Antimicrobial strength increases with group size: implications for social evolution

Abstract

We hypothesize that aggregations of animals are likely to attract pathogenic micro-organisms and that this is especially the case for semisocial and eusocial insects where selection ultimately led to group sizes in the thousands or even millions, attracting the epithet 'superorganism'. Here, we analyse antimicrobial strength, per individual, in eight thrips species (Insecta: Thysanoptera) that present increasing innate group sizes and show that species with the largest group size (100-700) had the strongest antimicrobials, those with smaller groups (10-80) had lower antimicrobial activity, while solitary species showed none. Species with large innate group sizes showed strong antimicrobial activity while the semisocial species showed no activity until group size increased sufficiently to make activity detectable. The eusocial species behaved in a similar way, with detectable activity appearing once group size exceeded 120. These analyses show that antimicrobial strength is determined by innate group size. This suggests that the evolution of sociality that, by definition, increases group size, may have had particular requirements for defences against microbial pathogens. Thus, increase in group size, accompanied by increased antibiotic strength, may have been a critical factor determining the 'point of no return', early in the evolution of social insects, beyond which the evolution of social anatomical and morphological traits was irreversible. Our data suggest that traits that increase group size in general are accompanied by increased antimicrobial strength and that this was critical for transitions from solitary to social and eusocial organization.

Figure 1.

Concentration–growth response curves showing activity of extracts from eight thrips species against S. aureus. Axes x, number of thrips; y, ratio of test well to control well growth. The highest extract concentration was equivalent to 80 individuals with a three-fourth dilution series, except for O. aloba where the highest concentration was equivalent to 150 individuals with a one-half dilution series. Following incubation at 37°C for 18 h, growth was measured as an increase in optical density (OD) and expressed as: increased OD test well/increased OD S. aureus control. The curves were compared by functional analysis of variance [16] and differed significantly between group-size classes (F = 55.108, d.f. = 2. p < 0.005). (a) Open circles, Kladothrips arotrum; filled diamonds, Kladothrips antennatus. (b) Open circles, Teuchothrips ater; filled diamonds, Klambothrips oleariae. (c) Open circles, Haplothrips froggatti; filled diamonds, Odontothripiella aloba; open triangles, Dunatothrips vestitor. (d) Open circles, Kladothrips intermedius.