Social immunity modulates competition between coinfecting pathogens

• Published in: Ecology letters 2020-03, Vol.23 (3), p.565-574
• Main Authors: Milutinović, Barbara, Stock, Miriam, Grasse, Anna V., Naderlinger, Elisabeth, Hilbe, Christian, Cremer, Sylvia, Pinter‐Wollman, Noa
• Format: Article
• Language: English
• Subjects: Animals; Ants; Argentine ants; Cadavers; Competition; Grooming; Group dynamics; Host-Pathogen Interactions; immune‐mediated competition; Immunity; Infections; infectious disease; Mathematical models; Metarhizium; Metarhizium fungus; multiple infections; pathogen competition; pathogen diversity; Pathogens; Social Behavior; Social factors; social insects; Social interactions; Sporulation; Virulence
• ISSN: 1461-023X; 1461-0248
• DOI: 10.1111/ele.13458

Coinfections with multiple pathogens can result in complex within‐host dynamics affecting virulence and transmission. While multiple infections are intensively studied in solitary hosts, it is so far unresolved how social host interactions interfere with pathogen competition, and if this depends on coinfection diversity. We studied how the collective disease defences of ants – their social immunity – influence pathogen competition in coinfections of same or different fungal pathogen species. Social immunity reduced virulence for all pathogen combinations, but interfered with spore production only in different‐species coinfections. Here, it decreased overall pathogen sporulation success while increasing co‐sporulation on individual cadavers and maintaining a higher pathogen diversity at the community level. Mathematical modelling revealed that host sanitary care alone can modulate competitive outcomes between pathogens, giving advantage to fast‐germinating, thus less grooming‐sensitive ones. Host social interactions can hence modulate infection dynamics in coinfected group members, thereby altering pathogen communities at the host level and population level. When hosts are coinfected with multiple pathogens, their immune systems can interfere with the pathogen competition within their bodies, providing advantage to one pathogen over the other. Using ants and their fungal pathogens, we here describe ‘socially mediated competition’ as a similar phenomenon at the level of social groups of hosts. We show that social interactions between hosts have the capacity to modulate pathogen competition dynamics within hosts, altering success of coinfecting pathogen species and inducing changes in pathogen diversity at both, the host level and the community level.