Abstract

In social insects, alerting nestmates to the presence of a pathogen should be critical for limiting its spread and initiating social mechanisms of defense. Here we show that subterranean termites use elevated vibratory alarm behavior to help prevent fatal fungal infections. The elevated alarm leads to elevated social hygiene. This requires that termites coalesce so that they can groom each other’s cuticular surfaces of contaminating conidial spores. Groups of 12 Reticulitermes flavipes workers varied in their response when immersed in conidia solutions of nine different strains of Metarhizium. Pathogen alarm displays of short 2–7-second bursts of rapid longitudinal oscillatory movement (LOM), observed over 12 min following a fungal challenge, were positively correlated with the time that workers spent aggregated together grooming each other. The frequency of these LOMs was inversely correlated with fatal fungal infections. The variation in fatalities appeared to be largely attributable to a differential response to Metarhizium brunneum and Metarhizium robertsii in the time spent in aggregations and the frequency of allogrooming. Isolated workers challenged with conidia did not display LOMs, which suggests that the alarm is a conditional social response. LOMs appear to help signal the presence of fungal pathogens whose virulence depends on the level of this emergency alert.

Highlights

  • An effective immune system requires a rapid response in order to curtail the replication and spread of a pathogen

  • This frontline strategy is especially important in the defense against microparasites such as Metarhizium, which is commonly encountered by insects that move through the soil [5]

  • The inverse correlation between Hazard ratios of death (HRs) and the time spent in aggregations was significant (Table 1, Figure 3) and allogrooming was significantly positively correlated with the time spent in aggregations (Table 1, Figure 4)

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Summary

Introduction

An effective immune system requires a rapid response in order to curtail the replication and spread of a pathogen. Groups are often better at surviving challenges with conidia than individuals apparently because allogrooming affords greater protection against infection than autogrooming (for example [3,4]) This frontline strategy is especially important in the defense against microparasites such as Metarhizium, which is commonly encountered by insects that move through the soil [5]. Its conidial spores attach and rapidly grow through the insect cuticle and, once inside the hemocoel, replicating fungal cells mask themselves from cellular and humoral defense mechanisms with the secretion of a collagenous coat [6] This evasive strategy appears to be effective against termites, which are less susceptible to fatal infections when exposed to a mutant strain that cannot produce the coat [7]

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