Evolution of diabroticite rootworm beetle (Chrysomelidae) receptors for Cucurbita blossom volatiles.

Abstract

The diabroticite rootworm beetles coevolved with plants of the family Cucurbitaceae as demonstrated by their feeding dependence on the tetracyclic triterpenoid cucurbitacins. These beetles also exhibit strong attraction to phenylpropanoid volatile components of Cucurbita blossoms. A mixture of 1,2,4-trimethoxybenzene, indole, and (E)-cinnamaldehyde, all blossom components, is highly attractive to the several species of diabroticite cucumber beetles and corn rootworms and is considered a simplified Cucurbita blossom kairomone odor. The evolutionary divergence in antennal receptor complementarity is best understood by comparing the species-specific responses of several Diabrotica to structural analogues of (E)-cinnamaldehyde, the major attractant for Diabrolica undecimpunctata howardi. Cinnamyl alcohol is a strong attractant for Diabrotica barberi, and 4-methoxycinnamaldehyde is an exceptional attractant for Diabrotica virgifera. The very closely related species D. barberi and Diabrotica cristata are most strongly attracted to 4-methoxyphenethanol, which is unattractive to the other species studied.The blossoms of Cucurbitaceae are well known to be highly attractive to many species of diabroticite rootworm beetles, including such major pests as the northern corn rootworm Diabrotica barberi Smith and Lawrence, the southern corn rootworm Diabrotica undecimpunctata howardi Barber, the western corn rootworm Diabrotica virgifera virgifera LeConte, the banded cucumber beetle Diabrotica balteata Leconte, and the striped cucumber beetle Acalymma vittatum (Fabricius) (1)(2)(3)(4). The aggregations of diabroticite beetles in Cucurbita blossoms are the result of the concerted attraction from an array of blossom volatiles that increases the arrival rate, acting together with the singular arrestant and phagostimulant properties of the tetracyclic triterpenoid cucubitacins in the blossoms that delay departure (2, 4-7). The blossoms of Cucurbita maxima produce an array of >40 volatile chemicals (1, 2), and 22 of these chemicals have been identified by MS (8). Extensive field evaluations have shown that at least 10 of the volatile compounds are attractive to adults of both sexes of the diabroticite rootworms (4, 9).Most of the highly attractive Cucurbita volatiles are phenylpropanoids, C6C3 compounds formed in the shikimic acid pathway through phenylalanine to cinnamic acid (10). Phenylpropanoids are produced from cinnamic acid in relatively large amounts during pollen maturation in blossoms (11,12). Thus, the remarkable long-range attraction of many species of diabroticites to the blossoms of Cucurbitaceae implies that the original coevolutionary association between Cucurbitaceae and diabroticites (5) was that of pollen seeking and consequent fertilization. Coleoptera are considered to be the most primitive pollinators of angiosperms and were probably associated with open bowl-shaped flowers, where the beetles fed on floral secretions, nectar, and pollen (13).All of the diabroticite species examined are attracted to chem...

Volatile semiochemical impact on trapping and distribution in maize of northern and western corn rootworm beetles (Coleoptera: Chrysomelidae)

“…These results are consistent with those of an earlier study conducted in South Dakota that showed no attraction to 4-methoxyphenethanol before maize reached late dough to early dent stage, when it captured fewer D. barberi than did eugenol (Hesler et al, 1994). Both sets of results contrast with reports of high potency of 4-methoxyphenethanol in studies conducted in more easterly maize-growing regions in the U.S.A. (Metcalf & Lampman, 1991;Metcalf et al, 1995). Hesler et al (1994) hypothesized that geographical variation among populations accounts for the discrepancy and discussed other traits for which differences have been documented among geographically separated D. barberi populations.…”

“…To my knowledge, the amine, unlike 2-phenyl-1-ethanol (Flath et al, 1978;Andersen & Metcalf, 1987), occurs in neither maize nor Cucurbitaceae, a group that probably includes ancestral hosts of diabroticite corn rootworms and has yielded many compounds affecting rootworm behaviours (Metcalf & Metcalf, 1992;Metcalf & Lampman, 1997). Metcalf & Lampman (1991) provisionally attributed attractiveness of the amine to its interaction with antennal receptors attuned to the structurally related alcohol; however, the confirmation of synergy between the amine and alcohol, at least during later maize reproductive stages, does not support this interpretation, especially when combined with results of earlier computational chemistry analyses (Petroski & Hammack, 1998).…”

“…This change in dispenser design was made to facilitate placement and removal of multiple semiochemical sources within field plots. Semiochemical release rates from this dispenser were estimated gravimetrically by methods generally similar to those of Metcalf & Lampman (1991). However, because of absorbency of the paper discs and relative humidity variation during testing, the mean weight of four odouranttreated dispensers was adjusted for any change in the mean weight of four simultaneously exposed, control dispensers that lacked odourant.…”

“…Positive results are lacking for D. barberi (Lance, 1988ab), although more effective lures than the eugenol used in earlier studies are now available. For example, 2-phenyl-1-ethylamine proved highly effective by itself (Metcalf & Lampman, 1991) and appeared to synergistically increase capture of D. barberi beetles when dispensed with 2-phenyl-1-ethanol (Petroski & Hammack, 1998). 4-Methoxyphenethanol [2-(4-methoxyphenyl)ethanol] is also reported to be a potent attractant for D. barberi (Metcalf & Lampman, 1991;Metcalf et al, 1995), although not all tests confirm its efficacy (Hesler et al, 1994).…”

Pollinator and Herbivore Attraction to Cucurbita Floral Volatiles

“…Plants are monoecious with separate male and female flowers that last for 1 day, opening before sunrise and wilting by early afternoon (McGregor 1976). The scent of male and female Cucurbita blossoms attracts Acalymma vittatum Fabricius (striped cucumber beetle, Chrysomelidae) (Andersen and Metcalf 1986;Lewis et al 1990;Metcalf and Lampman 1991;Metcalf et al 1995;Granero et al 2004;Ferrari et al 2006), a specialist herbivore that is responsible for extensive damage to northeastern cucurbit crops (Hoffmann et al 1996). Leaves and roots of some Cucurbita species also produce volatiles that may attract cucumber beetles and other insects (Peterson et al 1994;Cosse and Baker 1999).…”