Variation in Volatile Emission in Mimulus guttatus and Implications for Plant-Insect Interactions

The volatile compounds emitted from plants function as key host-location cues for their insect visitors. Floral volatiles guide pollinators to nectar and pollen, and in turn, pollinators initiate plant reproduction, potentially promoting a mutualistic interaction. Constitutive and herbivore-induced foliar volatiles function as an important plant defense by deterring herbivores and attracting natural enemies of herbivores. Given the importance of plant volatiles in insect behavior, variation in volatile phenotypes is expected to affect insect visitation patterns, and consequently, plant reproductive success and susceptibility to herbivores. Inbreeding is an important source of genetic variation that it is extremely common in natural populations of flowering plants. Since inbreeding increases homozygosity, inbreeding could increase expression of recessive alleles that disrupt biosynthesis of volatile compounds. In previous work, inbreeding in the mixed-mating herb Mimulus guttatus (yellow monkeyflower) decreased pollinator attraction and resistance to herbivory. However, the plant traits underlying these effects are unknown. This dissertation examined the effects of inbreeding on the floral and foliar volatile phenotypes of M. guttatus and the consequences of these effects for its pollinators and herbivores.
The first chapter of this dissertation investigates floral volatile profiles from experimentally inbred and outbred M. guttatus. Since olfactory cues are known to signal the quality of floral rewards, and since inbreeding in M. guttatus is known to reduce the quantity and quality of pollen (its only floral reward), it also investigates whether the floral volatile profile is associated with pollen rewards. Results demonstrated that inbreeding reduced emission of a sesquiterpene, β-trans-bergamotene. Six monoterpenes were positively associated with pollen rewards in M. guttatus, but there was no overlap between compounds exhibiting inbreeding effects and compounds associated with pollen rewards. The second chapter of this dissertation examines the foraging behavior of bumblebees (Bombus impatiens) in response to β-trans-bergamotene and compounds correlated with pollen rewards. Behavioral assays demonstrated that bumblebees are innately attracted to β-bergamotene. Moreover, after foraging on M. guttatus, bumblebees learned to prefer floral odors correlated with pollen rewards. However, bumblebees were only able to base foraging decisions on associative learning when presented floral scents that did not contain β-bergamotene, suggesting that its innate attractive properties could interfere with learned olfactory signals.
The third chapter of this dissertation investigates the effects of inbreeding and herbivory on foliar volatile emission in M. guttatus. Results demonstrated that herbivory significantly increased foliar volatile emission. In particular, herbivory increased emission of 1-octen-3-ol and neophytadiene, compounds that are known to function as indirect and direct defenses, respectively. This study also found an interaction between inbreeding and herbivory in the overall volatile profile, and that inbreeding reduced constitutive emission of individual components of the volatile blend. The fourth chapter of this dissertation examines performance and preferences of a generalist herbivore, Helicoverpa zea, and a specialist, Junonia coenia, in response to inbreeding and trichome density in M. guttatus. Results demonstrated that H. zea developed most efficiently on inbred plants with low trichome density, but did not exhibit a preference for inbred versus outbred plants. Junonia coenia performed best on outbred plants with low trichome density, and consistently preferred outbred over inbred plants, even when presented only olfactory cues. Both species consumed more leaf tissue in outbred plants, suggesting that inbred plants could have an advantage in defending against herbivores.
This dissertation is one of only a few studies to examine effects of inbreeding on plant volatile profiles, and it is the first study to demonstrate that innate olfactory preferences of bumblebees can override learned preferences for floral scents. It is also among the first to differentiate the responses of specialist and generalist herbivores to inbreeding effects in their host. The findings in this dissertation enhance our understanding of the ecology and evolution of plant-insect interactions, which can have important implications for the evolution of plant mating systems and the vulnerability of small populations.