Symbiotic microbiota may reflect host adaptation by resident to invasive ant species

Exotic invasive species can influence the behavior and ecology of native and resident species, but these changes are often overlooked. Here we hypothesize that the ghost ant, Tapinoma melanocephalum, living in areas that have been invaded by the red imported fire ant, Solenopsis invicta, displays be...

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Veröffentlicht in:PLoS pathogens 2019-07, Vol.15 (7), p.e1007942-e1007942
Hauptverfasser: Cheng, Daifeng, Chen, Siqi, Huang, Yuquan, Pierce, Naomi E, Riegler, Markus, Yang, Fan, Zeng, Ling, Lu, Yongyue, Liang, Guangwen, Xu, Yijuan
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container_issue 7
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container_title PLoS pathogens
container_volume 15
creator Cheng, Daifeng
Chen, Siqi
Huang, Yuquan
Pierce, Naomi E
Riegler, Markus
Yang, Fan
Zeng, Ling
Lu, Yongyue
Liang, Guangwen
Xu, Yijuan
description Exotic invasive species can influence the behavior and ecology of native and resident species, but these changes are often overlooked. Here we hypothesize that the ghost ant, Tapinoma melanocephalum, living in areas that have been invaded by the red imported fire ant, Solenopsis invicta, displays behavioral differences to interspecific competition that are reflected in both its trophic position and symbiotic microbiota. We demonstrate that T. melanocephalum workers from S. invicta invaded areas are less aggressive towards workers of S. invicta than those inhabiting non-invaded areas. Nitrogen isotope analyses reveal that colonies of T. melanocephalum have protein-rich diets in S. invicta invaded areas compared with the carbohydrate-rich diets of colonies living in non-invaded areas. Analysis of microbiota isolated from gut tissue shows that T. melanocephalum workers from S. invicta invaded areas also have different bacterial communities, including a higher abundance of Wolbachia that may play a role in vitamin B provisioning. In contrast, the microbiota of workers of T. melanocephalum from S. invicta-free areas are dominated by bacteria from the orders Bacillales, Lactobacillales and Enterobacteriales that may be involved in sugar metabolism. We further demonstrate experimentally that the composition and structure of the bacterial symbiont communities as well as the prevalence of vitamin B in T. melanocephalum workers from S. invicta invaded and non-invaded areas can be altered if T. melanocephalum workers are supplied with either protein-rich or carbohydrate-rich food. Our results support the hypothesis that bacterial symbiont communities can help hosts by buffering behavioral changes caused by interspecies competition as a consequence of biological invasions.
doi_str_mv 10.1371/journal.ppat.1007942
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Here we hypothesize that the ghost ant, Tapinoma melanocephalum, living in areas that have been invaded by the red imported fire ant, Solenopsis invicta, displays behavioral differences to interspecific competition that are reflected in both its trophic position and symbiotic microbiota. We demonstrate that T. melanocephalum workers from S. invicta invaded areas are less aggressive towards workers of S. invicta than those inhabiting non-invaded areas. Nitrogen isotope analyses reveal that colonies of T. melanocephalum have protein-rich diets in S. invicta invaded areas compared with the carbohydrate-rich diets of colonies living in non-invaded areas. Analysis of microbiota isolated from gut tissue shows that T. melanocephalum workers from S. invicta invaded areas also have different bacterial communities, including a higher abundance of Wolbachia that may play a role in vitamin B provisioning. In contrast, the microbiota of workers of T. melanocephalum from S. invicta-free areas are dominated by bacteria from the orders Bacillales, Lactobacillales and Enterobacteriales that may be involved in sugar metabolism. We further demonstrate experimentally that the composition and structure of the bacterial symbiont communities as well as the prevalence of vitamin B in T. melanocephalum workers from S. invicta invaded and non-invaded areas can be altered if T. melanocephalum workers are supplied with either protein-rich or carbohydrate-rich food. Our results support the hypothesis that bacterial symbiont communities can help hosts by buffering behavioral changes caused by interspecies competition as a consequence of biological invasions.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>31323076</pmid><doi>10.1371/journal.ppat.1007942</doi><orcidid>https://orcid.org/0000-0001-7363-431X</orcidid><orcidid>https://orcid.org/0000-0003-1304-6289</orcidid><oa>free_for_read</oa></addata></record>
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subjects Adaptation, Physiological
Analysis
Animal behavior
Animals
Ants - microbiology
Ants - physiology
Bacteria
Biology and Life Sciences
Carbohydrate metabolism
Carbohydrates
Colonies
Communities
Competition
Diet
Displays (Marketing)
Ecological effects
Ecology
Ecology and Environmental Sciences
Ecosystem
Ecosystem biology
Ecosystems
Entomology
Feeding Behavior
Fire ants
Genomes
Glucose metabolism
Health aspects
Host Microbial Interactions - physiology
Host-bacteria relationships
Hypotheses
Indigenous species
Interspecific
Introduced Species
Invasive insects
Invasive species
Medicine and Health Sciences
Metabolism
Microbiota
Microbiota (Symbiotic organisms)
Microbiota - physiology
Nitrogen (Chemical element)
Nitrogen isotopes
Nonnative species
Physical Sciences
Proteins
Provisioning
Social Sciences
Solenopsis invicta
Species Specificity
Sugar
Supervision
Symbiosis - physiology
Tapinoma melanocephalum
Thiamine
Vitamin B complex
Vitamin B Complex - metabolism
Wolbachia - physiology
Workers (insect caste)
title Symbiotic microbiota may reflect host adaptation by resident to invasive ant species
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