Pathogen evasion of social immunity

Abstract

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.

Frequent horizontal chromosome transfer between asexual fungal insect pathogens

“…Multiple independent transfers of accessory chrA from the ancestral M. robertsii R1-A to evolved M. robertsii R3 during an experimental co-infection of an ant host. A) Experimental procedure of the selection experiment performed by Stock et al (32). Argentine ants (green) were exposed to a mix of six strains – three M. robertsii and three M. brunneum – and kept either alone (individual treatment, n=10 replicate lines) or with two nestmates (grey; social treatment, n=10 replicate lines).…”

“…Argentine ants (green) were exposed to a mix of six strains – three M. robertsii and three M. brunneum – and kept either alone (individual treatment, n=10 replicate lines) or with two nestmates (grey; social treatment, n=10 replicate lines). The produced infectious spores were used to expose ants in ten serial infection cycles as described in (32). We here performed whole genome sequencing of the six ancestral and the individually- and socially-evolved strains at the end of the experiment.…”

“…Next, we wanted to understand the temporal dynamics of the horizontal transfers and whether recipient strains had a competitive advantage or disadvantage compared to the same strain without chrA. To this end, we performed a detailed analysis of the clone diversity at passages 1, 3, 5 and 10 testing the proportion of R3 spores with present versus absent chrA for the six above-mentioned R3-strains that had persisted until passage 10, plus another two that had persisted at least until passage 5, but had become outcompeted by passage 10 (R3-S1, R3-S8), see Stock et al (32). We found that chrA was transferred from R1 to R3 in five out of the eight selection lines (in all three individually-evolved, as well as in two of five of the socially-evolved) (Fig 2 A-B).…”

“…We used the six ancestral strains and the evolved lines of the fungal pathogens Metarhizium robertsii and M. brunneum obtained during the selection experiment performed by Stock et al (32). In this experiment, the six ancestral strains were mixed in equal amounts and used to experimentally co-infect Argentine ants, which subsequently were either kept alone (individual treatment (abbreviation: I)) or in the presence of two nestmates (social treatment (abbreviation: S)) over ten consecutive host infection cycles (passages).…”

“…In addition to their parasitic lifestyle in insects, some are also associated with plants as rhizosphere colonizers and root endophytes (31). Here we used a set of fungal strains derived from a selection experiment, in which Argentine ants ( Linepithema humile ) were co-infected with a mixture of six strains of M. robertsii and M. brunneum and then kept under conditions either allowing only the ant’s individual immune defenses to act, or both their individual and cooperative social defenses (32). By analyzing the ancestral and the evolved fungal strains resulting from that experiment we show that i) horizontal transfer of an accessory chromosome occurred frequently between two distinct strains of M. robertsii , and ii) only the accessory chromosome was transferred and spread through the population over ten host infection cycles depending on the presence or absence of the ant’s social immune defenses.…”