orco Mutagenesis Causes Loss of Antennal Lobe Glomeruli and Impaired Social Behavior in Ants
Life inside ant colonies is orchestrated with diverse pheromones, but it is not clear how ants perceive these social signals. It has been proposed that pheromone perception in ants evolved via expansions in the numbers of odorant receptors (ORs) and antennal lobe glomeruli. Here, we generate the fir...
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Veröffentlicht in: | Cell 2017-08, Vol.170 (4), p.727-735.e10 |
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creator | Trible, Waring Olivos-Cisneros, Leonora McKenzie, Sean K. Saragosti, Jonathan Chang, Ni-Chen Matthews, Benjamin J. Oxley, Peter R. Kronauer, Daniel J.C. |
description | Life inside ant colonies is orchestrated with diverse pheromones, but it is not clear how ants perceive these social signals. It has been proposed that pheromone perception in ants evolved via expansions in the numbers of odorant receptors (ORs) and antennal lobe glomeruli. Here, we generate the first mutant lines in the clonal raider ant, Ooceraea biroi, by disrupting orco, a gene required for the function of all ORs. We find that orco mutants exhibit severe deficiencies in social behavior and fitness, suggesting they are unable to perceive pheromones. Surprisingly, unlike in Drosophila melanogaster, orco mutant ants also lack most of the ∼500 antennal lobe glomeruli found in wild-type ants. These results illustrate that ORs are essential for ant social organization and raise the possibility that, similar to mammals, receptor function is required for the development and/or maintenance of the highly complex olfactory processing areas in the ant brain.
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•We generated odorant receptor co-receptor (orco) mutants in an ant•orco mutants did not follow pheromone trails or cluster with other ants•Mutant ants also had greatly reduced antennal lobes in the brain•Odorant receptors are essential for the complex organization of ant societies
Development of the first line of mutant ants, using CRISPR/Cas technology, reveals what happens inside of a colony when ants lose the ability to recognize odors. |
doi_str_mv | 10.1016/j.cell.2017.07.001 |
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•We generated odorant receptor co-receptor (orco) mutants in an ant•orco mutants did not follow pheromone trails or cluster with other ants•Mutant ants also had greatly reduced antennal lobes in the brain•Odorant receptors are essential for the complex organization of ant societies
Development of the first line of mutant ants, using CRISPR/Cas technology, reveals what happens inside of a colony when ants lose the ability to recognize odors.</description><identifier>ISSN: 0092-8674</identifier><identifier>EISSN: 1097-4172</identifier><identifier>DOI: 10.1016/j.cell.2017.07.001</identifier><identifier>PMID: 28802042</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; ant colonies ; antennal lobe ; Ants - genetics ; Ants - physiology ; Arthropod Antennae - cytology ; Arthropod Antennae - physiology ; chemical communication ; CRISPR ; Drosophila melanogaster ; evo-devo ; Formicidae ; genes ; Insect Proteins - genetics ; Insect Proteins - metabolism ; mammals ; Mutagenesis ; mutants ; Mutation ; odorant receptors ; Odorants ; Ooceraea biroi ; pheromones ; Receptors, Odorant - genetics ; Receptors, Odorant - metabolism ; Social Behavior ; social structure</subject><ispartof>Cell, 2017-08, Vol.170 (4), p.727-735.e10</ispartof><rights>2017 Elsevier Inc.</rights><rights>Copyright © 2017 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c488t-8c8bdb0844ce9ac71684be5d70152e3ad71be03554273e4ef2f905cf045504ec3</citedby><cites>FETCH-LOGICAL-c488t-8c8bdb0844ce9ac71684be5d70152e3ad71be03554273e4ef2f905cf045504ec3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0092867417307729$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28802042$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Trible, Waring</creatorcontrib><creatorcontrib>Olivos-Cisneros, Leonora</creatorcontrib><creatorcontrib>McKenzie, Sean K.</creatorcontrib><creatorcontrib>Saragosti, Jonathan</creatorcontrib><creatorcontrib>Chang, Ni-Chen</creatorcontrib><creatorcontrib>Matthews, Benjamin J.</creatorcontrib><creatorcontrib>Oxley, Peter R.</creatorcontrib><creatorcontrib>Kronauer, Daniel J.C.</creatorcontrib><title>orco Mutagenesis Causes Loss of Antennal Lobe Glomeruli and Impaired Social Behavior in Ants</title><title>Cell</title><addtitle>Cell</addtitle><description>Life inside ant colonies is orchestrated with diverse pheromones, but it is not clear how ants perceive these social signals. It has been proposed that pheromone perception in ants evolved via expansions in the numbers of odorant receptors (ORs) and antennal lobe glomeruli. Here, we generate the first mutant lines in the clonal raider ant, Ooceraea biroi, by disrupting orco, a gene required for the function of all ORs. We find that orco mutants exhibit severe deficiencies in social behavior and fitness, suggesting they are unable to perceive pheromones. Surprisingly, unlike in Drosophila melanogaster, orco mutant ants also lack most of the ∼500 antennal lobe glomeruli found in wild-type ants. These results illustrate that ORs are essential for ant social organization and raise the possibility that, similar to mammals, receptor function is required for the development and/or maintenance of the highly complex olfactory processing areas in the ant brain.
