We explored the effects of inbreeding on volatile production and host-plant quality and resistance to herbivory using the common weed, Solanum carolinense L (horsenettle).  Horsenettle, like other Solanaceae, exhibits RNase-mediated gametophytic self-incompatibility (SI)—a genetically based system that prevents self-fertilization. However, SI is uncommon in weedy and invasive species that are short lived and undergo repeated cycles of colonization and extinction. Our previous research has shown that the SI response in horsenettle is a plastic trait: self-fertility varies with flower age and conditions of low fruit production. Consequently, horsenettle can self-fertilize when outcross pollen is limited, but avoid the adverse effects of inbreeding when outcross pollen is available. A greenhouse study revealed that there is significant, but surprisingly low levels of inbreeding depression in horsenettle. To examine the consequences of inbreeding on plant-insect interactions, we grew ramets of inbred and outbred plants from eight maternal families under field conditions; collected the volatile organic compounds that were produced by these ramets; and analyzed the volatiles using GC-MS. We also examined the preference, performance, and total leaf consumption of Manduca sexta caterpillars on leaves of selfed and outcrossed progeny of eight maternal plants.

Results/Conclusions

We found that selfed plants released significantly lower quantities of volatiles compared to outcrossed plants and that there was a significant maternal family effect on the total amount and blend of volatiles released.  In addition, we found a breeding by family interaction for the total amount and blend of volatiles, indicating genetic variation among families for inbreeding depression. Analysis of only outcrossed plants revealed a genet effect on the total amount and blend of volatiles released, indicating broad-sense heritability of volatile traits among genets. In the laboratory, we found that caterpillars preferred leaf disks from selfed versus outcrossed plants and that caterpillars had higher relative growth rates (RGR) and total leaf consumption (TC) on selfed versus outcrossed plants.  We also found a breeding-by-family interaction for insect RGR and TC, indicating variation among these families for inbreeding depression. Our findings suggest that inbreeding can alter the volatile cues available to foraging insects in wild plants. We believe that this is the first study to demonstrate genetic variation for plant volatiles in a non-cultivated species under field conditions. Our results also suggest that inbreeding increased host-plant quality and decreased herbivore resistance and that this effect varied among maternal families. These findings indicate that inbreeding can alter volatile mediated plant-herbivore interactions.