Costs and Benefits of Plant Resistance in Datura wrightii

If plant resistance is beneficial, then why aren’t all plants resistant?  In reality, variation in resistance levels, or resistance polymorphisms, are often found and require explanation.  A common model assumes that there are trade-offs between the benefits of plant resistance and its cost.  A simple formulation of “cost” postulates that photosynthate might be allocated to growth or defense, but not to both processes simultaneously [1], though now we also know of other costs based upon differences in ecological context.  If the benefits of resistance vary among plant populations at any point in time, or over time within a single population, then resistance polymorphisms might be expected from stabilizing selection, favoring resistant plants when losses from herbivory are high, and susceptible plants when herbivore populations might be low (Fig. 1).

We tested the possibility that the variation in frequency of sticky plants among populations of D. wrightii could be due to variation in the costs and benefits of the production of glandular trichomes over several years in natural populations and in several field experiments.  We conducted our experiments over multiple years, recognizing that D. wrightii is a perennial species that reproduces every year.  Differences seen in the first year of life might not persist in the second and subsequent years.  Alternatively, small differences may become more apparent with continued growth over subsequent seasons.

Figure 1.  Schematic of stabilizing selection in which the benefits of resistance drive the frequency of the trait to 100%, whereas the costs drive the frequency to 0%

Measuring plant growth, herbivory, and seed production 

We developed a common set of methods to estimate herbivory and plant growth visually in the field based upon regular, frequent assessments of the percentage of leaf area damaged or removed from randomly-selected branches of plants coupled with estimates of the average number of leaves per branch and the number of branches per plant.  Observers were trained to recognize the characteristic type of damage done by the different herbivore species using diagrams and photos of known levels of damage and leaf removal.  A typical result from assessing plant growth and leaf damage over the full growing season is shown in Fig. 2 [2].  Although one might expect equivalent effects of species that remove leaf area similarly, it is misleading to equate levels of damaged inflicted by piercing-sucking insects like T. notatus with a similar level of leaf removal by chewing insects like Manduca sexta or Lema daturaphila.  Indeed, as was the case with my earlier research assessing the impact of feeding by the citrus red mite on leaves of orange trees, D. wrightii leaves heavily damaged by T. notatus retained a substantial fraction of their photosynthetic activity [3].

Figure 2.  Summary of censuses of plant growth and removal or damage of leaf area by different herbivore species.  From Elle and Hare, 2000

Total viable seed production by D. wrightii is easily estimated as the product of the number of seed capsules per plant (which remain on the plant until the end of the season) times an estimate of the number of seeds per capsule, times their germination rate assessed several times during the growing season [4].  As we gained additional experience with the system, we learned that the variation in total seed production was largely due to the variation in the number of seed capsules per plant, with relatively little influence due to variation in the number of seeds per capsule or in germination rate [4, 5], such that counting seed capsules per plant at the end of the season is an effective way to estimate season-long viable seed production in D. wrightii [6].

Experimental Determination of Costs and Benefits in the field.

Our first major field experiment included the two trichome phenotypes, plants either exposed to natural herbivory or protected from herbivory, and irrigated to provide water, a putative limiting resource, or unwatered.  Plant growth, flower production and herbivory were determined weekly, and total viable seed production was determined as described above.  We tested not only for the main effects but also for all two- and three-way interactions. The precise impact of each treatment effect depended upon the level of the others because the three-way interaction among them was statistically significant (Fig. 3).

In the absence of herbivores, sticky plants produced 45% fewer viable seeds than velvety plants, but in the presence of herbivores, then there was no difference in seed production between sticky and velvety phenotypes. Herbivory reduced plant fitness by 50 – 70%, depending upon the combination of trichome phenotype and irrigation treatment, with irrigation reducing the difference in seed production between plant phenotypes.  Irrigation increased seed production by 40% in the herbivore-free treatments but irrigation benefited seed production of sticky plants more than velvety plants when exposed to herbivores [4].   

Figure 3.  Total viable seed production in a field experiment of sticky and velvety plants when protected or exposed to insect herbivores and either left unwatered or given additional water throughout the growing season. From Elle et al. 1999.

