Extensive population-level sampling reveals clinal variation in (R)-(−)-linalool produced by the flowers of an endemic evening primrose, Oenothera harringtonii

Mutualism has its limits: consequences of asymmetric interactions between a well-defended plant and its herbivorous pollinator

“…For most experiments, we grew O. harringtonii plants from seeds collected in natural populations, one whose flowers either emit ( R )-(−)-linalool (Lin+) or do not (Lin−), in a greenhouse at Cornell University [37]. Plants from adjacent populations with similar Lin+ or Lin− chemotypes were substituted in some experiments due to unexpectedly low seed germination (see electronic supplementary material, table S1 for source populations).…”

“…One test was motivated by our finding that the addition of ( R )-(−)-linalool to Lin− plants elicited different patterns of oviposition than did plants from a Lin+ wild population. A previous study of 650 plants across the full geographical distribution of O. harringtonii revealed that a second volatile compound (( Z )-7-decen-5-olide = ‘jasmine lactone’), emitted in low amounts, represented the next strongest contribution after linalool to population-level differentiation in a random forest statistical analysis [37]. Thus, we compared Lin− plants with plants from the same population to which a 33 : 1 ratio of ( R )-(−)-linalool: jasmine lactone (v/v in hexane) was added to a septum, as described above.…”

“…Thus, we compared Lin− plants with plants from the same population to which a 33 : 1 ratio of ( R )-(−)-linalool: jasmine lactone (v/v in hexane) was added to a septum, as described above. This treatment was chosen to match floral emission ratios from Lin+ (both compounds are absent in plants from Lin− populations; [37]) and to test the effects of combining the lactone with linalool as a potentially mitigating factor in oviposition.…”

“…Here we explored how the use of O. harringtonii plants as adult nectar sources and larval host plants affects the individual-level health of H. lineata moths as pollinating herbivores. Prior studies revealed sharp clinal variation in the floral scent composition of O. harringtonii, for the presence of linalool, a common floral volatile, in northwestern populations and its absence in southeastern populations [37]. This drew our attention because previous research on similar interactions between Datura wrightii plants in southwestern USA, pollinated by adult Manduca sexta moths and eaten by their larvae, revealed that a specific enantiomer, (R)-(−)-linalool, emitted by D. wrightii flowers suppresses oviposition by female M. sexta [38], providing a potential mechanism for mediating conflicts of interest between pollinating herbivores and their host plants.…”

“…This drew our attention because previous research on similar interactions between Datura wrightii plants in southwestern USA, pollinated by adult Manduca sexta moths and eaten by their larvae, revealed that a specific enantiomer, ( R )-(−)-linalool, emitted by D. wrightii flowers suppresses oviposition by female M. sexta [38], providing a potential mechanism for mediating conflicts of interest between pollinating herbivores and their host plants. Flowers from different populations of O. harringtonii either emit very large amounts of the same specific enantiomer, ( R )-(−)-linalool, or none at all, as this species does not produce the ( S )-(+)-linalool enantiomer [37]. Because linalool can affect both nectar feeding and oviposition by adult hawkmoths [38] and mediate indirect defences against their larvae [39,40] in related model systems, we focused on the polymorphism of floral ( R )-(−)-linalool in O. harringtonii as a potential key to understanding its impacts on the health of the plant's most important pollinator, H. lineata .…”