Abstract
Animals living in large colonies are especially vulnerable to infectious pathogens and may therefore have evolved additional defences. Eusocial insects supplement their physiological immune systems with ‘social immunity’, a set of adaptations that impedes the entrance, establishment, and spread of pathogens in the colony. We here find that honey bee workers (Apis mellifera) that had been experimentally immune-challenged with bacterial lipopolysaccharide (LPS) often exited the hive and subsequently died; some individuals were dragged out by other workers, while others appeared to leave voluntarily. In a second experiment, we found that healthy workers treated with surface chemicals from LPS-treated bees were evicted from the hive more often than controls, indicating that immune-challenged bees produce chemical cues or signals that elicit their eviction. Thirdly, we observed pairs of bees under lab conditions, and found that pairs spent more time apart when one member of the pair had received LPS, relative to controls. Our findings suggest that immune-challenged bees altruistically banish themselves, and that workers evict sick individuals which they identify using olfactory cues, putatively because of (kin) selection to limit the spread of pathogens within colonies.Significance statementJust as in humans, animals living in large groups must contend with infectious diseases. Social insects such as honey bees have evolved a range of behavioural and organisational defences against disease, collectively termed ‘social immunity’. Here, we describe experiments in which we introduced immune-stimulated bee workers into hives to study social immunity. We find that bees that were wounded or immune-challenged were more likely to leave the hive—resulting in their death—compared to healthy controls. Some of the bees leaving the hive were ejected by other workers, while some left the hive seemingly by choice: we thus find evidence for both ‘banishment’ of immune-challenged bees and self-imposed exile. Furthermore, using experiments transferring chemical signals between healthy and immune stimulated bees, we establish that the latter are identified for banishment by the chemicals present on their body surface.
Highlights
Colony-living animals face a heightened risk of infectious disease, which can spread rapidly when conspecifics are in frequent contact (Naug and Camazine 2002; Pie et al 2004)
One might predict highly social species to have evolved stronger immune systems than their more solitary relatives. This prediction has received only partial support in the eusocial Hymenoptera, and some evidence suggests that eusocial species have comparatively weak immune systems
Inspired by the lack of a clear strengthening of the immune system among eusocial taxa, as well as observations of their behaviour, researchers have proposed that eusocial insects combat pathogens using ‘social immunity’, which provides a complementary defence system that reduces pathogen exposure and thereby weakens selection for stronger individual immune defences (Cremer et al 2007)
Summary
Colony-living animals face a heightened risk of infectious disease, which can spread rapidly when conspecifics are in frequent contact (Naug and Camazine 2002; Pie et al 2004). One might predict highly social species to have evolved stronger immune systems than their more solitary relatives. This prediction has received only partial support in the eusocial Hymenoptera, and some evidence suggests that eusocial species have comparatively weak immune systems. Asian honey bee larvae (Apis cerana) were found to die more quickly upon exposure to parasitic mites than a non-coevolved species of honey bee (A. mellifera), leading the authors to hypothesise that A. cerana has evolved ‘social apoptosis’ in order to limit within-colony parasite transmission (Page et al 2016). Pull et al (2018) observed ant workers identifying infected ant pupae via chemical cues, and spraying them with antimicrobial poison, in a similar manner to how diseased cells are removed by the immune system in the bodies of multicellular organisms Asian honey bee larvae (Apis cerana) were found to die more quickly upon exposure to parasitic mites than a non-coevolved species of honey bee (A. mellifera), leading the authors to hypothesise that A. cerana has evolved ‘social apoptosis’ in order to limit within-colony parasite transmission (Page et al 2016). Pull et al (2018) observed ant workers identifying infected ant pupae via chemical cues, and spraying them with antimicrobial poison, in a similar manner to how diseased cells are removed by the immune system in the bodies of multicellular organisms
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