Chemical phenotype matching between a plant and its insect herbivore

Abstract

Two potential outcomes of a coevolutionary interaction are an escalating arms race and stable cycling. The general expectation has been that arms races predominate in cases of polygenic inheritance of resistance traits and permanent cycling predominates in cases in which resistance is controlled by major genes. In the interaction between Depressaria pastinacella, the parsnip webworm, and Pastinaca sativa, the wild parsnip, traits for plant resistance to insect herbivory (production of defensive furanocoumarins) as well as traits for herbivore "virulence" (ability to metabolize furanocoumarins) are characterized by continuous heritable variation. Furanocoumarin production in plants and rates of metabolism in insects were compared among four midwestern populations; these traits then were classified into four clusters describing multitrait phenotypes occurring in all or most of the populations. When the frequency of plant phenotypes belonging to each of the clusters is compared with the frequency of the insect phenotypes in each of the clusters across populations, a remarkable degree of frequency matching is revealed in three of the populations. That frequencies of phenotypes vary among populations is consistent with the fact that spatial variation occurs in the temporal cycling of phenotypes; such processes contribute in generating a geographic mosaic in this coevolutionary interaction on the landscape scale. Comparisons of contemporary plant phenotype distributions with phenotypes of herbarium specimens collected 9-125 years ago from across a similar latitudinal gradient, however, suggest that for at least one resistance trait-sphondin concentration-interactions with webworms have led to escalatory change.

Figure 1

Collection year and location of herbarium specimens of wild parsnip from which seed furanocoumarins (isopimpinellin, xanthotoxin, and sphondin) were quantified, as well as locations of Illinois populations included in the study. Not shown are three specimens collected in 1889, 1916, and 1989, respectively, with origin labeled simply as “Illinois” and one specimen (1941) with origin labeled simply as “Michigan”.

Figure 2

Mean (±SD) furanocoumarin content (μg/mg) of wild parsnip seeds and furanocoumarin metabolism (nmol/min) by parsnip webworm larvae from four midwestern U.S. populations. Furanocoumarins for which significant differences were found between populations by one-way ANOVA (P < 0.05) are indicated by ∗.

Figure 3

Three-dimensional representation of the four clusters including both plant and insect phenotypes (each point represents a single plant or insect). Cluster analysis was performed to identify groups of chemically similar phenotypes in webworm detoxification and plant furanocoumarin production. Before cluster analysis, insect metabolism rates and plant furanocoumarin contents were standardized to a mean of one by dividing each individual value by the raw mean value across all populations. Clusters were produced by Proc fasclus Version 6.12 (SAS Institutes, Cary, NC). Proc candisc was used to generate three canonical variables (CAN1, CAN2, and CAN3) from the cluster analysis output for use in plotting the four clusters in three-dimensional space.

Figure 4

Characterization of the four clusters shown in Fig. 2 in terms of average furanocoumarin content (plants) and average furanocoumarin metabolism (insects).

Figure 5

Phenotype frequency distributions of insects and plants for each of the four populations. The χ² values are from likelihood-ratio estimates testing the hypothesis that the two distributions are the same (See Table 1); ∗ denotes a significant mismatch between plant and insect patterns.

Figure 6

Two-dimensional plots of furanocoumarin concentration (μg/mg) of seeds from herbarium specimens (•) and from the four study populations (○).