Do "Private Channels" mediate Obligate Mutualism?
All obligate mutualisms are fraught with conflict: fig wasps might lay too many eggs, and figs trees could kill wasp larvae after being pollinated. Such conflicts are thought to be resolved through several mechanisms, including “partner sanctions” and “partner encounter”. Partner sanctions were demonstrated by Pellmyr and Huth (1994), where Yucca plants selectively abort flowers in which female yucca moths have laid too many eggs. Partner encounter, in which mutualists are brought together by a kind of chemical “secret handshake”, a private channel to which other insects would be oblivious, has been more difficult to test.
All obligate mutualisms are fraught with conflict: fig wasps might lay too many eggs, and figs trees could kill wasp larvae after being pollinated. Such conflicts are thought to be resolved through several mechanisms, including “partner sanctions” and “partner encounter”. Partner sanctions were demonstrated by Pellmyr and Huth (1994), where Yucca plants selectively abort flowers in which female yucca moths have laid too many eggs. Partner encounter, in which mutualists are brought together by a kind of chemical “secret handshake”, a private channel to which other insects would be oblivious, has been more difficult to test.
For the past 25 years, I have collaborated with a large team, including Olle Pellmyr and my first postdoc, Glenn Svensson, to study floral scent as a partner encounter signal in the genus Yucca. Yucca flowers are strongly scented, and yucca moths (both sexes) are attracted to yucca scent in Y-mazes, 4-way olfactometers and field traps, justifying a closer look at scent composition. Yucca volatiles are new to science, comprising a mix of unique alcohols, aldehydes, ketones and lactones derived from an 11-carbon terpene ([E]-1,4,8-dimethyl nonatriene = DMNT) common to herbivore-wounded vegetation in most plants, including crops like maize and soy.
[Above left, Yucca glauca in its prairie habitat, Boulder CO. Right, female yucca moth actively pollinating a flower of Y. treculeana, overlaid with solved structures of the unique volatile compounds produced by yucca flowers. Below, putative biosynthetic scheme leading from trans-DMNT to novel yucca scent compounds]
[Above left, Yucca glauca in its prairie habitat, Boulder CO. Right, female yucca moth actively pollinating a flower of Y. treculeana, overlaid with solved structures of the unique volatile compounds produced by yucca flowers. Below, putative biosynthetic scheme leading from trans-DMNT to novel yucca scent compounds]
Wittko Francke and his team at Univ. Hamburg utilized a full arsenal of chemical analytical tools over nearly a decade to solve these structures. Studies by Roman Kaiser, Stefan Schulz and Stefan Dötterl have identified other variations on a theme of trans-DMNT derived compounds in night blooming cacti, elm tree leaves and "love hotel" aroids and "Panama-hat" plants pollinated by scarab beetles.
[Left; results from binary choice bioassays in which male and female Tegeticula yuccasella moths respond to the concealed floral scent from Yucca filamentosa in a four-way-olfactometer]
Yuccas are conservative in scent diversification: widespread species such as Y. filamentosa and Y. glauca emit a full complement of unique terpenoid volatiles, whereas species with smaller ranges or those that bloom in sympatry with other yuccas have simplified bouquets, featuring the lactones (Y. treculeana, along the Rio Grande) or alcohols (Y. schidigera, in the Mohave Desert) rather than the full blend. However, Yuccas evolved in Mesoamerica and we remain ignorant of chemical data and moth behavioral preferences for many key plant-pollinator pairs in Mexico. This story will undoubtedly become richer when we learn more about the core (Mexican) basal taxa in the genus Yucca.
Yuccas are conservative in scent diversification: widespread species such as Y. filamentosa and Y. glauca emit a full complement of unique terpenoid volatiles, whereas species with smaller ranges or those that bloom in sympatry with other yuccas have simplified bouquets, featuring the lactones (Y. treculeana, along the Rio Grande) or alcohols (Y. schidigera, in the Mohave Desert) rather than the full blend. However, Yuccas evolved in Mesoamerica and we remain ignorant of chemical data and moth behavioral preferences for many key plant-pollinator pairs in Mexico. This story will undoubtedly become richer when we learn more about the core (Mexican) basal taxa in the genus Yucca.