In general, sticky plants tended to grow larger but produced fewer seed capsules per unit of plant biomass.  We concluded that velvety plants were more reproduction-dominated, whereas sticky plants were more growth-dominated.  Recalling that glandular trichomes are a juvenile trait that is expressed in plants carrying the dominant allele, we hypothesized that all observed effects on growth and flower production were part of a juvenility syndrome and were all pleiotropic effects of, or linked to, the trichome gene.[4]

The observation that sticky plants grew to a larger size generated a subsequent hypothesis.  Whatever reductions in seed production that were observed in the first might be overcome in subsequent years as a result of cumulative increases in the growth of sticky plants relative to velvety plants.  We tested this hypothesis by continuing our observations and experiments on surviving plants over the next two years.

We used standard life-table methods to determine the net reproductive rate and the finite rate of increase of plants of each trichome phenotype.   The majority of experimental plants exposed to herbivores had died by the end of the three-year study, but few plants protected from herbivores had died (Fig. 4).  After three years, sticky plants were 187-245% larger than velvety plants depending upon irrigation treatments, but sticky plants continued to produce fewer seeds per unit of leaf canopy.  Although the net reproductive rate of sticky plants eventually caught up with that of velvety plants, this was insufficient to compensate for the advantage of increased seed production of velvety plants in the first year (Fig. 5).  The advantage of higher rates of seed production in the first year conferred an advantage in the finite rate of increase of 55 – 230% to velvety plants over sticky plants, depending upon herbivore and irrigation treatment.  In summary, the cost of producing glandular trichomes strictly for resistance to herbivores continued to exceed its benefits over the full three-year study [5] as it did in the first year. 

Figure 4.  Survival of sticky and velvety plants over three years in a field experiment when protected or exposed to herbivores.  For simplicity, only data from the treatment without additional water are shown.  From Hare et al 2003.

Figure 5.  Finite Rate of Increase of sticky and velvety plants over three years in a field experiment when protected or exposed to herbivores and either left unwatered or provided additional water during the growing season each year.  From Hare et al. 2003.

We also observed changes in the community of herbivores over the three years that affected the relative “resistance” of the two trichome phenotypes.  Because the herbivore community was dominated by species largely confined to velvety plants in the first year, sticky plants appeared more resistant to herbivory than velvety plants, but this was not the case in the second year, when the sticky specialist, Tupiocorus notatus, became relatively more abundant, nor in the third year, when Lema daturaphila, feeding heavily on both trichome phenotypes, dominated the herbivore community [3]. 

Competition between trichome phenotypes 

The differences in pattern of growth and reproduction of the two trichome phenotypes suggested a working hypothesis that the sticky phenotype might be the better competitor in intraspecific competition, and the cost of glandular trichome production on plant fitness might be mitigated if plants were grown at a more competitive spacing than at a noncompetitive spacing.  We tested this in a second three-year field study. Plants were grown at 0.5, 1.0, and 3.0 M spacing (Figs. 6-9) in pure sticky, pure velvety, and mixed stands.  Half of all plots were exposed to herbivores whereas the remainder were protected from herbivory.  Plant growth and herbivory were determined weekly, and total seed production was determined as above.  

Figure 6. Diagram of the plots to measure competition.  Each of the six numbered data plants in the inner hexagon competes with the center plant ("C”), two adjacent data plants, and three nondata plants in the outer hexagon.  For mixed stands each data plant competes with three sticky and three velvety plants.  From Hare and Smith 2005

Figure 7. Plants as in Fig. 6 at low density (3 m spacing).  From Hare and Smith 2005.

Figure 8. Plants as in Fig. 6 at medium density (1 m) spacing).  From Hare and Smith 2005.

Figure 9. Plants as in Fig. 6 at high density (0.5 m spacing).  From Hare and Smith 2005.

Competition reduced seed production, as did herbivory, as expected [7].

 A statistically significant interaction between competition and trichome phenotype on seed production would be consistent with our working hypothesis, but there was no such statistically significant interaction.

Although sticky plants grew larger than velvety plants in the second and third years of the study, these size differences emerged too late to provide a competitive benefit to sticky plants at the most competitive spacing.  Herbivores, by reducing plant size, mitigated the impact of competition (Fig. 10). 

Our working hypothesis that the sticky phenotype would be the stronger competitor at high plant density, was not supported, and we were still unable to find any fitness benefit to the production of glandular trichomes that exceeded its cost [7].

Figure 10.  Finite Rate of Increase of sticky and velvety plants over three years in a field experiment when protected or exposed to herbivores and raised at low density (3 m spacing), medium density (1 m spacing) or high density (0.5 m spacing).  From Hare and Smith 2005.

Benefits of glandular trichome production in natural populations?

