Abstract
Microbial pathogens are ancient selective agents that have driven many aspects of multicellular evolution, including genetic, behavioural, chemical and immune defence systems. It appears that fungi specialised to attack insects were already present in the environments in which social insects first evolved and we hypothesise that if the early stages of social evolution required antifungal defences, then covariance between levels of sociality and antifungal defences might be evident in extant lineages, the defences becoming stronger with group size and increasing social organisation. Thus, we compared the activity of cuticular antifungal compounds in thrips species (Insecta: Thysanoptera) representing a gradient of increasing group size and sociality: solitary, communal, social and eusocial, against the entomopathogen Cordyceps bassiana. Solitary and communal species showed little or no activity. In contrast, the social and eusocial species killed this fungus, suggesting that the evolution of sociality has been accompanied by sharp increases in the effectiveness of antifungal compounds. The antiquity of fungal entomopathogens, demonstrated by fossil finds, coupled with the unequivocal response of thrips colonies to them shown here, suggests two new insights into the evolution of thrips sociality: First, traits that enabled nascent colonies to defend themselves against microbial pathogens should be added to those considered essential for social evolution. Second, limits to the strength of antimicrobials, through resource constraints or self-antibiosis, may have been overcome by increase in the numbers of individuals secreting them, thus driving increases in colony size. If this is the case for social thrips, then we may ask: did antimicrobial traits and microbes such as fungal entomopathogens play an integral part in the evolution of insect sociality in general?
Highlights
Animal aggregations attract many kinds of enemies including predators and parasites, and this is especially the case for the social insects [1,2,3]
There was a suggestion that extracts from the communal species, Teucothrips ater, showed a little antifungal activity in the range of 25–50 thrips-equivalents, perhaps approximating natural densities within curled leaves
The social Kladothrips arotrum and K. antennatus, and the eusocial K. intermedius consistently exhibited stronger antifungal activity. As these and all other social and eusocial thrips species belong to the single genus Kladothrips, it might be argued that antifungal activity is somehow related to inhabiting Acacia galls rather than to social organisation
Summary
Animal aggregations attract many kinds of enemies including predators and parasites, and this is especially the case for the social insects [1,2,3]. Microbial pathogens were ancient selective agents that influenced many fundamental aspects of multicellular evolution [4] and instigated, or at least maintained, major defence mechanisms such as sexual reproduction and immune systems [5,6,7,8] With this in mind, we wondered if specialised fungal pathogens were among the most ancient enemies of social insects perhaps because they were common, pre-existing soil-dwelling species. If the early enemies of insect societies were microbial, the continued assembly of social traits may have been possible only in the presence of strong antimicrobials In this context, we assayed the anti-fungal activity of 6 thrips species against the native entomopathogen Cordyceps bassiana according to group size and the degree and type of social organisation (solitary, communal, social and eusocial). Our hypothesis was that there is a correlation between anti-Cordyceps activity and group size and that Cordyceps inhibition, measured from equivalent numbers of individuals, would be greatest in species that formed colonies, whether social or eusocial
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