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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
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    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. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
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