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•We generated odorant receptor co-receptor (orco) mutants in an ant•orco mutants did not follow pheromone trails or cluster with other ants•Mutant ants also had greatly reduced antennal lobes in the brain•Odorant receptors are essential for the complex organization of ant societies
Development of the first line of mutant ants, using CRISPR/Cas technology, reveals what happens inside of a colony when ants lose the ability to recognize odors.</description><subject>Animals</subject><subject>ant colonies</subject><subject>antennal lobe</subject><subject>Ants - genetics</subject><subject>Ants - physiology</subject><subject>Arthropod Antennae - cytology</subject><subject>Arthropod Antennae - physiology</subject><subject>chemical communication</subject><subject>CRISPR</subject><subject>Drosophila melanogaster</subject><subject>evo-devo</subject><subject>Formicidae</subject><subject>genes</subject><subject>Insect Proteins - genetics</subject><subject>Insect Proteins - metabolism</subject><subject>mammals</subject><subject>Mutagenesis</subject><subject>mutants</subject><subject>Mutation</subject><subject>odorant receptors</subject><subject>Odorants</subject><subject>Ooceraea biroi</subject><subject>pheromones</subject><subject>Receptors, Odorant - genetics</subject><subject>Receptors, Odorant - metabolism</subject><subject>Social Behavior</subject><subject>social structure</subject><issn>0092-8674</issn><issn>1097-4172</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkVFrFDEUhYModq3-AR8kj77M9iaTTDIgQrtoLaz4oL4JIZO502aZTdZkZsF_b4atxb4oXAgk3zncnEPIawZrBqy52K0djuOaA1NrKAPsCVkxaFUlmOJPyQqg5ZVulDgjL3LeAYCWUj4nZ1xr4CD4ivyIyUX6eZ7sLQbMPtONnTNmuo050zjQyzBhCHYsFx3S6zHuMc2jpzb09GZ_sD5hT79G5wtyhXf26GOiPiy6_JI8G-yY8dX9eU6-f_zwbfOp2n65vtlcbisntJ4q7XTXd6CFcNhap1ijRYeyV8Akx9r2inUItZSCqxoFDnxoQboBhJQg0NXn5P3J9zB3e-wdhinZ0RyS39v0y0TrzeOX4O_MbTyakkbTSigGb-8NUvw5Y57M3uclXBswztlwaBSXulb6vyhruZZMCMULyk-oSyXMhMPDRgzM0qDZmUVplgYNlAFWRG_-_suD5E9lBXh3ArAkevSYTHYeg8O-VOEm00f_L__fgamtGQ</recordid><startdate>20170810</startdate><enddate>20170810</enddate><creator>Trible, Waring</creator><creator>Olivos-Cisneros, Leonora</creator><creator>McKenzie, Sean K.</creator><creator>Saragosti, Jonathan</creator><creator>Chang, Ni-Chen</creator><creator>Matthews, Benjamin J.</creator><creator>Oxley, Peter R.</creator><creator>Kronauer, Daniel J.C.</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20170810</creationdate><title>orco Mutagenesis Causes Loss of Antennal Lobe Glomeruli and Impaired Social Behavior in Ants</title><author>Trible, Waring ; Olivos-Cisneros, Leonora ; McKenzie, Sean K. ; Saragosti, Jonathan ; Chang, Ni-Chen ; Matthews, Benjamin J. ; Oxley, Peter R. ; Kronauer, Daniel J.C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c488t-8c8bdb0844ce9ac71684be5d70152e3ad71be03554273e4ef2f905cf045504ec3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>ant colonies</topic><topic>antennal lobe</topic><topic>Ants - genetics</topic><topic>Ants - physiology</topic><topic>Arthropod Antennae - cytology</topic><topic>Arthropod Antennae - physiology</topic><topic>chemical communication</topic><topic>CRISPR</topic><topic>Drosophila melanogaster</topic><topic>evo-devo</topic><topic>Formicidae</topic><topic>genes</topic><topic>Insect Proteins - genetics</topic><topic>Insect Proteins - metabolism</topic><topic>mammals</topic><topic>Mutagenesis</topic><topic>mutants</topic><topic>Mutation</topic><topic>odorant receptors</topic><topic>Odorants</topic><topic>Ooceraea biroi</topic><topic>pheromones</topic><topic>Receptors, Odorant - genetics</topic><topic>Receptors, Odorant - metabolism</topic><topic>Social Behavior</topic><topic>social structure</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Trible, Waring</creatorcontrib><creatorcontrib>Olivos-Cisneros, Leonora</creatorcontrib><creatorcontrib>McKenzie, Sean K.