Social network plasticity decreases disease transmission in a eusocial insect

Stroeymeyt, Nathalie; Grasse, Anna V.; Crespi, Alessandro; Mersch, Danielle; Cremer, Sylvia; Keller, Laurent

doi:10.1126/science.aat4793

Cited by 230 publications

(316 citation statements)

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“…Prophylactic acidification of the crop lumen after feeding in C. floridanus might therefore act as an important barrier to disease spread within the colony and alleviate the cost of sharing pathogen contaminated food (Onchuru et al, 2018, Salem et al, 2015). Together with other parasite defence traits in social insect societies (Cremer et al, 2007, Stroeymeyt et al, 2018), acidification of crop lumens likely effectively counteracts the generally increased risk of pathogen exposure and transmission associated with group-living (Alexander, 1974, Boomsma et al, 2005, Kappeler et al, 2015)…”

Section: Resultsmentioning

confidence: 99%

Formicine ants swallow their highly acidic poison for gut microbial selection and control

Tragust

Herrmann

Häfner

et al. 2020

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12Animals continuously encounter microorganisms that are essential for health or cause disease. 13 They are thus challenged to control harmful microbes while allowing acquisition of beneficial 14 microbes, a challenge that is likely especially important concerning microbes in food and in 15 animals such as social insects that exchange food among colony members. Here we show that 16 formicine ants actively swallow their antimicrobial, highly acidic poison gland secretions 17 after feeding. The ensuing creation of an acidic environment in the stomach, the crop, 18 improves individual survival in the face of pathogen contaminated food and limits disease 19 transmission during mutual food exchange. At the same time, crop acidification selectively 20 allows acquisition and colonization by known bacterial gut associates. The results of our 21 study suggest that swallowing of acidic poison gland secretions acts as a microbial filter in 22 formicine ants and indicate a potentially widespread but so far underappreciated dual role of 23 antimicrobials in host-microbe interactions. 24 25 85 5 experimental manipulation of poison gland access, and behavioural observations. In loss of 86 poison gland function experiments, we then investigate whether analogous to acidic stomachs 87 of higher vertebrates and acidic midgut regions in the fruit fly, swallowing of poison gland 88 substances can serve gut microbial control and prevent bacterial pathogen infection and 89 transmission. Finally, we explore whether swallowing of poison gland substances acts as a 90 microbial filter that is permissible to gut colonization of bacteria from the family 91 Acetobacteracea. 92 93 Results and Discussion 94To reveal whether poison gland secretions are swallowed during acidopore grooming, we 95 monitored acidity levels in the crop lumen of the Florida carpenter ant Camponotus floridanus 96 at different time points after feeding them 10% honey water (pH = 5). We found that over 97 time, the crop lumen became increasingly acidic, reaching highly acidic values 48h after 98 feeding (median pH = 2; 95% CI: 1.5-3.4), whilst renewed access to food after 48h restored 99 the pH to levels recorded after the first feeding trial ( Fig. 1a; LMM, LR-test, χ 2 = 315.18, df = 100 3, P < 0.001; Westfall corrected post-hoc comparisons: 0+4h vs. 48h+4h: P = 0.317, all other 101 comparisons: P < 0.001). This acidification was limited to the crop and did not extend to the 102 midgut (Fig. 1figure supplement 1; pH-measurements at four points along the midgut 24h 103 after access to 10% honey-water; mean ± se; midgut position 1 = 5.08 ± 0.18, midgut position 104 2 = 5.28 ± 0.17, midgut position 3 = 5.43 ± 0.16, midgut position 4 = 5.31 ± 0.19). Prevention 105 of acidopore grooming in C. floridanus ants for 24h after feeding resulted in a significantly 106 diminished acidification of the crop lumen (Fig. 1b; LMM, LR-test, χ 2 = 44.68, df = 1, P < 107 0.001), a result that was invariably obtained in a comparative survey across seven formicine 108 ant species (g...

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Section: Resultsmentioning

confidence: 99%

Formicine ants swallow their highly acidic poison for gut microbial selection and control

Tragust

Herrmann

Häfner

et al. 2020

Preprint

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“…Tracking the effects of sickness behaviour on a dynamic social network requires large datasets with temporal and spatial resolutions that are high enough to be ecologically useful. Automated tracking of animal associations typically occurs in the lab [1] or at specific field locations such as feeders or nest boxes [2]. Proximity sensors by contrast can measure association times and durations, at high spatial and temporal resolution, among free-ranging animals at any location [5].…”

Section: Introductionmentioning

confidence: 99%

Sickness behaviour reduces network centrality in wild vampire bats

Ripperger

Stockmaier

Carter

2020

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11Sickness behaviours, like lethargy, can slow the spread of pathogens across a social network. 12We conducted a field experiment to investigate how sickness behaviour reduces individual 13 connectedness in a high-resolution dynamic social network. We captured adult female vampire 14 bats (Desmodus rotundus) from a wild roost. To create 'sick' bats, we injected a random half of 15 the bats (n=16) with the immune-challenging substance, lipopolysaccharide, and injected 16 control bats with saline (n=15). Over the next three days, we used proximity sensors to 17 continuously track their associations under natural conditions. The 'sick' bats showed a clear 18 decrease in social connectedness (degree, strength, and eigenvector centrality). Bats in the 19 control group encountered fewer 'sick' bats and also spent less time near them. These effects 20 varied by time of day and declined over 48 hours. High-resolution proximity data allow 21 researchers to define network connections based on how a pathogen spreads (e.g. the 22 minimum contact time or distance for transmission). We therefore show how the estimate of the 23 sickness effect changes as network ties are defined using varying distances and durations of 24 association. Tracking the effects of sickness behaviour on high-resolution dynamic social 25 .

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“…Experimental setups including automated triggers (e.g., acoustic playbacks or other sensory cues) might easily be integrated and direct proximity sensing will bring exciting research opportunities. Such setups will allow to study the effect of social network dynamics on phenomena such as transmission of social information 30 and pathogens 38 , and key ecosystem functions such as pollination and seed dispersal 39 .…”

Section: Discussionmentioning

confidence: 99%

Thinking small: next-generation sensor networks close the size gap in vertebrate biologging

Ripperger

Carter

Page³

et al. 2019

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AbstractRecent advances in animal tracking technology have ushered in a new era in biologging. However, the considerable size of many sophisticated biologging devices restricts their application to larger animals, while old-fashioned techniques often still represent the state-of-the-art for studying small vertebrates. In industrial applications, low-power wireless sensor networks fulfill requirements similar to those needed to monitor animal behavior at high resolution and at low tag weight. We developed a wireless biologging network (WBN), which enables simultaneous direct proximity sensing, high-resolution tracking, and long-range remote data download at tag weights of one to two grams. Deployments to study wild bats created social networks and flight trajectories of unprecedented quality. Our developments highlight the vast capabilities of WBNs and their potential to close an important gap in biologging: fully automated tracking and proximity sensing of small animals, even in closed habitats, at high spatial and temporal resolution.

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Social network plasticity decreases disease transmission in a eusocial insect

Cited by 230 publications

References 55 publications

Formicine ants swallow their highly acidic poison for gut microbial selection and control

Formicine ants swallow their highly acidic poison for gut microbial selection and control

Sickness behaviour reduces network centrality in wild vampire bats

Thinking small: next-generation sensor networks close the size gap in vertebrate biologging

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