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.

Evolving communicative complexity: insights from rodents and beyond

“…If a social group's boundaries are well defined, then a simple head count is all that is needed. For all these reasons, it is not surprising that social group size is one of the most commonly studied attributes of social complexity and has been used in a variety of taxa [7,[28][29][30][31][32][33][34][35][36][37][38].…”

Social context-dependent immune gene expression in bumblebees (Bombus terrestris)

“…An increased antimicrobial response has been described for bees and Thysanoptera varying in the levels of social organisation (Stow et al 2007;Turnbull et al 2011). These studies indicate that selection might have increased the levels of antimicrobial activity in social species because of their increased risk of disease transmission.…”

“…Amongst the Thysanoptera, several species showing various degrees of group living exist. A positive correlation has been found between the group size and the production of antimicrobial substances (Turnbull et al 2011). Similarly, in bumblebees (B. terrestris) group size effects on the immune system have been shown (RuizGonzález et al 2009); workers kept in isolation had higher antimicrobial activity but lower phenoloxidase activity in their hemolymph than workers kept in groups of five individuals.…”

Antifungal activity in thrips soldiers suggests a dual role for this caste

“…We have isolated one fungal pathogen from the galls of Kladothrips arotrum Mound, Kladothrips antennatus Moulton and K. intermedius (C. Turnbull 2011, unpublished data) and pathogenic fungi have been invoked for the biological control of pest thrips [14]. The strength of antimicrobials may be correlated with increasing degree of sociality and group size [8,15] and social insects have been shown to host many kinds of microorganisms-both harmful and beneficial [16]suggesting prolonged coevolution [17]. Entomopathogens such as Cordyceps were already present when sociality first evolved [18].…”

“…(b) Antimicrobial responses Soldiers and dispersers from healthy galls of K. intermedius were washed to obtain cuticular antimicrobials using established methods [8]. As soldiers were the less numerous caste, we collected all of them from each gall and these were matched by an equal number of dispersers from that gall.…”