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Tetranorsesquiterpenoids as Attractants of Yucca Moths to Yucca Flowers

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Abstract

The obligate pollination mutualism between Yucca and yucca moths is a classical example of coevolution. Oviposition and active pollination by female yucca moths occur at night when Yucca flowers are open and strongly scented. Thus, floral volatiles have been suggested as key sensory signals attracting yucca moths to their host plants, but no bioactive compounds have yet been identified. In this study, we showed that both sexes of the pollinator moth Tegeticula yuccasella are attracted to the floral scent of the host Yucca filamentosa. Chemical analysis of the floral headspace from six Yucca species in sections Chaenocarpa and Sarcocarpa revealed a set of novel tetranorsesquiterpenoids putatively derived from (E)-4,8-dimethyl-1,3,7-nonatriene. Their structure elucidation was accomplished by NMR analysis of the crude floral scent sample of Yucca treculeana along with GC/MS analysis and confirmed by total synthesis. Since all these volatiles are included in the floral scent of Y. filamentosa, which has been an important model species for understanding the pollination mutualism, we name these compounds filamentolide, filamentol, filamental, and filamentone. Several of these compounds elicited antennal responses in pollinating (Tegeticula) and non-pollinating (Prodoxus) moth species upon stimulation in electrophysiological recordings. In addition, synthetic (Z)-filamentolide attracted significant numbers of both sexes of two associated Prodoxus species in a field trapping experiment. Highly specialized insect-plant interactions, such as obligate pollination mutualisms, are predicted to be maintained through “private channels” dictated by specific compounds. The identification of novel bioactive tetranorsesquiterpenoids is a first step in testing such a hypothesis in the Yucca-yucca moth interaction.

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Data Availability

Voucher moth specimens have been deposited at the Cornell University Insect Collection (accessions CUIC000002359-CUIC000002431).

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not applicable.

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Acknowledgements

GPS was funded by the Crafoord Foundation, the Swedish Royal Academy of Sciences, and Wenner-Gren Foundations. KAS and DMA were funded by NSF DEB 1556568 and 1655544. We acknowledge the Archbold Biological Station for providing access to field sites and for permission to work with Tegeticula pupae. Special thanks to Christopher Smith (Willamette University) for providing key headspace samples from Yucca schidigera. We thank Wilhelm Boland (Max-Planck-Institute, Jena), Jim Leebens-Mack (University of Georgia), Mike Walla (University of South Carolina), and especially Olle Pellmyr (deceased) for the initial discussions that launched this project.

Funding

GPS was funded by the Crafoord Foundation, the Swedish Royal Academy of Sciences, and Wenner-Gren Foundations. KAS and DMA were funded by NSF DEB 1556568 and 1655544.

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Authors and Affiliations

  1. Institute of Organic Chemistry, University of Hamburg, Martin-Luther-King-Platz 6, 20146, Hamburg, Germany

    Armin Tröger, Hans-Martin Galbrecht, Robert Twele, Stephan von Reuss & Wittko Francke

  2. Department of Biology, Lund University, Solvegatan 37, 223 62, Lund, Sweden

    Glenn P. Svensson

  3. USDA-Agricultural Research Service, U.S. Horticultural Research Laboratory, 2001 South Rock Road, Fort Pierce, FL, 34945, USA

    Joseph M. Patt

  4. Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745, Jena, Germany

    Stefan Bartram

  5. Department of Chemistry, Federal University of Parana, Curitiba, PR, 81531-990, Brazil

    Paulo H. G. Zarbin

  6. Department of Biology, Syracuse University, 107 College Place, Syracuse, NY, 13244, USA

    Kari A. Segraves & David M. Althoff

  7. Laboratory of Bioanalytical Chemistry, University of Neuchatel, Avenue de Bellevaux 51, CH-2000, Neuchatel, Switzerland

    Stephan von Reuss

  8. Department of Neurobiology and Behavior, Cornell University, 215 Tower Road, Ithaca, NY, 14853, USA

    Robert A. Raguso

Authors
  1. Armin Tröger
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  2. Glenn P. Svensson
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  3. Hans-Martin Galbrecht
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  4. Robert Twele
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  5. Joseph M. Patt
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  6. Stefan Bartram
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  7. Paulo H. G. Zarbin
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  8. Kari A. Segraves
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  9. David M. Althoff
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  10. Stephan von Reuss
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  11. Robert A. Raguso
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  12. Wittko Francke
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Contributions

Headspace samples were collected by GPS, KAS, DMA, JMP, and RAR. Field trapping, behavioral and electrophysiological assays were performed by GPS, JMP, and RAR. Chemical analyses, organic synthesis, and structural determinations were accomplished by AT, H-MG, RT, SB, PHGZ, SvR, and WF. The manuscript was written by AT, GPS, SvR, and RAR and was edited by all authors.

Corresponding author

Correspondence to Robert A. Raguso.

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The authors disclose no competing interests.

Additional information

Wittko Francke, Deceased, 27th of December 2020

Supplementary Information

Synthesis of novel compounds is described in the electronic supplementary material, see link below.

Supplementary file1 (DOCX 1.03 MB)

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Tröger, A., Svensson, G.P., Galbrecht, HM. et al. Tetranorsesquiterpenoids as Attractants of Yucca Moths to Yucca Flowers. J Chem Ecol 47, 1025–1041 (2021). https://doi.org/10.1007/s10886-021-01308-4

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