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Ecology |
Biology Department, The Pennsylvania State University, University Park, Pennsylvania, USA; and 3Department of Entomology, The Pennsylvania State University, University Park, Pennsylvania, USA
Received for publication May 24, 2006. Accepted for publication October 2, 2006.
ABSTRACT
Self-pollination by plants gives rise to inbreeding depression. There is increasing recognition that plant inbreeding can have significant implications for interactions between plants and other organisms, including insects and pathogens. Many of these interactions are mediated by plant-derived volatiles, but the effects of inbreeding on volatile production have not previously been investigated. We examined variation in flower volatile production by the wild gourd Cucurbita pepo subsp. texana as a function of inbreeding, sex of the flower, and maternal line. We compared first-generation selfed progeny to outcrossed progeny to assess variation in blossom volatiles due to mating system. Our data indicate that self-pollination reduces total volatile production and changes the relative composition of individual compounds released by C. pepo subsp. texana blossoms. These findings have potentially important implications for interactions between C. pepo subsp. texana and its pollinators and herbivores—including diabroticite cucumber beetles, which vector the bacterial pathogen Erwinia tracheiphila—because previous studies have shown that a number of the individual compounds that vary with inbreeding level can influence insect behavior. We also found significant differences between the volatile profiles of male and female flowers and across maternal families.
Key Words: Cucurbita pepo subsp • texana • flower volatiles • inbreeding • insect behavior • plant volatiles • wild gourd
Self-pollination (inbreeding) is common among flowering plants and has a major impact on fitness. More than half of all species are estimated to self-pollinate 20% or more of the time (Barrett and Eckert, 1990
; Vogler et al., 1999
). Inbreeding reduces heterozygosity, thereby exposing deleterious recessive alleles to selection and simultaneously decreasing the contribution of overdominance to fitness; as a result, most species have a significant loss of fitness associated with inbreeding (e.g., Charlesworth, 1987; Husband, 1996; Crnokrak, 2002
). Although inbreeding depression—the reduction in fitness of inbred progeny relative to outbred progeny—is often considered to be a trait of the population at a given point in time, there is now substantial evidence that inbreeding depression can vary among family lines within populations, suggesting that there is genetic variation for inbreeding depression (Uyenoyama, 1993
; Dudash, 1997
; Vogler et al., 1999
). Moreover, the magnitude of inbreeding depression can vary with environmental conditions (Stephenson et al., 2004
; Hayes et al., 2005a
).
Recently, researchers have begun to explore the effects of inbreeding on ecological interactions between plants and other organisms. Inbreeding has been shown to affect both host plant quality and defenses, which in turn can influence the foraging behavior of arthropods. Inbred populations of Silene latifolia produced less nectar for potential pollinators (Ouborg et al., 2000
). Similarly, inbred Mimulus guttatus plants received fewer visits from pollinators (Ivey and Carr, 2005
). In this same Mimulus system, spittlebug development was affected significantly by inbreeding of the host plant (Carr and Eubanks, 2002
). In another system, specialist herbivores (tortoise beetles) performed significantly better when reared on outcrossed Ipomoea hederacea var. integriuscula, while generalist herbivores (aphids) performed better on inbred plants (Hull-Sanders and Eubanks, 2005
). In Cucurbita pepo subsp. texana (A. Gray) Filov (Cucurbitaceae), inbred plants suffered higher levels of damage by cucumber beetles and had a higher incidence of aphid-transmitted viral diseases than outcrossed plants (Hayes et al., 2004
; Stephenson et al., 2004
). In the same fields, however, outcrossed plants had higher rates of infection by the beetle-vectored bacterial pathogen, Erwinia tracheiphila (Smith, 1895; Ferrari, 2006).
