IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37046-2.html
   My bibliography  Save this article

Aggregation pheromones have a non-linear effect on oviposition behavior in Drosophila melanogaster

Author

Listed:
  • Thomas A. Verschut

    (University of Groningen
    Stockholm University)

  • Renny Ng

    (University of California, San Diego)

  • Nicolas P. Doubovetzky

    (University of Groningen)

  • Guillaume Calvez

    (University of Groningen)

  • Jan L. Sneep

    (University of Groningen)

  • Adriaan J. Minnaard

    (University of Groningen)

  • Chih-Ying Su

    (University of California, San Diego)

  • Mikael A. Carlsson

    (Stockholm University)

  • Bregje Wertheim

    (University of Groningen)

  • Jean-Christophe Billeter

    (University of Groningen)

Abstract

Female fruit flies (Drosophila melanogaster) oviposit at communal sites where the larvae may cooperate or compete for resources depending on group size. This offers a model system to determine how females assess quantitative social information. We show that the concentration of pheromones found on a substrate increases linearly with the number of adult flies that have visited that site. Females prefer oviposition sites with pheromone concentrations corresponding to an intermediate number of previous visitors, whereas sites with low or high concentrations are unattractive. This dose-dependent decision is based on a blend of 11-cis-Vaccenyl Acetate (cVA) indicating the number of previous visitors and heptanal (a novel pheromone deriving from the oxidation of 7-Tricosene), which acts as a dose-independent co-factor. This response is mediated by detection of cVA by odorant receptor neurons Or67d and Or65a, and at least five different odorant receptor neurons for heptanal. Our results identify a mechanism allowing individuals to transform a linear increase of pheromones into a non-linear behavioral response.

