4.5 Article

Pathogen evasion of social immunity

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NATURE ECOLOGY & EVOLUTION
卷 7, 期 3, 页码 450-+

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NATURE PORTFOLIO
DOI: 10.1038/s41559-023-01981-6

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Social insects groom nestmates as a defense against pathogens. In this study, researchers found that this grooming behavior selects for fungi to produce more spores, but with lower virulence and detectability, suggesting pathogen adaptation to social immunity.
Treating sick group members is a hallmark of collective disease defence in vertebrates and invertebrates alike. Despite substantial effects on pathogen fitness and epidemiology, it is still largely unknown how pathogens react to the selection pressure imposed by care intervention. Using social insects and pathogenic fungi, we here performed a serial passage experiment in the presence or absence of colony members, which provide social immunity by grooming off infectious spores from exposed individuals. We found specific effects on pathogen diversity, virulence and transmission. Under selection of social immunity, pathogens invested into higher spore production, but spores were less virulent. Notably, they also elicited a lower grooming response in colony members, compared with spores from the individual host selection lines. Chemical spore analysis suggested that the spores from social selection lines escaped the caregivers' detection by containing lower levels of ergosterol, a key fungal membrane component. Experimental application of chemically pure ergosterol indeed induced sanitary grooming, supporting its role as a microbe-associated cue triggering host social immunity against fungal pathogens. By reducing this detection cue, pathogens were able to evade the otherwise very effective collective disease defences of their social hosts. Social insects often groom nestmates as an anti-pathogen behaviour, providing social immunity. Here the authors show that anti-fungal grooming behaviour by ants selects for the fungus to produce more but less-virulent and less-detectable spores, suggesting pathogen adaptation to social immunity.

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