The mechanisms by which inbreeding affects plant–insect interactions remain little known (Carr and Eubanks, 2002
). Many interactions between plants and insects are mediated by volatile chemical compounds that plants release as part of their normal physiological activity and specifically in response to herbivory and other environmental stressors (Turlings et al., 1990
; De Moraes et al., 1998
, 2001
; Pichersky and Gershenzon, 2002
; De Moraes and Mescher, 2004
). Yet, to our knowledge, the effects of inbreeding on the expression of plant volatiles have not previously been explored. In this study, we examined the effects of inbreeding on floral volatile production in the wild gourd, Cucurbita pepo subsp. texana, an annual monoecious vine native to Texas and adjacent states that is thought to be the wild progenitor of the cultivated squashes (Decker and Wilson, 1986
; Kirkpatrick and Wilson, 1988
). Volatiles associated with flowers and nectar influence plant–insect interactions by serving as environmental cues for beneficial and harmful floral visitors including pollinators, nectar robbers, and florivores (Galen, 1999
; Raguso, 2001
, 2004a
, b). They may also have indirect effects on plant fitness through antimicrobial activity or by acting as cues for natural enemies of herbivores (Pichersky and Gershenzon, 2002
; Raguso, 2004b
).
In the wild, C. pepo subsp. texana has a mixed mating system, producing both selfed and outcrossed progeny. Kohn and Biardi (1995)
found that 73% of seeds of the closely related C. foetidissima, which grows in ecologically similar habitats, were produced through self-fertilization. Population genetic theory predicts that the magnitude of inbreeding depression should decrease over time with continuously high rates of selfing, as deleterious recessive alleles are purged from the population by selection against homozygotes (Lande and Schemske, 1985
). However, selfed C. pepo subsp. texana have reduced fitness for a range of traits including pollen performance (Stephenson et al., 2001
; Hayes et al., 2005b
), male and female flower production, and fruit number and mass (Stephenson et al., 2004
; Hayes et al., 2005b
).
Cucurbita species have large yellow flowers that produce several volatile compounds that presumably function in pollinator (e.g., squash bee) attraction. The floral volatiles, however, are also attractive to cucumber beetles (important herbivores) over relatively large distances (Andersen and Metcalf, 1986
, 1987
; Metcalf and Lampman, 1991
). Different species of cucumber beetles have been shown to discriminate among the volatile compounds of Cucurbita (squash) varieties (Andersen and Metcalf, 1987
; Lampman and Metcalf, 1988
), establishing a genetic basis for variation in attractiveness among artificially selected lines. Volatile profiles between male and female flowers varied within three varieties of cultivated zucchini (C. pepo subsp. pepo; Mena Granero et al., 2005
). Sources of variation in volatile production in wild (free-living) Cucurbita have received comparatively little attention.
We examined variation in volatile production in blossoms of a wild species, C. pepo subsp. texana, as a function of inbreeding, sex, and maternal family. We compared first generation selfed progeny to outcrossed progeny to assess variation in blossom volatiles due to mating system. Because many important measures of plant fitness (herbivory, pathogen exposure, and pollination) are mediated through insect responses to volatile cues, understanding the sources of variation in the population provides insights into the range of phenotypes upon which selection can act.
MATERIALS AND METHODS
Plants
An experimental population of C. pepo subsp. texana was initiated from seeds sampled randomly from a natural population in Texas, U.S.A. A random sample of five F = 0 progeny was used to found five maternal lines, and the remaining lines were reserved as potential pollen donors. A multiyear crossing program was used to generate plants with a range of inbreeding coefficients to study inbreeding depression in numerous traits (Stephenson et al., 2001
, 2004
; Hayes et al., 2004
; Hayes et al., 2005a
, b
, c
). To test for the effect of inbreeding on blossom volatiles, we grew six selfed (self-pollination on an outbred parent, F = 0.5) and six outcrossed (F = 0) plants of C. pepo subsp. texana from each of three maternal lines (I2, E3, and I3A) in 1-L pots. Plants were potted in peat-based general purpose potting mix (Promix, Premier Horticulture, Quakertown, Pennsylvania, USA) with time-release fertilizer. Plants began flowering 4 wk after germination and produced one flower (either staminate or pistillate) at most nodes. The large yellow flowers open in the morning and senesce at mid-day. In general, staminate flowers are produced prior to pistillate flowers.
