to a post hoc Tukey test. (D) Number of all visits to the familiar feeder (solid boxes) and a novel feeder (hatched boxes) for each type of colony, when both novel and familiar feeders were presented simultaneously (days 2 to 4). (E) Percentage of revisits out of the total number of visits to either the familiar or the novel feeder by type of colony when both novel and familiar feeders were presented simultaneously (days 2 to 4). In C–E, horizontal lines are the median, the boxes are the IQR, whiskers extend to 1.5*IQR, and the small points beyond the whiskers are outliers. n = 24 colonies, six colonies per group type, and 6,172 total visits.

Fig. 3.

Visits of individuals from different genetically selected lines when in a mixed colony. Daily visits to the familiar (solid) and novel (hatched) feeders by individual bees in mixed colonies from low-LI parents (yellow), high-LI parents (red) or open-mated queens (gray) in (A) in 2017, n = 6 mixed colonies, 2,347 overall visits and in (B) in mixed colonies from lines that were reselected in 2018, n = 6 colonies, 6,272 overall visits. The horizontal line in the box is the median, the box is 25 to 75% of the data, whiskers represent 95% of the data, and diamonds show outliers beyond 95%. Different letters above boxes indicate statistically significant differences according to a post hoc Tukey test.

Fig. 4.

Recruitment dances facilitate integration of information from different genetically selected lines. (A) The experimental setup illustrating the location of feeders in relation to the location of the colony entrance (Top Right, white) within the experimental arena (large rectangle). The familiar feeder F (red) was provided on day 1 and on all subsequent days. Novel feeder X (blue) was presented on day 2, novel feeder Y (purple) on day 3, and novel feeder Z (orange) on day 4. See SI Appendix, Table S2, for associated odors. Visitations to novel feeders were combined for statistical analysis. (B) Proportion of dances (n = 667) or follows (n = 1,201) across six colonies performed by bees from each line, relative to their abundance in the mixed colony (350 high LI, 350 low LI, 700 control). We accounted for the difference in abundance of each selected line by dividing the number of observed control dancers by 2 before calculating these proportions. (C) Proportion of dances performed per LI line type that were either followed by at least one individual (colored) or not followed by any other bees (black). (D) Proportion of dances by LI line type that were followed (from B) broken down by LI of the follower. (E) Relationship between number of followers and duration of a dance by line. Point and line colors indicate LI of dancer. Best-fit line represents the GLM, and shaded area represents the 95% confidence interval. (F) Rate of turns per second in a dance by line. The large black dots in the violin shape is the mean, the white box in the violin shape is 25 to 75% of the data, and whiskers represent 95% of the data. The violin shapes illustrate distribution of the data. Different letters above violins indicate statistically significant differences according to a post hoc Tukey test.