Selection for chemical trait remixing in an invasive SPECIAL FEATURE weed after reassociation with a coevolved specialist A. R. Zangerl*, M. C. Stanley†, and M. R. Berenbaum*‡ *Department of Entomology, 320 Morrill Hall, University of Illinois at Urbana-Champaign, 505 South Goodwin, Urbana, IL 61801-3795; and †School of Biological Sciences, The University of Auckland, Private Bag 92019, Auckland Mail Centre, Auckland 1142, New Zealand Edited by Jerrold Meinwald, Cornell University, Ithaca, NY, and approved December 19, 2007 (received for review November 1, 2007) The interaction between Depressaria pastinacella (parsnip web- predictable because the decoupling of defense and herbivory worm) and wild parsnip (Pastinaca sativa), in its native Europe and that has been observed in interactions between invasive plants in its longstanding nonindigenous range in the midwestern United and indigenous herbivores (11) is less likely to occur upon States, is characterized by chemical phenotype matching, ostensi- reassociation with a coevolved specialist. Whereas compelling bly mediated by reciprocal selective responses. The first appear- evidence for rapid contemporary evolution of size, fecundity, ance of D. pastinacella on P. sativa in New Zealand in 2004 provided and leaf area of invasive plant species has been found (12), the an opportunity to quantify selective impacts of a coevolved her- potential for evolutionary change of chemical traits, upon which bivore and calibrate rates of phytochemical response in its host resistance may be based, upon reassociation with a coevolved plant. Webworms in 2006 reduced seed production up to 75% in enemy has yet to be explicitly evaluated. The geographic mosaic New Zealand populations, and in 2007 infestations increased in theory of coevolution (2) specifically predicts rapid reciprocal severity in all populations except one. Most New Zealand popu- responses, including trait remixing, to result from intense selec- lations fall into a furanocoumarin phenotype cluster distinct from tion exerted by a reassociated coevolved specialist, and historical European and U.S. phenotypes, although one heavily attacked evidence (13) is suggestive of such responses. population clusters with two U.S. populations and one European A system in which the chemical consequences of reassociation population long associated with webworms. Multivariate selection with a coevolved herbivore may be examined involves the analysis substituting realized fitness (with webworms present) for introduced Eurasian weed Pastinaca sativa, wild parsnip, and its potential fitness (absent webworms) as the dependent variable European insect associate Depressaria pastinacella, the parsnip revealed that reassociation with a coevolved specialist in a non- webworm. This interaction has been well characterized within its indigenous area profoundly altered the selection regime, favoring native range in Europe and in its introduced range in North trait remixing and rapid chemical changes in parsnip populations, America, and the ecological effects of a diversity of plant as predicted by the geographic mosaic theory. That uninfested chemicals on the principal specialized herbivore have been populations of New Zealand parsnips contain higher amounts of determined. Brought to America by the earliest colonists, the octyl acetate, a floral volatile used by webworms for orientation, parsnip was ‘‘common’’ by 1630 (14). Escaped from cultivation, suggests that plants that escape from specialized enemies may also it is regarded as noxious because all aerial parts produce EVOLUTION experience selection to increase kairomones, as well as to reduce furanocoumarins, phototoxic allomones that, on contact with allomones. human skin, cause blistering and hyperpigmentation (15). Very few native North American insects have colonized P. sativa (16); insect–plant interactions ͉ Lepidoptera ͉ Pastinaca sativa ͉ parsnip currently, the principal (and occasionally only) herbivore webworm ͉ herbivore throughout its range in North America is D. pastinacella,acci- dentally introduced from Europe and first reported in 1869 in Ontario, Canada (17). D. pastinacella webs together and feeds on lthough the ability of herbivorous insects to act as selective the reproductive structures of species in the closely allied genera agents on the chemistry of their host plants is an essential A Pastinaca and Heracleum; since their introduction, webworms component of coevolutionary theory (1, 2), experimental dem- have become established widely in North America (18). onstrations of such impacts