Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Cheng, Daifeng, Chen, Siqi, Huang, Yuquan, Pierce, Naomi E., Riegler, Markus, Yang, Fan, Zeng, Ling, Lu, Yongyue, Liang, Guangwen, Xu, Yijuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668852/
https://www.ncbi.nlm.nih.gov/pubmed/31323076
http://dx.doi.org/10.1371/journal.ppat.1007942
_version_ 1783440278861905920
author Cheng, Daifeng
Chen, Siqi
Huang, Yuquan
Pierce, Naomi E.
Riegler, Markus
Yang, Fan
Zeng, Ling
Lu, Yongyue
Liang, Guangwen
Xu, Yijuan
author_facet Cheng, Daifeng
Chen, Siqi
Huang, Yuquan
Pierce, Naomi E.
Riegler, Markus
Yang, Fan
Zeng, Ling
Lu, Yongyue
Liang, Guangwen
Xu, Yijuan
author_sort Cheng, Daifeng
collection PubMed
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.
format Online
Article
Text
id pubmed-6668852
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-66688522019-08-06 Symbiotic microbiota may reflect host adaptation by resident to invasive ant species Cheng, Daifeng Chen, Siqi Huang, Yuquan Pierce, Naomi E. Riegler, Markus Yang, Fan Zeng, Ling Lu, Yongyue Liang, Guangwen Xu, Yijuan PLoS Pathog Research Article 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. Public Library of Science 2019-07-19 /pmc/articles/PMC6668852/ /pubmed/31323076 http://dx.doi.org/10.1371/journal.ppat.1007942 Text en https://creativecommons.org/publicdomain/zero/1.0/ This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
Cheng, Daifeng
Chen, Siqi
Huang, Yuquan
Pierce, Naomi E.
Riegler, Markus
Yang, Fan
Zeng, Ling
Lu, Yongyue
Liang, Guangwen
Xu, Yijuan
Symbiotic microbiota may reflect host adaptation by resident to invasive ant species
title Symbiotic microbiota may reflect host adaptation by resident to invasive ant species
title_full Symbiotic microbiota may reflect host adaptation by resident to invasive ant species
title_fullStr Symbiotic microbiota may reflect host adaptation by resident to invasive ant species
title_full_unstemmed Symbiotic microbiota may reflect host adaptation by resident to invasive ant species
title_short Symbiotic microbiota may reflect host adaptation by resident to invasive ant species
title_sort symbiotic microbiota may reflect host adaptation by resident to invasive ant species
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668852/
https://www.ncbi.nlm.nih.gov/pubmed/31323076
http://dx.doi.org/10.1371/journal.ppat.1007942
work_keys_str_mv AT chengdaifeng symbioticmicrobiotamayreflecthostadaptationbyresidenttoinvasiveantspecies
AT chensiqi symbioticmicrobiotamayreflecthostadaptationbyresidenttoinvasiveantspecies
AT huangyuquan symbioticmicrobiotamayreflecthostadaptationbyresidenttoinvasiveantspecies
AT piercenaomie symbioticmicrobiotamayreflecthostadaptationbyresidenttoinvasiveantspecies
AT rieglermarkus symbioticmicrobiotamayreflecthostadaptationbyresidenttoinvasiveantspecies
AT yangfan symbioticmicrobiotamayreflecthostadaptationbyresidenttoinvasiveantspecies
AT zengling symbioticmicrobiotamayreflecthostadaptationbyresidenttoinvasiveantspecies
AT luyongyue symbioticmicrobiotamayreflecthostadaptationbyresidenttoinvasiveantspecies
AT liangguangwen symbioticmicrobiotamayreflecthostadaptationbyresidenttoinvasiveantspecies
AT xuyijuan symbioticmicrobiotamayreflecthostadaptationbyresidenttoinvasiveantspecies