Individual, but not population asymmetries, are modulated by social environment and genotype in Drosophila melanogaster

Abstract

Theory predicts that social interactions can induce an alignment of behavioral asymmetries between individuals (i.e., population-level lateralization), but evidence for this effect is mixed. To understand how interaction with other individuals affects behavioral asymmetries, we systematically manipulated the social environment of Drosophila melanogaster, testing individual flies and dyads (female-male, female-female and male-male pairs). In these social contexts we measured individual and population asymmetries in individual behaviors (circling asymmetry, wing use) and dyadic behaviors (relative position and orientation between two flies) in five different genotypes. We reasoned that if coordination between individuals drives alignment of behavioral asymmetries, greater alignment at the population-level should be observed in social contexts compared to solitary individuals. We observed that the presence of other individuals influenced the behavior and position of flies but had unexpected effects on individual and population asymmetries: individual-level asymmetries were strong and modulated by the social context but population-level asymmetries were mild or absent. Moreover, the strength of individual-level asymmetries differed between strains, but this was not the case for population-level asymmetries. These findings suggest that the degree of social interaction found in Drosophila is insufficient to drive population-level behavioral asymmetries.

Figure 1

Vectors used to measure circling asymmetry, as the angle between the previous trajectory (vector between t₁ and t₂) and the current trajectory (vector between t₂ and t₃). Clockwise deviations are negative, anticlockwise deviations are positive.

Figure 2

Social metrics calculated for dyads of flies. (a) Distance in mm between the centroids of the flies. (b) The Position of fly B is the angle between the vector trajectory of A and the vector between the centroids of A and B. When B is located to the right of A Position is negative, when B is located to the left of A Position is positive. (c) The relative Orientation between A and B is the angle between the facing vectors of the two flies. It ranges between 0°, when flies are parallel, and 180°, when flies are facing opposite directions.

Figure 3

(a) Overall mean population circling asymmetry by Context (FF, MM, FM, SINGLE) and (b) by Context and Strain. The dashed line indicates the absence of population-level circling asymmetry. Here and elsewhere, boxes demarcate the interquartile range, thick horizontal line the median, whiskers minimum/maximum excluding the outliers, and point outside this range outliers, namely points greater/lower than 1.5 times the interquartile range).

Figure 4

(a) Overall individual circling asymmetry index by Context (FF, MM, FM, SINGLE) and (b) by Context and Strain. The dashed line indicates the absence of individual-level circling asymmetry.

Figure 5

(a) Distribution of individual-level circling asymmetry values. (b) Distribution of population-level circling asymmetry values. (c) Distribution of individual-level wing use asymmetry values. (d) Distribution of population-level wing-use asymmetry values. Dashed lines indicate the distributions expected in the absence of individual or population level asymmetry (half normal or normal distribution), adjusted on the observed variance.

Figure 6

Kernel density distribution of the Position (in degrees) exhibited by the overall sample (all genotypes) during the test in each Context +/− Standard Error around our estimate of the distribution, calculated with bootstrap resampling.

Figure 7

Kernel density distribution of Position (in degrees) kept during the test in each Strain, Context and Sex +/− Standard Error around our estimate of the distribution, calculated with bootstrap resampling: (a) female-female dyads by strain, (b) females of female-male dyads by strain, (c) male-male dyads by strain, (d) males of female-male dyads by strain, (e) female-male dyads.

Figure 8

Heatmap in polar coordinates, showing the joint distribution of Orientation and Distance from the focal fly in each Context: (a) female-female, male-male and female-male dyads overall (b) female-female, male-male and female-male dyads for each strain.