Tetranorterpenoids as Attractants of Yucca Moths to Yucca Flowers

Authors: TROGER, ARMIN - University Of Hamburg; SVENSSON, GLENN - Lund University; GALBRECHT, HAMS-MARTIN - University Of Hamburg; TWELE, ROBERT - University Of Hamburg; Patt, Joseph - Joe; BARTRAM, STEFAN - Max Planck Institute For Chemistry; ZARBIN, PAULO H - Federal University Of Paraná; SEGRAVES, KARI - Syracuse University; ALTHOFF, DAVID - Syracuse University; VON REUSS, STEPHAN - Neuchatel University - Switzerland; RAGUSO, ROBERT - Cornell University; FRANCKE, WITTKO - University Of Hamburg

Submitted to: Journal of Chemical Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/23/2021
Publication Date: N/A
Citation: N/A

Interpretive Summary: Flowers of the yucca plant are pollinated only by a small group of moths called ‘yucca moths’. Yuccas and yucca moths have co-evolved to the point where they are entirely dependent on each other to reproduce and complete their life cycles. In Ecology and Biology textbooks, the relationship between yucca and yucca moths is often used as an example of the ecological relationship called an ‘obligate mutualism’. ‘Mutualism’ is the term used for ecological relationships where the interaction between two organisms is mutually beneficial to both. ‘Obligate’ is the term used to indicate that neither organism can perform a vital life function, such as reproduction, without the interacting together in specific ways. When a female yucca moth visits a yucca flower, she collects the pollen and places it in a pouch near her shoulder. When she visits the next flower, she will take some of the pollen from her shoulder pouch and deliberately pollinate the flower. After she pollinates the flower, she lays several eggs into the flower’s ovary, which develops into a fruit capsule. The eggs will hatch inside the developing fruit and the baby caterpillars will eat some of the seeds. However, enough seeds will mature to enable the yucca population to persist. So, in this ecological tradeoff, the flower sacrifices some of its seeds to the moth’s caterpillars while the moth provides a high level of pollination with consequent seed maturation. It has been long thought that the yucca’s floral fragrance is critical for guiding the moths to the flowers, but no biological-active compounds in the yucca’s floral fragrance have been identified. In this study, we identified the yucca’s floral fragrance compounds, which belong to a chemical class called tetranorterpenoids. Since all these fragrance compounds were identified in the floral scent of a yucca species with the scientific name of Yucca filamentosa, we named these compounds filamentolide, filamentol, filamental and filamentone. Yucca filamentosa, commonly known as ‘Spanish bayonets because of its knife-like leaves, has been an important model species for understanding the pollination mutualism between yuccas and yucca moths. To demonstrate that these fragrance compounds were indeed attractive to the moths, they were first synthesized in the laboratory and then tested in both laboratory and field experiments. The laboratory experiments demonstrated that the yucca moth’s sense of smell organs were highly attuned to the synthetic compound and that they were capable of detecting tiny amounts of the synthetic yucca scent compounds. A field experiment, using sticky traps baited with the synthetic compounds, was conducted to demonstrate the attractiveness of the synthetic compounds to yucca moths in nature. Each trap had a wax droplet containing a standard amount of the synthetic fragrance compound filamentolide. In this way, the wax droplet functioned as a fragrance dispenser, like a scented candle. The traps were placed in a line where each trap was positioned 100 ft apart from the nearest trap in either direction. The line of traps was established among stands of Spanish bayonets growing in Laguna Atascosa National Wildlife Refuge (Port Isabel, TX). A significantly greater number of yucca moths were captured in the traps with scented wax droplets versus the scentless traps, showing that filamentolide was attractive to the yucca moths. Highly specialized insect-plant interactions, such as obligate pollination mutualisms, are predicted to be maintained through “private channels” dictated by specific floral fragrance compounds. The identification of novel bioactive tetranorterpenoids is a first step in testing such a hypothesis in the yucca-yucca moth interaction.

Technical 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 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 tetranorterpenoids putatively derived from (E)-4,8-dimethyl-1,3,7-nonatriene. Their structure elucidation was accomplished by NMR analysis of the crude floral scent extract 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 trapping experiment. Highly specialized insect-plant interactions, such as obligate pollination mutualisms, are predicted to be maintained through “private channels” dicated by specific compounds. The identification of novel bioactive tetranorterpeniods is a first step in testing such a hypothesis in the Yucca-yucca moth interaction.