Volatile collection and analysis
We selected one male and one female flower from each plant at random for volatile collection and analysis. (For a balanced design, we collected from five male and five female flowers in each family–breeding combination.) We collected volatiles from intact live male and female flowers using a closed push/pull system (Analytical Research Systems, Gainesville, Florida, USA). Individual flowers were isolated, while attached to the vine, in a glass dome chamber (15 cm tall x 16 cm diameter) with a Teflon base consisting of two sliding plates that when pushed together left a hole for the vine to pass. A cotton ball was wrapped around the vine to fill space between the base and plant and to allow air to exit. Filtered air was pumped into the chamber (3.0 l/min) through Teflon tubing and pulled out of the chamber (1.0 L/min) through side ports and across traps containing 40 mg of adsorbent SuperQ (Alltech, Deerfield, Illinois, USA). Volatile collections were made for the duration of the period in which blossoms were open (0600 to 1300 hours).
Super-Q traps were rinsed with 150 µL of dichloromethane; 5 µL of n-octane (40 ng/µL) and n-nonyl-acetate (80 ng/µL) were added as internal standards. Volatiles were analyzed by gas chromatography with a Hewlett-Packard (Palo Alto, California, USA) model 6890 gas chromatograph (GC) with flame ionization detector (FID. Samples (1 µL) were injected with a splitless injector held at 240°C in the GC/FID. The column (15 m x 0.25 mm OV 101 methyl silicon, Agilent Technologies, Palo Alto, California, USA) was maintained at 35°C for 0.5 min and then increased 12°C per min to 180°C. Quantifications of compounds were made relative to the internal standard using Enhanced ChemStation software (Agilent Technologies). Identifications of volatile compounds were confirmed by comparing retention times and mass spectra to commercial standards analyzed by GC-MS using electron ionization. For more details, see De Moraes and Mescher (2004)
.
We analyzed the volatile profile for a subset of volatiles with a multivariate analysis of variance using the Wilks test statistic. We analyzed concentrations of total volatiles (peak area) and individual compounds using a multifactor ANOVA with maternal line, breeding, and sex as fixed effects. Post-hoc tests of effects within maternal lines were conducted using t tests of linear contrasts. Volatile concentrations were Box–Cox transformed prior to analysis to approximate normality. All statistical analyses were conducted using the R programming language (http://www.r-project.org).
RESULTS
The total amount of volatiles produced by flowers on outcrossed plants was significantly greater than that produced by flowers from selfed plants (P < 0.01). Further, there were significant differences in the total volatiles produced between the three maternal families (P < 0.01) indicating that there is broadsense heritability for volatile production among the three families sampled. Within the three maternal families, outcrossed plants produced more total volatiles, though the effect was significant only for family E3 (Fig. 1). The total quantity of volatiles produced by male and female flowers did not differ significantly. In addition, there was large individual variation in many of the compounds recovered (Table 1), with some peaks absent in many samples. We restricted our analyses of individual compounds to the five peaks (of 20 total compounds identified) found most consistently across all samples—1,4-dimethoxybenzene, 1,2,4-trimethoxybenzene, ß-caryophyllene, linalool, and (Z)-jasmone—as well as (3E)-4,8-dimethyl-1,3,7-nonatriene, which was often absent in selfed plants, but consistently found in outcrossed plants. We found significant differences in the volatile profiles among maternal families, sex of the flower, and breeding (Table 2; Appendix). There was also a significant interaction between sex and breeding (Table 2) indicating that inbreeding differentially affects male and female flowers. The significant sex and sex by breeding effects reflect differences in relative concentrations because these effects were not significant in the univariate analysis of total volatile production (Table 1).
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Self-fertilization is common in flowering plants in general (Barrett and Eckert, 1990
; Vogler et al., 1999
), and in Cucurbita specifically (Kohn and Biardi, 1995
). Our data indicate that self-fertilization reduces total volatile production and changes the relative composition of individual compounds released by C. pepo subsp. texana blossoms. The observed reduction of overall volatile production due to self-fertilization was consistent, though not always significant, across the three maternal families. Total volatile production was similar in male and female flowers, though the volatile composition between sexes differed significantly, in line with observations of sex-specific differences in cultivated varieties of C. pepo (Mena Granero et al., 2005
).
