A1 Refereed original research article in a scientific journal
Insect Herbivory Selects for Volatile-Mediated Plant-Plant Communication
Authors: Kalske A, Shiojiri K, Uesugi A, Sakata Y, Morrell K, Kessler A
Publisher: CELL PRESS
Publishing place: New York
Publication year: 2019
Journal: Current Biology
Journal name in source: CURRENT BIOLOGY
Journal acronym: CURR BIOL
Volume: 29
Issue: 18
First page : 3128
Last page: 3133
Number of pages: 9
ISSN: 0960-9822
DOI: https://doi.org/10.1016/j.cub.2019.08.011
Abstract
Plant volatile organic compounds (VOCs) are major vehicles of information transfer between organisms and mediate many ecological interactions [1-3]. Altering VOC emission in response to herbivore damage has been hypothesized to be adaptive, as it can deter subsequent herbivores [4], attract natural enemies of herbivores [5], or transmit information about attacks between distant parts of the same plant [6-9]. Neighboring plants may also respond to these VOC cues by priming their own defenses against oncoming herbivory, thereby reducing future damage [10-12]. However, under which conditions such information sharing provides fitness benefits to emitter plants, and, therefore, whether selection by herbivores affects the evolution of such VOC signaling, is still unclear [13]. Here, we test the predictions of two alternative hypotheses, the kin selection and mutual benefits hypotheses [14], to uncover the selective environment that may favor information sharing in plants. Measuring the response to natural selection in Solidago altissima, we found strong effects of herbivory on the way plants communicated with neighbors. Plants from populations that experienced selection by insect herbivory induced resistance in all neighboring conspecifics by airborne cues, whereas those from populations experiencing herbivore exclusion induced resistance only in neighbors of the same genotype. Furthermore, the information-sharing plants converged on a common, airborne VOC signal upon damage. We demonstrate that herbivory can drive the evolution of plant-plant communication via induction of airborne cues and suggest plants as a model system for understanding information sharing and communication among organisms in general.
Plant volatile organic compounds (VOCs) are major vehicles of information transfer between organisms and mediate many ecological interactions [1-3]. Altering VOC emission in response to herbivore damage has been hypothesized to be adaptive, as it can deter subsequent herbivores [4], attract natural enemies of herbivores [5], or transmit information about attacks between distant parts of the same plant [6-9]. Neighboring plants may also respond to these VOC cues by priming their own defenses against oncoming herbivory, thereby reducing future damage [10-12]. However, under which conditions such information sharing provides fitness benefits to emitter plants, and, therefore, whether selection by herbivores affects the evolution of such VOC signaling, is still unclear [13]. Here, we test the predictions of two alternative hypotheses, the kin selection and mutual benefits hypotheses [14], to uncover the selective environment that may favor information sharing in plants. Measuring the response to natural selection in Solidago altissima, we found strong effects of herbivory on the way plants communicated with neighbors. Plants from populations that experienced selection by insect herbivory induced resistance in all neighboring conspecifics by airborne cues, whereas those from populations experiencing herbivore exclusion induced resistance only in neighbors of the same genotype. Furthermore, the information-sharing plants converged on a common, airborne VOC signal upon damage. We demonstrate that herbivory can drive the evolution of plant-plant communication via induction of airborne cues and suggest plants as a model system for understanding information sharing and communication among organisms in general.