Tröger, A., G.P. Svensson, H-M. Galbrecht, R. Twele, J.M. Patt, S. Bartram, P.H.G. Zarbin, K.A. Segraves, D.M. Althoff, S. von Reuss, R.A. Raguso, W. Francke. 2021. Tetra-norsesquiterpenoids as attractants of yucca moths to yucca flowers. Journal of Chemical Ecology 47: 1025-1041.
https://doi.org/10.1007/s10886-021-01308-4
Tröger, A., G.P. Svensson, D.M. Althoff, K.A. Segraves, R.A. Raguso, W. Francke. 2019. The pattern of straight-chain hydrocarbons released by yucca flowers (Asparagaceae). Journal of Chemical Ecology 45: 46-49. https://doi.org/10.1007/s10886-018-1037-y
Svensson, G.P., R.A. Raguso, R. Flatz, C.I. Smith. 2016. Floral scent of Joshua trees (Yucca brevifolia sensu lato): divergence in scent profiles between species but breakdown of signal integrity in a narrow hybrid zone. American Journal of Botany 103: 1-10. https://doi.org/10.3732/ajb.1600033
Svensson, G.P., O. Pellmyr, R.A. Raguso. 2011. Pollinator attraction to volatiles from virgin and pollinated host flowers in a yucca/moth obligate mutualism. Oikos 120: 1577–1583. https://doi.org/10.1111/j.1600-0706.2011.19258.x
Svensson, G.P., O. Pellmyr, R.A. Raguso. 2006. Strong conservation of floral scent composition in two allopatric Yuccas. Journal of Chemical Ecology 32: 2657-2665. https://doi.org/10.1007/s10886-006-9189-6
Svensson, G.P., M.O. Hickman, S. Bartram, W. Boland, O. Pellmyr, R.A. Raguso. 2005. Chemistry and geographic variation of floral scent in Yucca filamentosa (Agavaceae). American Journal of Botany 92: 1624-1631. https://doi.org/10.3732/ajb.92.10.1624
https://doi.org/10.1007/s10886-021-01308-4
Tröger, A., G.P. Svensson, D.M. Althoff, K.A. Segraves, R.A. Raguso, W. Francke. 2019. The pattern of straight-chain hydrocarbons released by yucca flowers (Asparagaceae). Journal of Chemical Ecology 45: 46-49. https://doi.org/10.1007/s10886-018-1037-y
Svensson, G.P., R.A. Raguso, R. Flatz, C.I. Smith. 2016. Floral scent of Joshua trees (Yucca brevifolia sensu lato): divergence in scent profiles between species but breakdown of signal integrity in a narrow hybrid zone. American Journal of Botany 103: 1-10. https://doi.org/10.3732/ajb.1600033
Svensson, G.P., O. Pellmyr, R.A. Raguso. 2011. Pollinator attraction to volatiles from virgin and pollinated host flowers in a yucca/moth obligate mutualism. Oikos 120: 1577–1583. https://doi.org/10.1111/j.1600-0706.2011.19258.x
Svensson, G.P., O. Pellmyr, R.A. Raguso. 2006. Strong conservation of floral scent composition in two allopatric Yuccas. Journal of Chemical Ecology 32: 2657-2665. https://doi.org/10.1007/s10886-006-9189-6
Svensson, G.P., M.O. Hickman, S. Bartram, W. Boland, O. Pellmyr, R.A. Raguso. 2005. Chemistry and geographic variation of floral scent in Yucca filamentosa (Agavaceae). American Journal of Botany 92: 1624-1631. https://doi.org/10.3732/ajb.92.10.1624
[Yucca collaborative team members (L-R): Olle Pellmyr, Wittko Francke, Glenn Svensson, Kari Segraves and Dave Althoff, Chris Smith]