Outcrossed plants produced significantly more linalool, 1,4-dimethoxybenzene, and (3E)-4,8-dimethyl-1,3,7-nonatriene. The effects on total volatile production were dominated by 1,4-dimethoxybenzene, which accounted for >80% of blossom volatiles. In zucchini, flower nectar has been shown to be the main source of this compound (Mena Granero et al., 2005
), which is an attractant of diabroticite beetles. These beetles include many important herbivores of Cucurbita (e.g., Metcalf and Lampman, 1989
; Ventura et al., 2000
). Linalool, which was prevalent in outcrossed but not in selfed plants is also a nectar odorant that is important in bee-pollinated plants (Blight et al., 1997
). The third compound that was consistently higher in outcrossed plants, (3E)-4,8-dimethyl-1,3,7-nonatriene, has previously been shown in other species to play a role in attracting natural enemies of plant herbivores including parasitoids and predatory mites (e.g., Dicke et al., 1990
; De Moraes et al., 1998
; D'Alessandro and Turlings, 2005
).
There was considerable variation in the effect of inbreeding on the production of blossom volatiles. In general, outcrossed individuals tended to produce more of all the volatiles measured; however, 1,2,4-trimethoxybenzene levels in female flowers and (Z)-jasmone and ß-caryophyllene in male flowers were notably higher in selfed plants. The compound 1,2,4-trimethoxybenzene is a major component of a simplified Curcubita blossom odor that is highly attractive to several species of diatrobrite cucumber beetles and corn rootworms (Metcalf and Lampman, 1991
), while ß-caryophyllene has been shown to play a role in attracting natural enemies of plant herbivores (e.g., Dicke et al., 1990
; De Moraes et al., 1998
; D'Alessandro and Turlings, 2005
; Rasmann et al., 2005
). Further, there were significant differences in the volatiles produce by male and female flowers. Variation in volatile production by male and female flowers has previously been implicated in the relatively lower attractiveness of female flowers to pollinators (Ashman et al., 2005
).
These findings demonstrate that inbreeding can affect blossom volatile production. We speculate that the increases in homozygosity that accompany inbreeding—and the consequent expression of previously masked deleterious recessives—could have adverse affects on any of the several hundred genes that are known to be expressed in the biochemical pathways leading to volatile synthesis and emission (Arimura et al., 2000
; Mercke et al., 2004
; Schnee et al., 2006
). In addition, several mutations are known that directly alter the type of volatile compounds produced by plants or the magnitude of their production (Arimura et al., 2000
; Mercke et al., 2004
; Schnee et al., 2006
). Furthermore, the decreases in general plant vigor (e.g., growth rate, nutrient uptake rates) that are typically associated with inbreeding (Charlesworth and Charlesworth, 1987
; Husband and Schemske, 1996) could indirectly affect volatile production by decreasing the resources and energy available for their synthesis. Moreover, because inbreeding depression is usually greater under field conditions than under greenhouse conditions (e.g., McCall et al., 1989; Dudash, 1990
; Wolfe, 1993
; Cheptou et al., 2000
), our findings probably underestimate the differences in volatile production that might be expected in the field.
Under field conditions, reductions in blossom-volatile production with inbreeding could reduce fitness by reducing the attraction of pollinators or beneficial predators to the blossoms. Several volatile blossom compounds in Cucurbita spp. (e.g., indole, cinnamaldehyde, 1,2,4-trimethoxybenzene) are highly attractive to cucumber beetles (Metcalf and Lampman, 1991
) and affect the distribution of beetles on plants in the field (Andersen and Metcalf, 1987
). Other volatile compounds found in Cucurbita spp. blossoms (e.g., (E)-ß-ocimene, (3E)-4,8-dimethyl-1,3,7-nonatriene, and 
-farnesene), however, are known in other plant species to attract predaceous arthropods that can attack herbivores (Dicke et al., 1990
; Scutareanu et al., 1997
).
