Drosophila Free-Flight Odor Tracking is Altered in a Sex-Specific Manner By Preimaginal Sensory Exposure
In insects such as Drosophila melanogaster , flight guidance is based on converging sensory information provided by several modalities, including chemoperception. Drosophila flies are particularly attracted by complex odors constituting volatile molecules from yeast, pheromones and microbe-metaboliz...
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creator | Tolassy, Vincent Cazalé-Debat, Laurie Houot, Benjamin Reynaud, Rémy Heydel, Jean-Marie Ferveur, Jean-François Everaerts, Claude |
description | In insects such as
Drosophila melanogaster
, flight guidance is based on converging sensory information provided by several modalities, including chemoperception. Drosophila flies are particularly attracted by complex odors constituting volatile molecules from yeast, pheromones and microbe-metabolized food. Based on a recent study revealing that adult male courtship behavior can be affected by early preimaginal exposure to maternally transmitted egg factors, we wondered whether a similar exposure could affect free-flight odor tracking in flies of both sexes. Our main experiment consisted of testing flies differently conditioned during preimaginal development in a wind tunnel. Each fly was presented with a dual choice of food labeled by groups of each sex of
D. melanogaster
or
D. simulans
flies. The combined effect of food with the
cis
-vaccenyl acetate pheromone (
c
VA), which is involved in aggregation behavior, was also measured. Moreover, we used the headspace method to determine the "odorant" identity of the different labeled foods tested. We also measured the antennal electrophysiological response to
c
VA in females and males resulting from the different preimaginal conditioning procedures. Our data indicate that flies differentially modulated their flight response (take off, flight duration, food landing and preference) according to sex, conditioning and food choice. Our headspace analysis revealed that many food-derived volatile molecules diverged between sexes and species. Antennal responses to
c
VA showed clear sex-specific variation for conditioned flies but not for control flies. In summary, our study indicates that preimaginal conditioning can affect Drosophila free flight behavior in a sex-specific manner. |
doi_str_mv | 10.1007/s10886-023-01416-3 |
format | Article |
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Drosophila melanogaster
, flight guidance is based on converging sensory information provided by several modalities, including chemoperception. Drosophila flies are particularly attracted by complex odors constituting volatile molecules from yeast, pheromones and microbe-metabolized food. Based on a recent study revealing that adult male courtship behavior can be affected by early preimaginal exposure to maternally transmitted egg factors, we wondered whether a similar exposure could affect free-flight odor tracking in flies of both sexes. Our main experiment consisted of testing flies differently conditioned during preimaginal development in a wind tunnel. Each fly was presented with a dual choice of food labeled by groups of each sex of
D. melanogaster
or
D. simulans
flies. The combined effect of food with the
cis
-vaccenyl acetate pheromone (
c
VA), which is involved in aggregation behavior, was also measured. Moreover, we used the headspace method to determine the "odorant" identity of the different labeled foods tested. We also measured the antennal electrophysiological response to
c
VA in females and males resulting from the different preimaginal conditioning procedures. Our data indicate that flies differentially modulated their flight response (take off, flight duration, food landing and preference) according to sex, conditioning and food choice. Our headspace analysis revealed that many food-derived volatile molecules diverged between sexes and species. Antennal responses to
c
