Social immunity modulates competition between coinfecting pathogens

Abstract

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 antstheir social immunityinfluence 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.

Empirical Support for the Pattern of Competitive Exclusion between Insect Parasitic Fungi

“…It was assumed that host immunity was first inhibited by Metarhizium , which led to the mycosis of insects by the fast-growing saprophytes [ 54 , 55 ]. The coinfection of ants with different Metarhizium strains and species (i.e., M. robertsii and M. brunneum ) revealed that insect social immunity (sanitary care by grooming to reduce spore load) also affect the consequence of parasite competitions [ 56 ]. Thus, the host effect on competition can be species-dependent, which requires further investigation.…”

Superorganism Immunity: A Major Transition in Immune System Evolution

“…Additionally, this may confer improved tolerance to infections where the impact it has on the host is ameliorated, e.g., through increased food consumption (Almberg et al, 2015), leading eventually to reduced pathogen virulence. Pathogen evolution and diversity could be altered by simple social behaviors, such as grooming, leading to disrupted within-host pathogen dynamics during coinfections that result in altered pathogen communities and virulence (Milutinović et al, 2020). This could select for group-living if it positively affects host fitness.…”

Pathogen evasion of social immunity

“…We found that only the individual lines under current individual ant conditions caused high host mortality (Fig. 2a; Bayesian Multi Level Model, 0.44 mean probability of dying, highest density interval individual, so that strains that are outcompeted in individual hosts can in some cases gain competitive advantage in social hosts 24 . By biasing the competitive outcome of pathogen-pathogen interactions, social immunity thus exerts a modulatory effect on co-infecting pathogens.…”

“…To experimentally assess the long-term selective effect of social immunity on co-infecting pathogens, we performed a serial passage experiment using six representatives of a natural population of pathogenic Metarhizium fungi 24,27 and the invasive Argentine ant, Linepithema humile. We subjected the ants to two different selection treatments, one excluding social immunity by keeping exposed ants individually, and the other with social immunity provided by two caregiving nestmates.…”

“…Pathogens that infect their hosts via attaching to and penetrating the body surface, such as many fungal pathogens 23 , are therefore under strong selection to counteract the negative impact that mutual grooming of their social hosts has on their fitness. Notably, although grooming uniformly reduces the number of spores that is able to successfully infect the host, the degree of this effect can vary between even closely related fungal species, depending on their specific infection properties 24 . Therefore, social immunity can differentially affect pathogen strains or species when their spores co-infect the same host Article https://doi.org/10.1038/s41559-023-01981-6…”