Selection for chemical trait remixing in an invasive weed after reassociation with a coevolved specialist

Abstract

The interaction between Depressaria pastinacella (parsnip webworm) and wild parsnip (Pastinaca sativa), in its native Europe and in its longstanding nonindigenous range in the midwestern United States, is characterized by chemical phenotype matching, ostensibly mediated by reciprocal selective responses. The first appearance of D. pastinacella on P. sativa in New Zealand in 2004 provided an opportunity to quantify selective impacts of a coevolved herbivore and calibrate rates of phytochemical response in its host plant. Webworms in 2006 reduced seed production up to 75% in New Zealand populations, and in 2007 infestations increased in severity in all populations except one. Most New Zealand populations fall into a furanocoumarin phenotype cluster distinct from European and U.S. phenotypes, although one heavily attacked population clusters with two U.S. populations and one European population long associated with webworms. Multivariate selection analysis substituting realized fitness (with webworms present) for potential fitness (absent webworms) as the dependent variable revealed that reassociation with a coevolved specialist in a nonindigenous area profoundly altered the selection regime, favoring trait remixing and rapid chemical changes in parsnip populations, as predicted by the geographic mosaic theory. That uninfested populations of New Zealand parsnips contain higher amounts of octyl acetate, a floral volatile used by webworms for orientation, suggests that plants that escape from specialized enemies may also experience selection to increase kairomones, as well as to reduce allomones.

Fig. 1.

Realized fitness of wild parsnips in six N.Z. populations after consumption of reproductive parts by parsnip webworms. Average potential fitness (number of male flowers) of plants within a population is given below each pie chart. Estimates of potential fitness for many plants was not possible because webworms in addition to consuming all of the umbels had as well consumed the stalks bearing the umbels.

Fig. 2.

Clustering of 33 wild parsnip populations (involving 1,117 individuals) on the basis of average phenotypic furanocoumarin seed content; North American and European data are from Berenbaum and Zangerl (21). Populations in red have had either long-term associations with webworms [in the cases of North American, prefixed “na,” or European populations (green) from Austria, The Netherlands, or Germany, prefixed “aust,” “neth,” or “germ”] or only a recent association (between 2004 and 2006 in New Zealand, “nz”). Populations in black have had no, or only rare, interaction with webworms. Clustering is based on squared Euclidean distances (SPSS 14, Chicago, IL). Bar graphs show percent deviations (+ or −) from mean furanocoumarin content of each of six clusters for five furanocoumarins (left to right: imperatorin, bergapten, isopimpinellin, xanthotoxin, and sphondin). With one exception (nzLUMB), N.Z. populations are clustered separately from all others. Abbreviated N.Z. population names are LUMB, Lumber; TOWN, Townley; WAR, Warrington; COTT, Cottage; and OCEA, Ocean.

Fig. 3.

Differences between N.Z. and Midwest U.S. parsnips in chemical composition of buds and male flowers (means ± SE). All differences but those for cis- and trans-ocimene between countries were significant (P < 0.05) in a two-way ANOVA with country and plant part (bud or flower) as main effects. There were no significant interactions and only three compounds differed between buds and flowers: flowers were higher in octyl butyrate and lower in myristicin and cis-ocimene (data not shown).