VA showed clear sex-specific variation for conditioned flies but not for control flies. In summary, our study indicates that preimaginal conditioning can affect Drosophila free flight behavior in a sex-specific manner.</description><identifier>ISSN: 0098-0331</identifier><identifier>EISSN: 1573-1561</identifier><identifier>DOI: 10.1007/s10886-023-01416-3</identifier><identifier>PMID: 36881326</identifier><language>eng</language><publisher>New York: Springer US</publisher><subject>Acetic acid ; Aggregation behavior ; Agriculture ; Animals ; Biochemistry ; Biochemistry, Molecular Biology ; Biological Microscopy ; Biomedical and Life Sciences ; Chemosensory perception ; Conditioning ; Courtship ; Drosophila ; Drosophila melanogaster - physiology ; Drosophila Proteins - pharmacology ; Ecology ; Ecology, environment ; Entomology ; Exposure ; Female ; Flies ; Flight behavior ; Food ; Food preferences ; Free flight ; Fruit flies ; Headspace ; Insects ; Landing behavior ; Life Sciences ; Male ; Odor ; Odorants ; Odors ; Pheromones ; Pheromones - pharmacology ; Sensory evaluation ; Sex ; Sexes ; Sexual behavior ; Smell - physiology ; Tracking ; Wind tunnels ; Yeasts</subject><ispartof>Journal of chemical ecology, 2023-04, Vol.49 (3-4), p.179-194</ispartof><rights>The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c453t-c4cbf2c47d751298ac697715e49fdd4eba10f4910006094a445fc50a412492433</citedby><cites>FETCH-LOGICAL-c453t-c4cbf2c47d751298ac697715e49fdd4eba10f4910006094a445fc50a412492433</cites><orcidid>0000-0002-4022-686X ; 0000-0002-6089-9922 ; 0000-0002-7559-083X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s10886-023-01416-3$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s10886-023-01416-3$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,780,784,885,27922,27923,41486,42555,51317</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36881326$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-04080541$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Tolassy, Vincent</creatorcontrib><creatorcontrib>Cazalé-Debat, Laurie</creatorcontrib><creatorcontrib>Houot, Benjamin</creatorcontrib><creatorcontrib>Reynaud, Rémy</creatorcontrib><creatorcontrib>Heydel, Jean-Marie</creatorcontrib><creatorcontrib>Ferveur, Jean-François</creatorcontrib><creatorcontrib>Everaerts, Claude</creatorcontrib><title>Drosophila Free-Flight Odor Tracking is Altered in a Sex-Specific Manner By Preimaginal Sensory Exposure</title><title>Journal of chemical ecology</title><addtitle>J Chem Ecol</addtitle><addtitle>J Chem Ecol</addtitle><description>In insects such as
Drosophila melanogaster
, flight guidance is based on converging sensory information provided by several modalities, including chemoperception. Drosophila flies are particularly attracted by complex odors constituting volatile molecules from yeast, pheromones and microbe-metabolized food. Based on a recent study revealing that adult male courtship behavior can be affected by early preimaginal exposure to maternally transmitted egg factors, we wondered whether a similar exposure could affect free-flight odor tracking in flies of both sexes. Our main experiment consisted of testing flies differently conditioned during preimaginal development in a wind tunnel. Each fly was presented with a dual choice of food labeled by groups of each sex of
D. melanogaster
or
D. simulans
flies. The combined effect of food with the
cis
-vaccenyl acetate pheromone (
c
VA), which is involved in aggregation behavior, was also measured. Moreover, we used the headspace method to determine the "odorant" identity of the different labeled foods tested. We also measured the antennal electrophysiological response to
c
VA in females and males resulting from the different preimaginal conditioning procedures. Our data indicate that flies differentially modulated their flight response (take off, flight duration, food landing and preference) according to sex, conditioning and food choice. Our headspace analysis revealed that many food-derived volatile molecules diverged between sexes and species. Antennal responses to
c
