IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38722-z.html
   My bibliography  Save this article

Odor-regulated oviposition behavior in an ecological specialist

Author

Listed:
  • Raquel Álvarez-Ocaña

    (University of Lausanne)

  • Michael P. Shahandeh

    (University of Lausanne)

  • Vijayaditya Ray

    (Ludwig-Maximilians Universität München, Fakultät für Biologie, Biozentrum)

  • Thomas O. Auer

    (University of Lausanne)

  • Nicolas Gompel

    (Ludwig-Maximilians Universität München, Fakultät für Biologie, Biozentrum)

  • Richard Benton

    (University of Lausanne)

Abstract

Colonization of a novel ecological niche can require, or be driven by, evolution of an animal’s behaviors promoting their reproductive success. We investigated the evolution and sensory basis of oviposition in Drosophila sechellia, a close relative of Drosophila melanogaster that exhibits extreme specialism for Morinda citrifolia noni fruit. D. sechellia produces fewer eggs than other drosophilids and lays these almost exclusively on noni substrates. We show that visual, textural and social cues do not explain this species-specific preference. By contrast, we find that loss of olfactory input in D. sechellia, but not D. melanogaster, essentially abolishes egg-laying, suggesting that olfaction gates gustatory-driven noni preference. Noni odors are detected by redundant olfactory pathways, but we discover a role for hexanoic acid and the cognate Ionotropic receptor 75b (Ir75b) in odor-evoked oviposition. Through receptor exchange in D. melanogaster, we provide evidence for a causal contribution of odor-tuning changes in Ir75b to the evolution of D. sechellia’s oviposition behavior.

Suggested Citation

  • Raquel Álvarez-Ocaña & Michael P. Shahandeh & Vijayaditya Ray & Thomas O. Auer & Nicolas Gompel & Richard Benton, 2023. "Odor-regulated oviposition behavior in an ecological specialist," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38722-z
    DOI: 10.1038/s41467-023-38722-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38722-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38722-z?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. Fei Wang & Kaiyu Wang & Nora Forknall & Christopher Patrick & Tansy Yang & Ruchi Parekh & Davi Bock & Barry J. Dickson, 2020. "Neural circuitry linking mating and egg laying in Drosophila females," Nature, Nature, vol. 579(7797), pages 101-105, March.
    2. 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.
    3. Juan Antonio Sánchez-Alcañiz & Giovanna Zappia & Frédéric Marion-Poll & Richard Benton, 2017. "A mechanosensory receptor required for food texture detection in Drosophila," Nature Communications, Nature, vol. 8(1), pages 1-9, April.
    4. Lucia L. Prieto-Godino & Raphael Rytz & Benoîte Bargeton & Liliane Abuin & J. Roman Arguello & Matteo Dal Peraro & Richard Benton, 2016. "Olfactory receptor pseudo-pseudogenes," Nature, Nature, vol. 539(7627), pages 93-97, November.
    5. 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.
    6. Thomas O. Auer & Mohammed A. Khallaf & Ana F. Silbering & Giovanna Zappia & Kaitlyn Ellis & Raquel Álvarez-Ocaña & J. Roman Arguello & Bill S. Hansson & Gregory S. X. E. Jefferis & Sophie J. C. Caron , 2020. "Olfactory receptor and circuit evolution promote host specialization," Nature, Nature, vol. 579(7799), pages 402-408, 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. Suguru Takagi & Gizem Sancer & Liliane Abuin & S. David Stupski & J. Roman Arguello & Lucia L. Prieto-Godino & David L. Stern & Steeve Cruchet & Raquel Álvarez-Ocaña & Carl F. R. Wienecke & Floris Bre, 2024. "Olfactory sensory neuron population expansions influence projection neuron adaptation and enhance odour tracking," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Evan S. Schaffer & Neeli Mishra & Matthew R. Whiteway & Wenze Li & Michelle B. Vancura & Jason Freedman & Kripa B. Patel & Venkatakaushik Voleti & Liam Paninski & Elizabeth M. C. Hillman & L. F. Abbot, 2023. "The spatial and temporal structure of neural activity across the fly brain," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Kaitlyn Elizabeth Ellis & Sven Bervoets & Hayley Smihula & Ishani Ganguly & Eva Vigato & Thomas O. Auer & Richard Benton & Ashok Litwin-Kumar & Sophie Jeanne Cécile Caron, 2024. "Evolution of connectivity architecture in the Drosophila mushroom body," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. 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.
    5. J Roman Arguello & Carolina Sellanes & Yann Ru Lou & Robert A Raguso, 2013. "Can Yeast (S. cerevisiae) Metabolic Volatiles Provide Polymorphic Signaling?," PLOS ONE, Public Library of Science, vol. 8(8), pages 1-12, August.
    6. Liangyu Tao & Samuel P. Wechsler & Vikas Bhandawat, 2023. "Sensorimotor transformation underlying odor-modulated locomotion in walking Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    7. 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.
    8. Chen Zhang & Anmo J. Kim & Crisalesandra Rivera-Perez & Fernando G. Noriega & Young-Joon Kim, 2022. "The insect somatostatin pathway gates vitellogenesis progression during reproductive maturation and the post-mating response," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Gwénaëlle Bontonou & Bastien Saint-Leandre & Tane Kafle & Tess Baticle & Afrah Hassan & Juan Antonio Sánchez-Alcañiz & J. Roman Arguello, 2024. "Evolution of chemosensory tissues and cells across ecologically diverse Drosophilids," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    10. 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.

    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_s41467-023-38722-z. 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.