Symbiont selection via alcohol benefits fungus farming by ambrosia beetles

Ranger, Christopher M.; Biedermann, Peter H. W.; Phuntumart, Vipaporn; Beligala, Gayathri Udayangika; Ghosh, Satyaki; Palmquist, Debra E.; Mueller, R. J.; Barnett, Jenny; Schultz, Peter B.; Reding, Michael E.; Benz, J. Philipp

doi:10.1073/pnas.1716852115

Cited by 80 publications

(116 citation statements)

References 67 publications

Supporting

Mentioning

105

Contrasting

Unclassified

Order By: Relevance

“…The creation of a challenging gut environment through the ingestion of poison gland substances that is easier to endure if colonizing microbes are mutualists agrees with the theoretical concept of screening, as opposed to signalling, as a means of partner choice in cross-kingdom mutualisms (Archetti et al, 2011a, Archetti et al, 2011b, Biedermann and Kaltenpoth, 2014, Scheuring and Yu, 2012). Experimental evidence for screening is so far limited in insect-microbe associations (Innocent et al, 2018, Itoh et al, 2019, Ranger et al, 2018), but the results of our study provide support for the prediction that screening is more likely to evolve if a host’s challenging environment is derived from defence traits against parasites (Archetti et al, 2011a, Archetti et al, 2011b). Altogether, our study provides evidence that the well-established cross talk between the immune system and gut associated microbes in vertebrates and invertebrates (Chu and Mazmanian, 2013, Rakoff-Nahoum et al, 2004, Slack et al, 2009, Watnick and Jugder, 2020, Xiao et al, 2019) holds for a broader range of immune defence traits ( sensu Otti et al, 2014) and might be realized not only through signalling but also screening.…”

Section: Resultssupporting

confidence: 72%

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

Tragust

Herrmann

Häfner

et al. 2020

Preprint

View full text Add to dashboard Cite

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...

show abstract

Section: Resultssupporting

confidence: 72%

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

Tragust

Herrmann

Häfner

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Ethanol acts as a chemical indicator of weakened trees (Kelsey, ) and also benefits the colonization success of ambrosia beetles by promoting the growth of their fungal gardens (Ranger et al ., ). A variety of abiotic and biotic stressors can induce the production and emission of ethanol by trees, including flood and drought stress, frost injury, girdling, impaired root function, root and crown disturbance, pollutants, and pathogens (Kimmerer & Kozlowski, ; Kimmerer & MacDonald, ; Kelsey & Joseph, ; Kelsey et al ., ; Ranger et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Freeze stress of deciduous trees induces attacks by opportunistic ambrosia beetles

Ranger

Schultz

Frank

et al. 2018

Agri and Forest Entomology

Self Cite

View full text Add to dashboard Cite

1 A broad host range and the utilization of living but weakened trees contribute, in part, to the invasion success of ambrosia beetles (Curculionidae: Scolytinae). The present study assessed the capability of freeze stress to induce attacks by ambrosia beetles. 2 Freeze stress predisposed Cercis canadensis L., Cornus florida L., Malus pumilaMill. and Styrax japonicus Sieb. to attack under field conditions, although no attacks occurred on untreated trees. More attacks occurred on freeze-stressed versus flood-stressed M. pumila in Virginia but not for S. japonicus in Ohio. Attacks on flooded trees were skewed towards the base of the trunk, whereas attacks on freeze-stressed trees mainly occurred around the upper regions of the trunk and into the branches. The predominant species recovered were Anisandrus maiche Stark and Xylosandrus germanus (Blandford) in Ohio, and Xylosandrus crassiusculus (Motschulsky) in Virginia. 3 Ethanol emissions from trunks of S. japonicus were detected by solid phase microextraction-gas chromatography-mass spectrometry at 1 day after imposing freeze stress, peaking 4 days after injury. 4 Trees with an intolerance of freeze stress are predicted to be vulnerable to attack, especially when subjected to mild winter temperatures followed by late-spring freezes. Freeze stress could thereby facilitate the destructiveness of exotic ambrosia beetles.

show abstract

“…Furthermore, Egonyu & Torto (2018) demonstrated that ethanol is also a dominant component of F. solani and could induce an attraction towards X. compactus females, stimulating the infestation of plants suitable for fungal growth. Moreover, in a recent study, Ranger et al (2018) showed that ambrosia beetles can take advantage of an ethanol-rich substrate for growing their coevolved fungal symbionts.…”

Section: Introductionmentioning

confidence: 99%

First data on the flight activity and distribution of the ambrosia beetle Xylosandrus compactus (Eichhoff) on carob trees in Sicily

et al. 2019

View full text Add to dashboard Cite

The factors influencing the entry and the spread of the black twig borer, Xylosandrus compactus (Eichhoff), in the Mediterranean environment have not yet been characterized. Following its first report in Sicily (southern Italy) in 2016, and due to the high level of damage it causes on one of its host plants (Ceratonia siliqua L.), the flight activity of the pest was studied there. Monitoring was performed from spring 2017 to summer 2018 by exposing red cross‐shaped sticky traps combined with ethanol‐baited bottle traps. The three monitored sites were selected at different altitudes, representing the southern Mediterranean environment where the carob tree is widely present. The results showed that the pest populations are influenced by climatic factors. In particular, the first adults were caught when the maximum daily temperatures were stably higher than 20°C over several continuous days. Xylosandrus compactus occurred widely in the monitored territory and was continuously caught from spring to autumn. Furthermore, the traps used proved to be effective for intercepting the spring flight of the overwintering females. Moreover, the ability of the beetle to spread from a new infested area was also studied. It seems that the pest can spread more than 8 km from the last infested site of the previous flying season. It was not present above altitudes of 400 m in the conditions of the present study. This study represents the first step to better understand the behaviour of X. compactus in a newly colonized environment.

show abstract

Symbiont selection via alcohol benefits fungus farming by ambrosia beetles

Cited by 80 publications

References 67 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

Freeze stress of deciduous trees induces attacks by opportunistic ambrosia beetles

First data on the flight activity and distribution of the ambrosia beetle Xylosandrus compactus (Eichhoff) on carob trees in Sicily

Contact Info

Product

Resources

About