Suggested Citation

  • Thomas A. Verschut & Renny Ng & Nicolas P. Doubovetzky & Guillaume Calvez & Jan L. Sneep & Adriaan J. Minnaard & Chih-Ying Su & Mikael A. Carlsson & Bregje Wertheim & Jean-Christophe Billeter, 2023. "Aggregation pheromones have a non-linear effect on oviposition behavior in Drosophila melanogaster," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37046-2
    DOI: 10.1038/s41467-023-37046-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37046-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-37046-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Erwan Poivet & Kacem Rharrabe & Christelle Monsempes & Nicolas Glaser & Didier Rochat & Michel Renou & Frédéric Marion-Poll & Emmanuelle Jacquin-Joly, 2012. "The use of the sex pheromone as an evolutionary solution to food source selection in caterpillars," Nature Communications, Nature, vol. 3(1), pages 1-7, January.
    2. Bates, Douglas & Mächler, Martin & Bolker, Ben & Walker, Steve, 2015. "Fitting Linear Mixed-Effects Models Using lme4," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 67(i01).
    3. Simon N. Wood, 2011. "Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models," Journal of the Royal Statistical Society Series B, Royal Statistical Society, vol. 73(1), pages 3-36, January.
    4. Pavan Ramdya & Pawel Lichocki & Steeve Cruchet & Lukas Frisch & Winnie Tse & Dario Floreano & Richard Benton, 2015. "Mechanosensory interactions drive collective behaviour in Drosophila," Nature, Nature, vol. 519(7542), pages 233-236, March.
    5. Clara H. Ferreira & Marta A. Moita, 2020. "Behavioral and neuronal underpinnings of safety in numbers in fruit flies," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    6. William C. Wetzel & Heather M. Kharouba & Moria Robinson & Marcel Holyoak & Richard Karban, 2016. "Variability in plant nutrients reduces insect herbivore performance," Nature, Nature, vol. 539(7629), pages 425-427, November.
    7. Minrong Ai & Soohong Min & Yael Grosjean & Charlotte Leblanc & Rati Bell & Richard Benton & Greg S. B. Suh, 2010. "Acid sensing by the Drosophila olfactory system," Nature, Nature, vol. 468(7324), pages 691-695, December.
    8. Yael Grosjean & Raphael Rytz & Jean-Pierre Farine & Liliane Abuin & Jérôme Cortot & Gregory S. X. E. Jefferis & Richard Benton, 2011. "An olfactory receptor for food-derived odours promotes male courtship in Drosophila," Nature, Nature, vol. 478(7368), pages 236-240, October.
    9. Meghan Laturney & Jean-Christophe Billeter, 2016. "Drosophila melanogaster females restore their attractiveness after mating by removing male anti-aphrodisiac pheromones," Nature Communications, Nature, vol. 7(1), pages 1-11, November.
    10. Liming Wang & David J. Anderson, 2010. "Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila," Nature, Nature, vol. 463(7278), pages 227-231, January.
    11. Jean-Christophe Billeter & Jade Atallah & Joshua J. Krupp & Jocelyn G. Millar & Joel D. Levine, 2009. "Specialized cells tag sexual and species identity in Drosophila melanogaster," Nature, Nature, vol. 461(7266), pages 987-991, October.
    12. Roshan K. Vijendravarma & Sunitha Narasimha & Tadeusz J. Kawecki, 2013. "Predatory cannibalism in Drosophila melanogaster larvae," Nature Communications, Nature, vol. 4(1), pages 1-8, June.
    13. Amina Kurtovic & Alexandre Widmer & Barry J. Dickson, 2007. "A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone," Nature, Nature, vol. 446(7135), pages 542-546, March.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Philipp F. M. Baumann & Enzo Rossi & Alexander Volkmann, 2020. "What Drives Inflation and How: Evidence from Additive Mixed Models Selected by cAIC," Papers 2006.06274, arXiv.org, revised Aug 2022.
    2. Javier J How & Saket Navlakha & Sreekanth H Chalasani, 2021. "Neural network features distinguish chemosensory stimuli in Caenorhabditis elegans," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-38, November.
    3. Rebecca Rooke & Joshua J. Krupp & Amara Rasool & Mireille Golemiec & Megan Stewart & Jonathan Schneider & Joel D. Levine, 2024. "The gene “degrees of kevin bacon” (dokb) regulates a social network behaviour in Drosophila melanogaster," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    4. Øystein Sørensen & Anders M. Fjell & Kristine B. Walhovd, 2023. "Longitudinal Modeling of Age-Dependent Latent Traits with Generalized Additive Latent and Mixed Models," Psychometrika, Springer;The Psychometric Society, vol. 88(2), pages 456-486, June.
    5. Swen P. M. Bos & Tina Cornioley & Anne Dray & Patrick O. Waeber & Claude A. Garcia, 2020. "Exploring Livelihood Strategies of Shifting Cultivation Farmers in Assam through Games," Sustainability, MDPI, vol. 12(6), pages 1-17, March.
    6. David L. Miller & Richard Glennie & Andrew E. Seaton, 2020. "Understanding the Stochastic Partial Differential Equation Approach to Smoothing," Journal of Agricultural, Biological and Environmental Statistics, Springer;The International Biometric Society;American Statistical Association, vol. 25(1), pages 1-16, March.
    7. Shiu-Ling Chen & Bo-Ting Liu & Wang-Pao Lee & Sin-Bo Liao & Yao-Bang Deng & Chia-Lin Wu & Shuk-Man Ho & Bing-Xian Shen & Guan-Hock Khoo & Wei-Chiang Shiu & Chih-Hsuan Chang & Hui-Wen Shih & Jung-Kun W, 2022. "WAKE-mediated modulation of cVA perception via a hierarchical neuro-endocrine axis in Drosophila male-male courtship behaviour," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. James T. Stroud & Sean T. Giery & Robert J. P. Heathcote & Sarin Tiatragul & Michael L. Yuan & Kenneth J. Feeley & Jonathan B. Losos, 2024. "Observing character displacement from process to pattern in a novel vertebrate community," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    9. Daniel Paredes & Sara Mendes & José Paulo Sousa, 2024. "Habitat Diversity Increases Chrysoperla carnea s.l. (Stephens, 1836) (Neuroptera, Chrysopidae) Abundance in Olive Landscapes," Agriculture, MDPI, vol. 14(2), pages 1-11, February.
    10. Emily R Churchill & Calvin Dytham & Jon R Bridle & Michael D F Thom, 2021. "Social and physical environment independently affect oviposition decisions in Drosophila," Behavioral Ecology, International Society for Behavioral Ecology, vol. 32(6), pages 1391-1399.
    11. Nan-Ji Jiang & Xinqi Dong & Daniel Veit & Bill S. Hansson & Markus Knaden, 2024. "Elevated ozone disrupts mating boundaries in drosophilid flies," Nature Communications, Nature, vol. 15(1), pages 1-8, December.
    12. JANSSENS, Jochen & DE CORTE, Annelies & SÖRENSEN, Kenneth, 2016. "Water distribution network design optimisation with respect to reliability," Working Papers 2016007, University of Antwerp, Faculty of Business and Economics.
    13. Raymond Hernandez & Elizabeth A. Pyatak & Cheryl L. P. Vigen & Haomiao Jin & Stefan Schneider & Donna Spruijt-Metz & Shawn C. Roll, 2021. "Understanding Worker Well-Being Relative to High-Workload and Recovery Activities across a Whole Day: Pilot Testing an Ecological Momentary Assessment Technique," IJERPH, MDPI, vol. 18(19), pages 1-17, October.
    14. Christopher Hassall & Michael Nisbet & Evan Norcliffe & He Wang, 2024. "The Potential Health Benefits of Urban Tree Planting Suggested through Immersive Environments," Land, MDPI, vol. 13(3), pages 1-12, February.
    15. Jie Zhao & Ji Chen & Damien Beillouin & Hans Lambers & Yadong Yang & Pete Smith & Zhaohai Zeng & Jørgen E. Olesen & Huadong Zang, 2022. "Global systematic review with meta-analysis reveals yield advantage of legume-based rotations and its drivers," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    16. Elisabeth Beckmann & Lukas Olbrich & Joseph Sakshaug, 2024. "Multivariate assessment of interviewer-related errors in a cross-national economic survey (Lukas Olbrich, Elisabeth Beckmann, Joseph W. Sakshaug)," Working Papers 253, Oesterreichische Nationalbank (Austrian Central Bank).
    17. Gerhard Tutz & Moritz Berger, 2018. "Tree-structured modelling of categorical predictors in generalized additive regression," Advances in Data Analysis and Classification, Springer;German Classification Society - Gesellschaft für Klassifikation (GfKl);Japanese Classification Society (JCS);Classification and Data Analysis Group of the Italian Statistical Society (CLADAG);International Federation of Classification Societies (IFCS), vol. 12(3), pages 737-758, September.
    18. F J Heather & D Z Childs & A M Darnaude & J L Blanchard, 2018. "Using an integral projection model to assess the effect of temperature on the growth of gilthead seabream Sparus aurata," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-19, May.
    19. Valentina Krenz & Arjen Alink & Tobias Sommer & Benno Roozendaal & Lars Schwabe, 2023. "Time-dependent memory transformation in hippocampus and neocortex is semantic in nature," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    20. Morán-Ordóñez, Alejandra & Ameztegui, Aitor & De Cáceres, Miquel & de-Miguel, Sergio & Lefèvre, François & Brotons, Lluís & Coll, Lluís, 2020. "Future trade-offs and synergies among ecosystem services in Mediterranean forests under global change scenarios," Ecosystem Services, Elsevier, vol. 45(C).

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37046-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.