are few (3–5). Accordingly, some Certain furanocoumarins in wild parsnip function as resis- skepticism remains as to the efficacy of herbivores as selective tance factors against webworms in North America (19, 20) and agents (6), and alternative explanations, including top-down Europe (21). Webworm damage in the Midwest United States selection from natural enemies of herbivores, have proliferated selects for increased concentrations of three furanocoumarins: (albeit also without an abundance of experimental demonstra- xanthotoxin, bergapten, and sphondin (3, 20). Genotypes with tions). In addition to its importance in a theoretical context, high levels of these furanocoumarins experience lower fitness in quantifying selection and rates of response is critical for evalu- the absence of herbivores than genotypes with lower furanocou- ating the stability of host-plant resistance traits in agricultural marin content (22), indicative of a cost of producing these crops as well as the sustainability of classical biocontrol of weeds. compounds. These three furanocoumarins act as resistance One way to examine the rate and magnitude of evolutionary factors in part because webworms metabolize them less effi- change in phytochemical profiles in response to insect herbivory ciently by cytochrome P450 monooxygenases (23). In both is to examine an interaction involving coevolved species that are Europe and North America, interactions between parsnip separated and then, by sequential range extensions, reassociated. Reassociation with a specialized coevolved enemy in an area of nonindigeneity is likely to have a profound and more predictable Author contributions: A.R.Z. and M.R.B. designed research; A.R.Z. performed research; effect on host-plant chemistry. Although little quantitative and M.C.S. contributed new reagents/analytic tools; A.R.Z. and M.R.B. analyzed data; and A.R.Z. ecologically relevant information is available on phytochemical and M.R.B. wrote the paper. changes in plants that occur after introduction into a nonindig- The authors declare no conflict of interest. enous area and release from interactions with longtime insect This article is a PNAS Direct Submission. associates (7–10), even less information is available on phyto- ‡To whom correspondence should be addressed. E-mail: [email protected]. chemical changes that ensue when coevolved enemies that are This article contains supporting information online at www.pnas.org/cgi/content/full/ demonstrated reciprocal selective agents resume interacting with 0710280105/DC1. a host plant in an area of invasion. Such changes should be more © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0710280105 PNAS ͉ March 25, 2008 ͉ vol. 105 ͉ no. 12 ͉ 4547–4552 Downloaded by guest on September 27, 2021 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. webworms and wild parsnips are characterized by chemical near the center of the outbreak in the city of Dunedin were phenotype matching: close correspondence between furanocou- heavily infested in 2006: Crimp, Lumber, and Townley. A fourth marin defense profile of the plants and detoxification capacity of population, Warrington, at the northern edge of the range and the webworms. Ϸ15 km from the presumed point of introduction [Port Chalmers Before the appearance of webworms in North America, (25)], was lightly infested. By 2007, the northernmost edge of the parsnips exhibited reduced furanocoumarin defenses in com- range extended 5 km to include two additional populations of parison with contemporaneous European parsnips, as deter- wild parsnip (Rock and Ocean). mined by examination of herbarium specimens collected in Webworms in 2006 removed half or more of the total fitness North America over 152 years spanning the period before of Ϸ50% of the plants in the Crimp and Townley populations and introduction of webworms to the present, and European speci- eliminated seed production by Ͼ75% of the plants in the Lumber mens from the 19th century to the present, for webworm damage population (Fig. 1). In 2007, infestation severity increased in all and furanocoumarin content (24). Concomitant with the rise in of these populations except Crimp; 75% of the plants in the webworm infestation between 1890 and 1909, levels of all five Lumber and Townley populations failed to produce seed, and furanocoumarins (those previously associated with resistance as nearly half of the Warrington plants, only lightly infested in 2006, well as imperatorin and isopimpinellin) increased significantly failed to produce seeds. and continued to increase thereafter.