Feeding intensity of insect herbivores is associated more closely with key metabolite profiles than phylogenetic relatedness of their potential hosts

Authors: RAPO, CAROLE - Commonwealth Agricultural Bureau International (CABI) - Switzerland; SCHAFFNER, URS - Commonwealth Agricultural Bureau International (CABI) - Switzerland; EIGENBRODE, SANFOR - University Of Idaho; HINZ, HARIET - Commonwealth Agricultural Bureau International (CABI) - Switzerland; PRICE, WILLIAM - University Of Idaho; MORRA, MATTHEW - University Of Idaho; Gaskin, John; SCHWARZLAENDER, MARK - University Of Idaho

Submitted to: PeerJ
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/13/2019
Publication Date: 12/17/2019
Citation: Rapo, C.B., Schaffner, U., Eigenbrode, S.D., Hinz, H.L., Price, W., Morra, M., Gaskin, J.F., Schwarzlaender, M. 2019. Feeding intensity of insect herbivores is associated more closely with key metabolite profiles than phylogenetic relatedness of their potential hosts. PeerJ. https://doi.org/10.7717/peerj.8203.
DOI: https://doi.org/10.7717/peerj.8203

Interpretive Summary: Biological control of exotic weeds is the use of co-evolved insects from other countries that attack weeds in the invaded range. To make sure these biological control agents do not attack other species of plants, we test them in quarantine. We expect that the plant species most at risk are close relatives of the weed, but this is not always true; insects may be attracted to different plant species because the plant looks or smells the same as the weed, even if not a close relative of the weed. We tested this hypothesis in the laboratory with a mustard- specialized weevil, on 13 test plant species differing in their suitability as hosts for the weevil. We compared the associations between feeding by the weevil and either plant chemistry or genetic similarity using simple correlation. For comparison, we performed a similar test with an insect that typically attacks lots of plant species. We found using either method that plant chemistry was more strongly associated with feeding intensity by the weevil than the genetic similarity. In contrast, neither genetic nor plant chemistry was significantly associated with feeding intensity by the insect that attacks many species. The result indicates that plant chemistry can be more reliable indicators of the feeding preference of a specialist insect than relatedness of its potential hosts. The finding has implications for the evolution and maintenance of host specialization. It also has potential implications for identifying plant species for testing during prerelease assessment of specialized biocontrol candidates.

Technical Abstract: The basis of host specialization or restricted host ranges in insect herbivores is of interest from an evolutionary perspective but also for applications such as biological control. Although host ranges are often described in phylogenetic terms, ultimately insect performance is determined by phenotypic traits, which may or may not be phylogenetically conserved. Traits such as plant secondary metabolites are considered to be phylogenetically labile. Therefore, chemical phenotypes may be more strongly associated with herbivore preference than phylogenetic relatedness of these hosts. We tested this hypothesis in the laboratory with a Brassicaceae- specialized weevil, Ceutorhynchus cardariae Korotyaev (Coleoptera: Curculionidae), on 13 test plant species differing in their suitability as hosts for the weevil. We compared the statistical associations between feeding by C. cardariae and either phenotypic similarity (secondary chemistry – glucosinolate profile) or genetic similarity (sequence of the chloroplast gene ndhF) using simple correlation and by assessing the strengths of association between feedinb by the weevil and dendrograms based on glucosinolates or ndhF sequence (i.e., a phylogram). For comparison, we performed a similar test with the oligophagous Plutella xylostella L. (Lepidoptera: Plutellidae) using the same plant species. We found using either method that phenotypic similarit was more strongly associated with feeding intensity by C. cardariae than the genetic similarity. In contrast, neither genetic nor phenotypic similarity dendrogram was significantly associated with feeding intensity by P. xylostella. The result indicates that phenotypic traits can be more reliable indicators of the feeding preference of a specialist than phylogenetic relatedness of its potential hosts. The finding has implications for the evolution and maintenance of host specialization. It also has potential implications for identifying plant species for testing during prerelease assessment of specialized biocontrol candidates.