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Collective disease defence and pathogen detection abilities in ant societies: <br/>a chemo-neuro-immunological approach

Final Report Summary - PATHOGEN DETECTORS (Collective disease defence and pathogen detection abilities in ant societies: <br/>a chemo-neuro-immunological approach)

Pathogens causing infectious diseases have major impact on all organisms, thus driving the evolution of costly individual disease defences. Organisms living in societies, such as ants, have evolved additional collective disease defences to counteract elevated risks of pathogen transmission, that result from living close together and frequently interacting with related individuals. Fundamental to both individual and collective disease defences, is a rapid detection of, and response to, incoming pathogens, as only this allows prevention, or containment, of infectious disease outbreaks. The overarching object of the project was thus to identify and characterize the nature and origin of cues that elicit collective antiseptic behaviours in ants. The invasive garden ant, Lasius neglectus, and the insect pathogenic fungus, Metharizium brunneum, were used as model system to explore these questions.
An immediate behavioural response to pathogen-exposed individuals was indeed found in ant societies, with grooming being up-regulated at both the individual level (self-grooming by exposed workers; [Theis, Ugelvig, Marr and Cremer, in preparation; Konrad, Vyleta, Theis, Tragust, Stock, Klatt, Drescher, Marr, Ugelvig and Cremer, 2012]) and the colony level (allogrooming received from healthy workers; [Tragust, Ugelvig, Chapuisat, Heinze and Cremer, 2013a]). We could show that grooming of pathogen-exposed brood not only function to mechanically remove pathogenic agents, but also to chemically disinfect the body surface of the brood, through application poison [Tragust, Mitteregger, Barone, Konrad, Ugelvig and Cremer, 2013b]. Only if this treatment fails, workers will remove incurable brood from the nest thereby preventing sporulating cadavers to develop there [Tragust et al, 2013a].
The cues eliciting these collective antiseptic behaviours are likely to be of chemical nature. In the project we have thus focused on developing methods for our model system, in order to extract and analyse cuticular chemical profiles of pathogen-exposed and diseased individuals using gas chromatography-mass spectrometry (GC-MS). Applying state-of-the-art techniques from this field have allowed us to move beyond the largely non-volatile surface-bound compounds that so far received most attention in the context of social insect communication, to also analyse (semi-)volatile compounds. Through a combination of different experimental designs and pathogen exposure methods, we can now tease apart the origin of the chemical compounds, i.e. whether they stem from the pathogen or host alone, or the interaction between the two when the pathogen grows on and in the host. Moreover, the significance of particular compounds or fractions of profiles can be evaluated in behavioural assays that we specifically developed and optimised for this system. This includes an extended olfactometer set-up to test repellence or attraction at different odour concentrations. These assays can also be used to evaluate differences in odour perception among worker ants, and how such differences can affect the ability to efficiently perform antiseptic behaviours, with impacts at both the individual and colony level. The results from these experiments are still to be published.
In a review of the current literature [Ugelvig and Cremer, 2012] we explored to which extend the great invasiveness of some ant species, like the invasive garden ant, may be shaped by direct and indirect effects of their parasites in combination with their social lifestyle and thus collective disease defences. We highlight the importance of studying these effects in concert across scales (individual – colony – population) and include interactions between behavioural and genetic processes. This is crucial to be able to develop efficient management and biocontrol strategies.