Applying error management theory to understand the evolution of decision-making in plant defense

Despite their reputation for passivity, plants, like animals, have evolved a remarkable capacity to perceive and respond to information about threats in their environment. Unlike animals, however, it is unknown how plants prioritize different information and assess risk to 'make decisions' about how to respond. This research project will use error management theory to evaluate how tall goldenrod plants (Solidago altissima) assess threats of herbivory from cues that they receive from the environment. It is already known that tall goldenrod can perceive and respond to two different airborne cues to initiate defenses before herbivores arrive: (1) a mate-attracting chemical (pheromone) from a key damaging herbivore species and (2) volatile chemicals released from neighboring tall goldenrod plants that are being attacked by generalist insects. Greenhouse and field experiments will be conducted to determine cue thresholds, what genes are triggered by different cues, and the costs and benefits of responding when cues are matched versus mismatched with the type of damage received. Ultimately the cost of making an error in not responding will be measured by reduced reproductive output due to herbivore damage. The results will reveal whether tall goldenrod takes a bet-hedging approach and allocates defenses to minimize costly errors in favor of less costly errors. By exploring plant defenses from this novel perspective, this research will significantly broaden our understanding of how plants make decisions and provide insight on the evolution of plant defenses against herbivores. Interactions between plants and herbivores are the backbone of terrestrial ecosystems, so understanding how plants 'decide' to defend themselves has applications from crop protection to control of invasive species. The project will support training and mentorship of students and a postdoctoral researcher, as well as public outreach initiatives through established programs at The Pennsylvania State University.

Solidago altissima is among the few plant species known to detect and alter its defenses in response to two volatile chemical cues: one from neighboring plants, one from the mating activity of a key, specialist herbivore. Greenhouse and field experiments will test error management theory to elucidate costs and benefits of the defensive strategies of genotypes of S. altissima following exposure to cues that are matched and mismatched with key herbivore damage. Subsequent phytohormone and transcriptomic analyses of plant tissue from these experiments will identify key mechanisms underlying defense responses of the genotypes following exposure to cues and insect damage. Under the various experimental scenarios, the effectiveness of defense responses of the genotypes against herbivores will reveal evolutionary selection pressures that have encouraged plants to minimize responses to false alarms or insects that do not do substantial damage that would reduce fitness, while prioritizing responses against more damaging foes. The research from this project will provide key insight into how plant defenses evolved to handle multiple threats and has significant potential to inform development of novel management tactics while providing an intriguing topic that will help engage middle- and high-school students and the general public in the novelty and significance of chemical communication between common plant and insect species.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.