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Social immune systems: collective disease defence in insect societies

Final Activity Report Summary - COLLECTIVE IMMUNITY (Social immune systems: collective disease defence in insect societies)

Group living has many benefits when compared to a solitary lifestyle. Cooperation can increase the efficiency of brood care, foraging, or anti-predator defences. These benefits are considered as one of the main reasons why for example social insects - the ants and termites, some bees and wasps - have become dominant species in many habitats. However, living in social groups also has drawbacks: infectious diseases can potentially spread more easily between group members, when compared to solitary living individuals. The reasons for this are that, firstly, transmission is more likely to happen when individuals live at high densities and have frequent social contacts and, secondly, that group members are often close relatives and thus susceptible to the same parasite infections. Hence, it is expected that social groups offer particularly amenable conditions for the spread of infectious diseases, but they should also have evolved several tactics to counter this threat.

Social insect societies have indeed evolved a great variety of anti-parasite defences that comprise both hygienic behaviours and the physiological immune systems of all group members. Aim of this project was to investigate these collective immune defences in several ant species that differ in their social and genetic organisation, both within and between species. It was studied how these different ant societies recognize the presence of parasites and diseased group members in their colonies, and which defence mechanisms they employ to prevent disease spread between group members.

One result of the study was that individual ant workers that were infected with fungal spores spent less time inside their nest and that they perform less brood care than their healthy nestmates. This behaviour does not seem to be triggered by any antagonistic behaviour by the healthy group members, but rather seems to represent an altruistic behaviour by the sick individual itself, by which disease transmission in the colony is effectively reduced. Also, healthy group members do not only show hygienic behaviour directed towards the incoming infected individual, but also increase their own sanitation behaviour, as well as the cleaning of hitherto uninfected group members. Many of the behaviours shown in a social insect colony are therefore not only activated when the individuals themselves get infected, but already when another group members gets in contact with a contagious item, and are thus of prophylactic nature. In addition to this behavioural disease prophylaxis, social insect colonies can also show physiological changes that prevent parasite infections to spread within the colony.

These collective defences are very efficient and whilst providing a great benefit to the infected individual - exposed individuals typically have much higher survival chances when reared within their social group than in isolation - the costs for the individuals performing the sanitation behaviour seem to be very low, as transmission rates from infected towards naïve nestmates could be shown to be nearly negligible. This is also because ants try to avoid contact with infectious items with great efficiency. They cannot only detect the presence of diseased brood in their colonies, but already remove brood that has been exposed to fungal spores, but does not yet show any signs of disease. In this, the ants can differentiate between dead and live, infectious, spores and explicitly remove the brood contaminated with live spores.

However, this recognition capacity is impaired, when the genetic diversity of the group is reduced by inbreeding, suggesting that genetic variation is an important factor to efficiently recognize and control diseases in ant societies. This is an important result also for the management of ecosystems, as many suffer from a strong reduction of genetic diversity as a result of, for example, habitat fragmentation or species introductions.