Conversely, the reduction in floral volatiles associated with inbreeding might be expected to increase fitness if the plants become less attractive to nectar robbers, florivores, or other herbivores. However, Stephenson et al. (2004)
found increased levels of leaf damage by cucumber beetles (Acalymma vittata and Diabrotica undecimpunctata subsp. howardii) in inbred Cucurbita pepo subsp. texana. In the same fields, outcrossed plants had higher rates of infection by the beetle-vectored bacterial pathogen, Erwinia tracheiphila than did the inbred plants, despite the lack of a significant difference in resistance after a standardized, experimental inoculation (Ferrari, 2006
). In light of the data presented here, it is reasonable to hypothesize that outcrossed C. pepo subsp. texana plants may be less susceptible to herbivory by cucumber beetles, but may experience greater exposure to the pathogen because more beetles are attracted to outcrossed plants because of their greater production of flower volatiles.
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1 The authors thank J. F. Tooker and J. H. Tumlinson for helpful comments on the manuscript. The project was supported by the David and Lucile Packard Foundation and the Arnold and Mabel Beckman Foundation. 
2 Author for correspondence (e-mail: czd10{at}psu.edu
), phone: (814) 863-2867, fax: (814) 865-3048
LITERATURE CITED
Andersen J. F. Metcalf R. L.. 1986. Identification of a volatile attractant for Diabrotica (Coleoptera, Chrysomelidae) and Acalymma (Coleoptera, Chrysomelidae) spp. from blossoms of Cucurbita maxima duchesne. Journal of Chemical Ecology 12: 687-699.[CrossRef][ISI]
Andersen J. F. Metcalf R. L.. 1987. Factors influencing distribution of Diabrotica spp. (Coleoptera, Chyrsomelidae) in blossoms of cultivated Cucurbita spp. Journal of Chemical Ecology 13: 681-699.[CrossRef][ISI]
Arimura G. Ozawa R. Shimoda T. Nishioka T. Boland W. Takabyashi J.. 2000. Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406: 512-515.[CrossRef][Medline]
Ashman T. L. Bradburn M. Cole D. H. Blaney B. H. Raguso R. A.. 2005. The scent of a male: the role of floral volatiles in pollination of a gender dimorphic plant. Ecology 86: 2099-2105.[CrossRef][ISI]
Barrett S. C. Eckert C. G.. 1990. Variation and evolution of mating systems in seed plants. In S. Kawano [ed.], Biological approaches and evolutionary trends in plants 229-254 Academic Press, New York, New York, USA.
Blight M. M. LeMetayer M. Delegue M. H. P. Pickett J. A. Marion Poll F. Wadhams L. J.. 1997. Identification of floral volatiles involved in recognition of oilseed rape flowers, Brassica napus by honeybees, Apis mellifera. Journal of Chemical Ecology 23: 1715-1727.[CrossRef][ISI]
Carr D. E. Eubanks M. D.. 2002. Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Scrophulariaceae). Evolution 56: 22-30.[CrossRef][ISI][Medline]
Charlesworth D. Charlesworth B.. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18: 237-268.[CrossRef][ISI]
Cheptou P. O. Berger A. Blanchard A. Collin C. Escarre J.. 2000. The effect of drought stress on inbreeding depression in four populations of the Mediterranean outcrossing plant Crepis sancta (Asteraceae). Heredity 85: 294-302.
Crnokrak P. Barrett S. C. H.. 2002. Perspective: Purging the genetic load: a review of the experimental evidence. Evolution 56: 2347-2358.[ISI][Medline]
D'Alessandro M. Turlings T. C. J.. 2005. In situ modification of herbivore-induced plant odors: a novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. Chemical Senses 30: 739-753.
De Moraes C. M. Lewis W. J. Pare P. W. Alborn H. T. Tumlinson J. H.. 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393: 570-573.[CrossRef][ISI]
De Moraes C. M. Mescher M. C.. 2004. Biochemical crypsis in the avoidance of natural enemies by an insect herbivore. Proceedings of the National Academy of Sciences, USA 101: 8993-8997.