</creatorcontrib><creatorcontrib>Saragosti, Jonathan</creatorcontrib><creatorcontrib>Chang, Ni-Chen</creatorcontrib><creatorcontrib>Matthews, Benjamin J.</creatorcontrib><creatorcontrib>Oxley, Peter R.</creatorcontrib><creatorcontrib>Kronauer, Daniel J.C.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Trible, Waring</au><au>Olivos-Cisneros, Leonora</au><au>McKenzie, Sean K.</au><au>Saragosti, Jonathan</au><au>Chang, Ni-Chen</au><au>Matthews, Benjamin J.</au><au>Oxley, Peter R.</au><au>Kronauer, Daniel J.C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>orco Mutagenesis Causes Loss of Antennal Lobe Glomeruli and Impaired Social Behavior in Ants</atitle><jtitle>Cell</jtitle><addtitle>Cell</addtitle><date>2017-08-10</date><risdate>2017</risdate><volume>170</volume><issue>4</issue><spage>727</spage><epage>735.e10</epage><pages>727-735.e10</pages><issn>0092-8674</issn><eissn>1097-4172</eissn><abstract>Life inside ant colonies is orchestrated with diverse pheromones, but it is not clear how ants perceive these social signals. It has been proposed that pheromone perception in ants evolved via expansions in the numbers of odorant receptors (ORs) and antennal lobe glomeruli. Here, we generate the first mutant lines in the clonal raider ant, Ooceraea biroi, by disrupting orco, a gene required for the function of all ORs. We find that orco mutants exhibit severe deficiencies in social behavior and fitness, suggesting they are unable to perceive pheromones. Surprisingly, unlike in Drosophila melanogaster, orco mutant ants also lack most of the ∼500 antennal lobe glomeruli found in wild-type ants. These results illustrate that ORs are essential for ant social organization and raise the possibility that, similar to mammals, receptor function is required for the development and/or maintenance of the highly complex olfactory processing areas in the ant brain.
[Display omitted]
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•We generated odorant receptor co-receptor (orco) mutants in an ant•orco mutants did not follow pheromone trails or cluster with other ants•Mutant ants also had greatly reduced antennal lobes in the brain•Odorant receptors are essential for the complex organization of ant societies
Development of the first line of mutant ants, using CRISPR/Cas technology, reveals what happens inside of a colony when ants lose the ability to recognize odors.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>28802042</pmid><doi>10.1016/j.cell.2017.07.001</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals ant colonies antennal lobe Ants - genetics Ants - physiology Arthropod Antennae - cytology Arthropod Antennae - physiology chemical communication CRISPR Drosophila melanogaster evo-devo Formicidae genes Insect Proteins - genetics Insect Proteins - metabolism mammals Mutagenesis mutants Mutation odorant receptors Odorants Ooceraea biroi pheromones Receptors, Odorant - genetics Receptors, Odorant - metabolism Social Behavior social structure |
title | orco Mutagenesis Causes Loss of Antennal Lobe Glomeruli and Impaired Social Behavior in Ants |
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