VA showed clear sex-specific variation for conditioned flies but not for control flies. In summary, our study indicates that preimaginal conditioning can affect Drosophila free flight behavior in a sex-specific manner.</description><subject>Acetic acid</subject><subject>Aggregation behavior</subject><subject>Agriculture</subject><subject>Animals</subject><subject>Biochemistry</subject><subject>Biochemistry, Molecular Biology</subject><subject>Biological Microscopy</subject><subject>Biomedical and Life Sciences</subject><subject>Chemosensory perception</subject><subject>Conditioning</subject><subject>Courtship</subject><subject>Drosophila</subject><subject>Drosophila melanogaster - physiology</subject><subject>Drosophila Proteins - pharmacology</subject><subject>Ecology</subject><subject>Ecology, environment</subject><subject>Entomology</subject><subject>Exposure</subject><subject>Female</subject><subject>Flies</subject><subject>Flight behavior</subject><subject>Food</subject><subject>Food preferences</subject><subject>Free flight</subject><subject>Fruit flies</subject><subject>Headspace</subject><subject>Insects</subject><subject>Landing behavior</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Odor</subject><subject>Odorants</subject><subject>Odors</subject><subject>Pheromones</subject><subject>Pheromones - pharmacology</subject><subject>Sensory evaluation</subject><subject>Sex</subject><subject>Sexes</subject><subject>Sexual behavior</subject><subject>Smell - physiology</subject><subject>Tracking</subject><subject>Wind tunnels</subject><subject>Yeasts</subject><issn>0098-0331</issn><issn>1573-1561</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kU9v1DAQxS0EotvCF-CALHEpB8P4X-Icl9KllRYVqeVseZ3Jrks2Cfam6n77eklbJA5cPJL9m-c38wh5x-ETByg_Jw7GFAyEZMAVL5h8QWZcl5JxXfCXZAZQGQZS8iNynNItAIjC6NfkSBbGcCmKGdl8jX3qh01oHV1ERLZow3qzo1d1H-lNdP5X6NY0JDpvdxixpqGjjl7jPbse0IcmePrddR1G-mVPf0QMW7cOnWsz0qU-7un5_dCnMeIb8qpxbcK3j_WE_Fyc35xdsOXVt8uz-ZJ5peUun37VCK_KutRcVMb5oipLrlFVTV0rXDkOjary_FBApZxSuvEanOJCVUJJeUI-Trob19ohZj9xb3sX7MV8aQ93oMCAVvyOZ_Z0YofY_x4x7ew2JI9t6zrsx2RFaZQ0eaGQ0Q__oLf9GPOgmTKQNUutD4JionzeaorYPDvgYA-Z2SkzmzOzfzKzB8fvH6XH1Rbr55ankDIgJyDlp26N8e_f_5F9AN5GnrY</recordid><startdate>20230401</startdate><enddate>20230401</enddate><creator>Tolassy, Vincent</creator><creator>Cazalé-Debat, Laurie</creator><creator>Houot, Benjamin</creator><creator>Reynaud, Rémy</creator><creator>Heydel, Jean-Marie</creator><creator>Ferveur, Jean-François</creator><creator>Everaerts, Claude</creator><general>Springer US</general><general>Springer Nature B.V</general><general>Springer Verlag</general><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>3V.</scope><scope>7QG</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7U7</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PCBAR</scope><scope>PDBOC</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0002-4022-686X</orcidid><orcidid>https://orcid.org/0000-0002-6089-9922</orcidid><orcidid>https://orcid.org/0000-0002-7559-083X</orcidid></search><sort><creationdate>20230401</creationdate><title>Drosophila Free-Flight Odor Tracking is Altered in a Sex-Specific Manner By Preimaginal Sensory Exposure</title><author>Tolassy, Vincent ; Cazalé-Debat, Laurie ; Houot, Benjamin ; Reynaud, Rémy ; Heydel, Jean-Marie ; Ferveur, Jean-François ; Everaerts, Claude</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c453t-c4cbf2c47d751298ac697715e49fdd4eba10f4910006094a445fc50a412492433</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Acetic acid</topic><topic>Aggregation behavior</topic><topic>Agriculture</topic><topic>Animals</topic><topic>Biochemistry</topic><topic>Biochemistry, Molecular Biology</topic><topic>Biological Microscopy</topic><topic>Biomedical and Life Sciences</topic><topic>Chemosensory perception</topic><topic>Conditioning</topic><topic>Courtship</topic><topic>Drosophila</topic><topic>Drosophila melanogaster - physiology</topic><topic>Drosophila Proteins - pharmacology</topic><topic>Ecology</topic><topic>Ecology, environment</topic><topic>Entomology</topic><topic>Exposure</topic><topic>Female</topic><topic>Flies</topic><topic>Flight behavior</topic><topic>Food</topic><topic>Food preferences</topic><topic>Free flight</topic><topic>Fruit flies</topic><topic>Headspace</topic><topic>Insects</topic><topic>Landing behavior</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Odor</topic><topic>Odorants</topic><topic>Odors</topic><topic>Pheromones</topic><topic>Pheromones - pharmacology</topic><topic>Sensory evaluation</topic><topic>Sex</topic><topic>Sexes</topic><topic>Sexual behavior</topic><topic>Smell - physiology</topic><topic>Tracking</topic><topic>Wind