Costs of resistance only can be determined in the absence of herbivores, so our studies in natural systems focused upon determining if there were a net benefit of the production of glandular trichomes in natural populations.  We studied replicate populations in three regions – the Mojave Desert, the Riversidian Sage Scrub, and in the coastal Santa Ana Mountains.  Herbivory, plant survival and seed production were monitored as above [2].  At the end of the first year, additional populations per region were added to the study, and data were collected on survival and seed production or four additional years.  Standard life-table methods were used to analyze for differences in survival and reproduction of the survivors each year.

In the first year, damage caused by the herbivore community varied spatially, with significant differences in herbivore-specific damage between plants of the two trichome phenotypes, and among populations within habitats (Fig. 11) but velvety plants always had a reproductive advantage over sticky plants (Fig. 12) [2].

Figure 11.  Mean seasonal proportional damage by plant phenotype for two populations within three habitats caused by each of five herbivore species.   Population codes: BC: Bell Canyon; OF: Ortega Flats; MV: Moreno Valley; UCR: UC Riverside; BD: Barker Dam; WT: White Tank.  From Elle et al. 2000.

Figure 12.  Viable seed production (mean + SE) of sticky and velvety plants in six populations spanning three habitats.  Population codes as in Fig. 11.  From Elle et al. 2000.

Over five years, survival rates differed among populations with mortality ranging from 50% to 100% over the course of the study, depending upon population and trichome phenotype (Fig. 13) [6].  The finite rates of increase, however, always favored the velvety trichome phenotype, being 60 – 274% greater than that for the sticky phenotype (Fig. 14).

Figure 13.  Survival of sticky and velvety plants over four or five years in Mountain (Arroyo Trabuco: AT; Bell Canyon: BC), Scrub (Coyote Pass: CP and Pictograph Trail: PT), and Desert (Barker Dam: BD; Wilson Canyon: WC; White Tank: WT) habitats.  Only velvety plants are found in the Desert.  Survival of sticky and velvety plants were identical in the AT population.  From Hare and Elle 2004.

Figure 14.  Finite rate of increase of sticky and velvety plants in Mountain, Sage, and Desert habitats in southern California.  Population codes as in Fig. 13.  From Hare and Elle 2004.

Conclusion

All of our observational and experimental field studies showed a substantial fitness cost associated with the production of glandular trichomes, with no net benefit.  Although the impact of glandular trichomes and the acyl sugars that they produce have substantial influence on which herbivorous insects attack the sticky phenotype, it seems unlikely that conferring host plant resistance is the phenotype’s most important consequence.  The linked or pleiotropic effects of the trichome gene on plant growth or reproduction are profound, and selection on these life history traits may be of greater significance than selection by herbivores for resistant plants.  Though dramatic, the impact of trichome morphology and chemistry on the community of herbivorous insects may be incidental to the growth vs. reproduction- dominated life history traits associated with trichome phenotype.  Rather than being the primary trait under selection, trichome morphology may be a convenient visible marker for the life history traits linked to trichome morphology that actually are the targets of selection.

1 Herms, D.A. and Mattson, W.J. (1992) The dilemma of plants: to grow or defend. Q. Rev. Biol. 67, 283-335.  DOI:  10.1086/417659

2 Elle, E. and Hare, J.D. (2000) No benefit of glandular trichome production in natural populations of Datura wrightii? Oecologia 123, 57-65.   DOI:  10.1007/s004420050989.

3 Hare, J.D. and Elle, E. (2002) Variable impact of diverse insect herbivores on dimorphic Datura wrightii. Ecology 83, 2711-2720.  DOI:  10.1890/0012-9658(2002)083[2711:VIODIH]2.0.CO;2

4 Elle, E., et al. (1999) Cost of glandular trichomes, a "resistance" character in Datura wrightii Regel (Solanaceae). Evolution 53, 22-35.    DOI: 10.2307/2640917.

5 Hare, J.D., et al. (2003) Costs of glandular trichomes in Datura wrightii: A three-year study. Evolution 57, 793-805.  DOI:  10.1111/j.0014-3820.2003.tb00291.x.

6 Hare, J.D. and Elle, E. (2004) Survival and seed production of sticky and velvety Datura wrightii in the field: A five-year study. Ecology 85, 615-622.   DOI: 10.1890/03-3069.

7 Hare, J.D. and Smith, J.L. (2005) Competition, Herbivory, and Reproduction of Trichome Phenotypes of Datura wrightii. Ecology 86, 334-339.   DOI: 10.1890/04-0972