Impact of reassociation with a coevolved herbivore on oviposition deterrence in a hostplant.

Although selection by herbivores for increased feeding deterrence in hostplants is well documented, selection for increased oviposition deterrence is rarely examined. We investigated chemical mediation of oviposition by the parsnip webworm (Depressaria pastinacella) on its principal hostplant Pastinaca sativa to determine whether ovipositing adults choose hostplants based on larval suitability and whether hostplants experience selection for increased oviposition deterrence. Webworms consume floral tissues and florivory selects for increased feeding deterrents; moths, however, oviposit on leaves of pre-bolting plants. Exclusive use of different plant parts for oviposition and larval feeding suggests oviposition should select for increased foliar deterrents. Recent webworm colonization of New Zealand (NZ) allowed us to assess phenotypic changes in foliar chemicals in response to webworm oviposition. In a common garden experiment, we compared NZ populations with and without a history of infestation from 2004 to 2006 for changes in leaf chemistry in response to oviposition. Three leaf volatiles, cis- and trans-ocimene, and ß-farnesene, elicit strong responses in female moth antennae; these compounds were negatively associated with oviposition and are likely oviposition deterrents. Leaf ß-farnesene was positively correlated with floral furanocoumarins that deter florivory; greater oviposition on plants with low floral furanocoumarins indicates that moths preferentially oviposit on parsnips most suitable for larval growth. Unlike florivory, high oviposition on leaves did not lower plant fitness, consistent with the fact that NZ parsnip foliar chemistry was unaffected by 3-6 years of webworm infestation. Thus, in this system, selection by ovipositing moths on foliar chemistry is weaker than selection by larvae on floral chemistry.

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

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.

Lutein sequestration and furanocoumarin metabolism in parsnip webworms under different ultraviolet light regimes in the montane west.

Both biotic and abiotic selection pressures can contribute to geographic variation in allelochemical production in plants. We examined furanocoumarin production in western North American populations of Heracleum lanatum and Pastinaca sativa that, at different latitudes and altitudes, experience different ultraviolet (UV) light regimes. Total furanocoumarins and linear furanocoumarins of fruits were negatively correlated with UV irradiance, whereas amounts of angular furanocoumarins, which are generally less phototoxic, were not. Another factor potentially influencing furanocoumarin production is the presence of the parsnip webworm Depressaria pastinacella, (Lepidoptera: Oecophoridae), an herbivore that feeds on reproductive structures of both plant species. These insects sequester lutein from their host plants; this carotenoid acts to ameliorate furanocoumarin toxicity. Although the concentration of lutein in fruits did not vary with UV irradiance, lutein sequestration by sixth instars was positively correlated with UV irradiance. Webworm populations are variably infested with the polyembryonic webworm parasitoid Copidosoma sosares Walker (Hymenoptera: Encyrtidae). H. lanatum fruits from populations with webworms parasitized by C. sosares had lower concentrations of furanocoumarins, with the exception of sphondin, than fruits from plants infested with webworms free from parasitism. Lower levels of these furanocoumarins may reduce negative effects on the fitness of this parasitoid. In contrast with the variation in furanocoumarin content, the ability of webworms to metabolize furanocoumarins by cytochrome P450 did not differ significantly among populations from New Mexico to Alberta.

Parsnip webworms and host plants at home and abroad: trophic complexity in a geographic mosaic.

Due to differences in the structure of communities in which interactions are embedded, the intensity of interactions between species may vary with location; thus, what results from differences in outcomes and in degree of specialization is a geographic mosaic, which provides the raw material for divergent coevolutionary trajectories. Where selection intensity is great, reciprocal responses are likely in so-called "hotspots"; in contrast, where selection pressures are relaxed, reciprocal responses in "coldspots" are far less likely to occur. There are few if any studies examining how a gradient of increasing trophic complexity might influence the probability of phenotype matching and, correspondingly, the "temperature" of the coevolutionary interaction. This study was conducted to compare outcomes of the interaction between wild parsnip (Pastinaca sativa) and parsnip webworm (Depressaria pastinacella) in its indigenous area, Europe, to its area of introduction, the midwestern United States. Specifically, we tested the hypothesis that increasing trophic complexity, represented by alternate host plants or the presence of natural enemies, reduces the selective impact of parsnip webworms and hence diminishes linkage between host plant chemistry and webworms that would be expected in coevolutionary hotspots. This comparison of a two-species interaction in its area of introduction and its area of indigeneity revealed common patterns that are more reflective of interaction temperature than of continental origin. Where webworms are rare, parsnips produce lower levels of xanthotoxin and bergapten in both the midwestern United States and Netherlands populations. However, the most striking result from this intercontinental comparison is that what is a ubiquitous two-species interaction in North America is in fact exceptional in Europe; webworms could more reliably be found infesting H. sphondylium even where P. sativa was available as well. This preference for H. sphondylium exists despite the comparatively high probability of parasitism associated with this host plant and may reflect the overall lower furanocoumarin content of H. sphondylium. The interaction of parsnip webworms and wild parsnips at home and away demonstrates clearly the potential for rapid contemporary evolution of chemical traits upon re-association with a coevolved enemy, a potential evolutionary outcome that should be considered in the design and implementation of future weed biological control programs.

Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore.

The ability of weeds to proliferate into nonindigenous habitats has been attributed to escape from their native natural enemies, allowing reallocation of resources from chemical defense into growth and reproduction. Many invasive weeds, however, eventually encounter their native, coevolved enemies in areas of introduction. Examination of herbarium specimens of an invasive phototoxic European weed, Pastinaca sativa, through 152 years reveals phytochemical shifts coincident in time with the accidental introduction of a major herbivore, the parsnip webworm, Depressaria pastinacella. Plants collected before the introduction of webworms in North America and during the earliest stages of establishment (1850-1889) are lower in toxic furanocoumarins than all plants subsequently collected in North America and lower than European plant samples collected before 1889. Thus, introduction of a major specialist herbivore can increase noxiousness of a species in its area of introduction, illuminating a potential consequence of classical biocontrol programs involving insect herbivores and poisonous weeds.