tunnels</topic><topic>Yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tolassy, Vincent</creatorcontrib><creatorcontrib>Cazalé-Debat, Laurie</creatorcontrib><creatorcontrib>Houot, Benjamin</creatorcontrib><creatorcontrib>Reynaud, Rémy</creatorcontrib><creatorcontrib>Heydel, Jean-Marie</creatorcontrib><creatorcontrib>Ferveur, Jean-François</creatorcontrib><creatorcontrib>Everaerts, Claude</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Toxicology Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection (ProQuest)</collection><collection>Natural Science Collection</collection><collection>Earth, Atmospheric & Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Earth, Atmospheric & Aquatic Science Database</collection><collection>Materials Science Collection</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Journal of chemical ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tolassy, Vincent</au><au>Cazalé-Debat, Laurie</au><au>Houot, Benjamin</au><au>Reynaud, Rémy</au><au>Heydel, Jean-Marie</au><au>Ferveur, Jean-François</au><au>Everaerts, Claude</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Drosophila Free-Flight Odor Tracking is Altered in a Sex-Specific Manner By Preimaginal Sensory Exposure</atitle><jtitle>Journal of chemical ecology</jtitle><stitle>J Chem Ecol</stitle><addtitle>J Chem Ecol</addtitle><date>2023-04-01</date><risdate>2023</risdate><volume>49</volume><issue>3-4</issue><spage>179</spage><epage>194</epage><pages>179-194</pages><issn>0098-0331</issn><eissn>1573-1561</eissn><abstract>In insects such as
Drosophila melanogaster
, flight guidance is based on converging sensory information provided by several modalities, including chemoperception. Drosophila flies are particularly attracted by complex odors constituting volatile molecules from yeast, pheromones and microbe-metabolized food. Based on a recent study revealing that adult male courtship behavior can be affected by early preimaginal exposure to maternally transmitted egg factors, we wondered whether a similar exposure could affect free-flight odor tracking in flies of both sexes. Our main experiment consisted of testing flies differently conditioned during preimaginal development in a wind tunnel. Each fly was presented with a dual choice of food labeled by groups of each sex of
D. melanogaster
or
D. simulans
flies. The combined effect of food with the
cis
-vaccenyl acetate pheromone (
c
VA), which is involved in aggregation behavior, was also measured. Moreover, we used the headspace method to determine the "odorant" identity of the different labeled foods tested. We also measured the antennal electrophysiological response to
c
VA in females and males resulting from the different preimaginal conditioning procedures. Our data indicate that flies differentially modulated their flight response (take off, flight duration, food landing and preference) according to sex, conditioning and food choice. Our headspace analysis revealed that many food-derived volatile molecules diverged between sexes and species. Antennal responses to
c
VA showed clear sex-specific variation for conditioned flies but not for control flies. In summary, our study indicates that preimaginal conditioning can affect Drosophila free flight behavior in a sex-specific manner.</abstract><cop>New York</cop><pub>Springer US</pub><pmid>36881326</pmid><doi>10.1007/s10886-023-01416-3</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-4022-686X</orcidid><orcidid>https://orcid.org/0000-0002-6089-9922</orcidid><orcidid>https://orcid.org/0000-0002-7559-083X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acetic acid Aggregation behavior Agriculture Animals Biochemistry Biochemistry, Molecular Biology Biological Microscopy Biomedical and Life Sciences Chemosensory perception Conditioning Courtship Drosophila Drosophila melanogaster - physiology Drosophila Proteins - pharmacology Ecology Ecology, environment Entomology Exposure Female Flies Flight behavior Food Food preferences Free flight Fruit flies Headspace Insects Landing behavior Life Sciences Male Odor Odorants Odors Pheromones Pheromones - pharmacology Sensory evaluation Sex Sexes Sexual behavior Smell - physiology Tracking Wind tunnels Yeasts |
title | Drosophila Free-Flight Odor Tracking is Altered in a Sex-Specific Manner By Preimaginal Sensory Exposure |
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