De Moraes C. M. Mescher M. C. Tumlinson J. H.. 2001. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410: 577-580.[CrossRef][Medline]
Decker D. S. Wilson H. D.. 1986. Numerical-analysis of seed morphology in Cucurbita pepo. Systematic Botany 11: 595-607.[CrossRef][ISI]
Dicke M.. 1994. Local and systemic production of volatile herbivore-induced terpenoids: their role in plant-carnivore mutualism. Journal of Plant Physiology 143: 465-472.[ISI]
Dicke M. Vanbeek T. A. Posthumus M. A. Bendom N. Vanbokhoven H. Degroot A. E.. 1990. Isolation and identification of volatile kairomone that affects Acarine predator–prey interactions: involvement of host plant in its production. Journal of Chemical Ecology 16: 381-396.[CrossRef][ISI]
Dudash M. R.. 1990. Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentianaceae): a comparison in three environments. Evolution 44: 1129-1139.[CrossRef][ISI]
Dudash M. R. Carr D. E. Fenster C. B.. 1997. Five generations of enforced selfing and outcrossing in Mimulus guttatus: inbreeding depression variation at the population and family level. Evolution 51: 54-65.[CrossRef][ISI]
Ferrari M. J.. 2006. Mixing models and the geometry of epidemics Ph.D. dissertation, Pennsylvania State University, University Park, Pennsylvania, USA.
Galen C.. 1999. Flowers and enemies: predation by nectar-thieving ants in relation to variation in floral form of an alpine wildflower, Polemonium viscosum. Oikos 85: 426-434.[CrossRef][ISI]
Hayes C. N. James A. W. Stephenson A. G.. 2005a. A comparison of male and female responses to inbreeding in Cucurbita pepo subsp. texana (Cucurbitaceae). American Journal of Botany 92: 107-115.
Hayes C. N. Winsor J. A. Stephenson A. G.. 2004. Inbreeding influences herbivory in Cucurbita pepo ssp. texana (Cucurbitaceae). Oecologia 140: 601-608.[ISI][Medline]
Hayes C. N. Winsor J. A. Stephenson A. G.. 2005b. Multigenerational effects of inbreeding in Cucurbita pepo ssp. texana (Cucurbitaceae). Evolution 59: 276-286.[ISI][Medline]
Hayes C. N. Winsor J. A. Stephenson A. G.. 2005c. Environmental variation influences the magnitude of inbreeding depression in Cucurbita pepo ssp. texana (Cucurbitaceae). Journal of Evolutionary Biology 18: 147-155.[CrossRef][ISI][Medline]
Hull-Sanders H. M. Eubanks M. D.. 2005. Plant defense theory provides insight into interactions involving inbred plants and insect herbivores. Ecology 86: 897-904.[CrossRef][ISI]
Ivey C. T. Carr D. E.. 2005. Effects of herbivory and inbreeding on the pollinators and mating system of Mimulus guttatus (Phrymaceae). American Journal of Botany 92: 1641-1649.
Kirkpatrick K. J. Wilson H. D.. 1988. Interspecific gene flow in Cucurbita: C. texana vs. C. pepo. American Journal of Botany 75: 519-527.[CrossRef][ISI]
Kohn J. R. Biardi J. E.. 1995. Outcrossing rates and inferred levels of inbreeding depression in gynodioecious Cucurbita foetidissima (Cucurbitaceae). Heredity 75: 77-83.[ISI]
Lampman R. L. Metcalf R. L.. 1988. The comparative response of Diabrotica species (Coleoptera, Chrysomelidae) to volatile attractants. Environmental Entomology 17: 644-648.[ISI]
Lampman R. L. Metcalf R. L. Andersen J. F.. 1987. Semiochemical attractants of Diabrotica undecimpunctata howardi Barber, southern corn-rootworm, and Diabrotica virgifera virgifera Leconte, the western corn-rootworm (Coleoptera, Chrysomelidae). Journal of Chemical Ecology 13: 959-975.[CrossRef][ISI]
Lande R. Schemske D. W.. 1985. The evolution of self-fertilization and inbreeding depression in plants. 1. Genetic models. Evolution 39: 24-40.[CrossRef][ISI]
Mena Granero A. Gonzalez F. J. E. Sanz J. M. G. Vidal J. L. M.. 2005. Analysis of biogenic volatile organic compounds in zucchini flowers: identification of scent sources. Journal of Chemical Ecology 31: 2309-2322.[CrossRef][ISI][Medline]
Mercke P. Kappers I. F. Verstappen F. W. A. Vorst O. Dicke M. Bouwmeester H. J.. 2004. Combined transcript and metabolite analysis reveals genes involved in spider mite induced volatile formation in cucumber plants. Plant Physiology 135: 2012-2024.
