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The trichome dimorphism of Datura wrightii is intriguing because glandular trichome production has a high fitness cost. Plants producing glandular trichomes (‘sticky’ plants) are resistant to many insect herbivores that attack plants producing non-glandular trichomes (‘velvety’ plants). When protected from herbivores, sticky plants initially produce fewer seeds than velvety plants but grow to a larger size. In a three-year field experiment, we tested the hypothesis that sticky plants acquire a competitive advantage through greater vegetative growth. In the absence of herbivores, sticky and velvety plants grew to similar sizes in their first year but sticky plants grew larger in the second and third years. Seed production of sticky plants was 46 – 60% less than velvety plants in their first year and this caused a 13% reduction in their finite rate of increase overall, even though sticky plants produced more seeds than velvety plants in later years. The impact of herbivory varied with plant density and herbivores reduced plant fitness more at low plant density than at high. The differences in growth associated with trichome morphology occurred too late to provide a competitive advantage to sticky plants and probably contribute little to the maintenance of D. wrightii’s trichome dimorphism.

Leaves of Datura wrightii in California (USA) are covered either with glandular trichomes ("sticky" plants) or non-glandular trichomes ("velvety" plants), and sticky plants are resistant to many insect herbivores. Theoretical models suggest that variation in resistance to herbivores may persist if resistance is costly and herbivore damage is variable. If so, then natural selection should favor resistant plants when damage is high and disfavor it when damage is low. However, without long-term equivalence between costs and benefits, then natural selection either should drive the trait to fixation if it has a net benefit or eliminate it if it has a net cost. Previously we showed that the production of glandular trichomes carried a net cost in short-term studies, suggesting that this expensive resistant trait might be eliminated from D. wrightii populations. To test this hypothesis we monitored survival and seed production of sticky and velvety D. wrightii in the presence of herbivores in 11 natural populations over four or five years. In eight populations where both types occurred, the finite rate of increase for velvety plants was 60-274% greater than for sticky plants. Plant survival averaged between two and three years and did not differ significantly between types. Because seed production consistently favored velvety plants, our prediction that the proportion of sticky plants should decline was met within five years in seven of those eight populations. If the variation in trichome morphology in D. wrightii is indeed maintained by variation in costs and benefits of glandular trichomes, then the periodicity of such variation extends over more than five seasons.

Traits that confer plant resistance to some herbivore species but increase plant susceptibility to other herbivore species are said to carry an "ecological cost" of herbivore resistance. The native perennial, Datura wrightii, is dimorphic for leaf trichome type, and the production of glandular trichomes carries a potential ecological cost over the production of non-glandular trichomes. Glandular trichomes provide resistance to at least six herbivore species, but they also confer susceptibility to Tupiocoris notatus, an abundant mirid bug with special adaptations to glandular trichomes. We estimated herbivore-specific damage to plants of each trichome type and measured plant seed production, a component of fitness, in a common garden over three years. Plant seed production increased with the size and persistence of leaf canopies and occasionally declined with increasing damage caused by some of the defoliating insects. Plant seed production was never reduced by T. notatus damage, however. Even though the ecological cost of glandular trichome production was not apparent in D. wrightii, the trait still was not beneficial. The fitness of plants with glandular trichomes never exceeded that of plants with non-glandular trichomes despite variation in both the composition of the herbivore community and the total level of damage inflicted by herbivores over three years of study. The persistence of the allele coding for glandular trichomes cannot be explained solely on the basis of the herbivore resistance that those trichomes provide.