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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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. |
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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.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1007942</identifier><identifier>PMID: 31323076</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>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)</subject><ispartof>PLoS pathogens, 2019-07, Vol.15 (7), p.e1007942-e1007942</ispartof><rights>COPYRIGHT 2019 Public Library of Science</rights><rights>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 public domain dedication: https://creativecommons.org/publicdomain/zero/1.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c606t-bc3709a93bf6fade760e540b2960c5956cc4a383f97cb3dd4d88e9383bd04bd13</citedby><cites>FETCH-LOGICAL-c606t-bc3709a93bf6fade760e540b2960c5956cc4a383f97cb3dd4d88e9383bd04bd13</cites><orcidid>0000-0001-7363-431X ; 0000-0003-1304-6289</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668852/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668852/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31323076$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cheng, Daifeng</creatorcontrib><creatorcontrib>Chen, Siqi</creatorcontrib><creatorcontrib>Huang, Yuquan</creatorcontrib><creatorcontrib>Pierce, Naomi E</creatorcontrib><creatorcontrib>Riegler, Markus</creatorcontrib><creatorcontrib>Yang, Fan</creatorcontrib><creatorcontrib>Zeng, Ling</creatorcontrib><creatorcontrib>Lu, Yongyue</creatorcontrib><creatorcontrib>Liang, Guangwen</creatorcontrib><creatorcontrib>Xu, Yijuan</creatorcontrib><title>Symbiotic microbiota may reflect host adaptation by resident to invasive ant species</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><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.</description><subject>Adaptation, Physiological</subject><subject>Analysis</subject><subject>Animal behavior</subject><subject>Animals</subject><subject>Ants - microbiology</subject><subject>Ants - physiology</subject><subject>Bacteria</subject><subject>Biology and Life Sciences</subject><subject>Carbohydrate metabolism</subject><subject>Carbohydrates</subject><subject>Colonies</subject><subject>Communities</subject><subject>Competition</subject><subject>Diet</subject><subject>Displays (Marketing)</subject><subject>Ecological effects</subject><subject>Ecology</subject><subject>Ecology and Environmental Sciences</subject><subject>Ecosystem</subject><subject>Ecosystem biology</subject><subject>Ecosystems</subject><subject>Entomology</subject><subject>Feeding Behavior</subject><subject>Fire ants</subject><subject>Genomes</subject><subject>Glucose metabolism</subject><subject>Health aspects</subject><subject>Host Microbial Interactions - physiology</subject><subject>Host-bacteria relationships</subject><subject>Hypotheses</subject><subject>Indigenous species</subject><subject>Interspecific</subject><subject>Introduced Species</subject><subject>Invasive insects</subject><subject>Invasive species</subject><subject>Medicine and Health Sciences</subject><subject>Metabolism</subject><subject>Microbiota</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Microbiota - physiology</subject><subject>Nitrogen (Chemical element)</subject><subject>Nitrogen isotopes</subject><subject>Nonnative species</subject><subject>Physical Sciences</subject><subject>Proteins</subject><subject>Provisioning</subject><subject>Social Sciences</subject><subject>Solenopsis invicta</subject><subject>Species Specificity</subject><subject>Sugar</subject><subject>Supervision</subject><subject>Symbiosis - physiology</subject><subject>Tapinoma melanocephalum</subject><subject>Thiamine</subject><subject>Vitamin B complex</subject><subject>Vitamin B Complex - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cheng, Daifeng</au><au>Chen, Siqi</au><au>Huang, Yuquan</au><au>Pierce, Naomi E</au><au>Riegler, Markus</au><au>Yang, Fan</au><au>Zeng, Ling</au><au>Lu, Yongyue</au><au>Liang, Guangwen</au><au>Xu, Yijuan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Symbiotic microbiota may reflect host adaptation by resident to invasive ant species</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2019-07-01</date><risdate>2019</risdate><volume>15</volume><issue>7</issue><spage>e1007942</spage><epage>e1007942</epage><pages>e1007942-e1007942</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>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.</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 |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-21T14%3A33%3A30IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Symbiotic%20microbiota%20may%20reflect%20host%20adaptation%20by%20resident%20to%20invasive%20ant%20species&rft.jtitle=PLoS%20pathogens&rft.au=Cheng,%20Daifeng&rft.date=2019-07-01&rft.volume=15&rft.issue=7&rft.spage=e1007942&rft.epage=e1007942&rft.pages=e1007942-e1007942&rft.issn=1553-7374&rft.eissn=1553-7374&rft_id=info:doi/10.1371/journal.ppat.1007942&rft_dat=%3Cgale_plos_%3EA595183159%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2274435962&rft_id=info:pmid/31323076&rft_galeid=A595183159&rft_doaj_id=oai_doaj_org_article_36c240c2724f4383a0c6b9e189ac3fb8&rfr_iscdi=true |