Metcalf R. L. Lampman R. L.. 1989. The chemical ecology of Diabroticites and Cucurbitaceae. Experientia 45: 240-247.[CrossRef][ISI]
Metcalf R. L. Lampman R. L.. 1991. Evolution of diabroticite rootworm beetle (Chrysomelidae) receptors for Cucurbita blossom volatiles. Proceedings of the National Academy of Sciences, USA 88: 1869-1872.
Ouborg N. J. Biere A. Mudde C. L.. 2000. Inbreeding effects on resistance and transmission-related traits in the Silene–Microbotryum pathosystem. Ecology 81: 520-531.[CrossRef][ISI]
Pichersky E. Gershenzon J.. 2002. The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Current Opinion in Plant Biology 5: 237-243.[CrossRef][ISI][Medline]
Raguso R. A.. 2001. Floral scent, olfaction, and scent-driven foraging behavior. In L. Chittka, J. D. Thomson [eds.], Cognitive ecology of pollination: animal behavior and floral evolution 83-105 Cambridge University Press, Cambridge, UK.
Raguso R. A.. 2004a. Flowers as sensory billboards: progress towards an integrated understanding of floral advertisement. Current Opinion in Plant Biology 7: 434-440.[CrossRef][ISI][Medline]
Raguso R. A.. 2004b. Why are some floral nectars scented?. Ecology 85: 1486-1494.[CrossRef][ISI]
Rasmann S. Kollner T. G. Degenhardt J. Hiltpold I. Toepfer S. Kuhlmann U. Gershenzon J. Turlings T. C. J.. 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434: 732-737.[CrossRef][Medline]
Schnee C. Kollner T. G. Held M. Turlings T. C. J. Gershenzon J. Degenhardt J.. 2006. The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proceedings of the National Academy of Sciences, USA 103: 1129-1134.
Scutareanu P. Drukker B. Bruin J. Posthumus M. A. Sabelis M. W.. 1997. Volatiles from Psylla-infested pear trees and their possible involvement in attraction of anthocorid predators. Journal of Chemical Ecology 23: 2241-2260.[CrossRef][ISI]
Stephenson A. G. Hayes C. N. Johannsson M. H. Winsor J. A.. 2001. The performance of microgametophytes is affected by inbreeding depression and hybrid vigor in the sporophytic generation. Sexual Plant Reproduction 14: 77-83.
Stephenson A. G. Leyshon B. Travers S. E. Hayes C. N. Winsor J. A.. 2004. Interrelationships among inbreeding, herbivory, and disease on reproduction in a wild gourd. Ecology 85: 3023-3034.[CrossRef][ISI]
Turlings T. C. J. Tumlinson J. H. Lewis W. J.. 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250: 1251-1253.
Uyenoyama M. K. Holsinger K. E. Waller D. M.. 1993. Ecological and genetic factors directing the evolution of self-fertilisation. Oxford Surveys in Evolutionary Biology 9: 327-381.
Ventura M. U. Martins M. C. Pasini A.. 2000. Responses of Diabrotica speciosa and Cerotoma arcuata tingomariana (Coleoptera : Chrysomelidae) to volatile attractants. Florida Entomologist 83: 403-410.[CrossRef][ISI]
Vogler D. W. Filmore K. Stephenson A. G.. 1999. Inbreeding depression in Campanula rapunculoides L. I. A comparison of inbreeding depression in plants derived from strong and weak self-incompatibility phenotypes. Journal of Evolutionary Biology 12: 483-494.
Wolfe L. M.. 1993. Inbreeding depression in Hydrophyllum appendiculatum: role of maternal effects, crowding, and parental mating history. Evolution 47: 374-386.[CrossRef][ISI]
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