Guillermo Castillo

Selection Mosaic Exerted by Specialist and Generalist Herbivores on Chemical and Physical Defense of Datura stramonium

Selection exerted by herbivores is a major force driving the evolution of plant defensive characters such as leaf trichomes or secondary metabolites. However, plant defense expression is highly variable among populations and identifying the sources of this variation remains a major challenge. Plant populations are often distributed across broad geographic ranges and are exposed to different herbivore communities, ranging from generalists (that feed on diverse plant species) to specialists (that feed on a restricted group of plants). We studied eight populations of the plant Datura stramonium usually eaten by specialist or generalist herbivores, in order to examine whether the pattern of phenotypic selection on secondary compounds (atropine and scopolamine) and a physical defense (trichome density) can explain geographic variation in these traits. Following co-evolutionary theory, we evaluated whether a more derived alkaloid (scopolamine) confers higher fitness benefits than its precursor (atropine), and whether this effect differs between specialist and generalist herbivores. Our results showed consistent directional selection in almost all populations and herbivores to reduce the concentration of atropine. The most derived alkaloid (scopolamine) was favored in only one of the populations, which is dominated by a generalist herbivore. In general, the patterns of selection support the existence of a selection mosaic and accounts for the positive correlation observed between atropine concentration and plant damage by herbivores recorded in previous studies.

Natural selection on plant resistance to herbivores in the native and introduced range.

Plants introduced into a new range are expected to harbour fewer specialized herbivores and to receive less damage than conspecifics in native ranges. Datura stramonium was introduced in Spain about five centuries ago. Here, we compare damage by herbivores, plant size, and leaf trichomes between plants from non-native and native ranges and perform selection analyses. Non-native plants experienced much less damage, were larger and less pubescent than plants of native populations. While plant size was related to fitness in both ranges, selection to increase resistance was only detected in the native region. We suggest this is a consequence of a release from enemies in this new environment.

Geographic association and temporal variation of chemical and physical defense and leaf damage in Datura stramonium

The evolution of plant defense traits has traditionally been explained trough the “coevolutionary arms race” between plants and herbivores. According to this, specialist herbivores have evolved to cope effectively with the defensive traits of their host plants and may even use them as a cue for host location. We analyzed the geographic association between leaf trichomes, two tropane alkaloids (putative resistance traits), and leaf damage by herbivores in 28 populations of Datura stramonium in central Mexico. Since the specialist leaf beetles Epitrix parvula and Lema trilineata are the main herbivores of D. stramonium in central Mexico, we predicted a positive association between plant defense and leaf damage across populations. Also, if physical environmental conditions (temperature or precipitation) constrain the expression of plant defense, then the geographic variation in leaf damage should be explained partially by the interaction between defensive traits and environmental factors. Furthermore, we studied the temporal and spatial variation in leaf trichome density and leaf damage in five selected populations of D. stramonium sampled in two periods (1997 vs. 2007). We found a positive association between leaf trichomes density and atropine concentration with leaf damage across populations. The interaction between defensive traits and water availability in each locality had a significant effect on the geographic variation in leaf damage. Differences among populations in leaf trichome density are maintained over time. Our results indicate that local plant–herbivore interaction plays an important role in shaping the geographic and temporal variation in plant defense in D. stramonium.

Developmental Reaction Norms for Water Stressed Seedlings of Succulent Cacti

Succulent cacti are remarkable plants with capabilities to withstand long periods of drought. However, their adult success is contingent on the early seedling stages, when plants are highly susceptible to the environment. To better understand their early coping strategies in a challenging environment, two developmental aspects (anatomy and morphology) in Polaskia chichipe and Echinocactus platyacanthus were studied in the context of developmental reaction norms under drought conditions. The morphology was evaluated using landmark based morphometrics and Principal Component Analysis, which gave three main trends of the variation in each species. The anatomy was quantified as number and area of xylem vessels. The quantitative relationship between morphology and anatomy in early stages of development, as a response to drought was revealed in these two species. Qualitatively, collapsible cells and collapsible parenchyma tissue were observed in seedlings of both species, more often in those subjected to water stress. These tissues were located inside the epidermis, resembling a web of collapsible-cell groups surrounding turgid cells, vascular bundles, and spanned across the pith. Occasionally the groups formed a continuum stretching from the epidermis towards the vasculature. Integrating the morphology and the anatomy in a developmental context as a response to environmental conditions provides a better understanding of the organisms dynamics, adaptation, and plasticity.

Adaptive divergence in resistance to herbivores in Datura stramonium.

Defensive traits exhibited by plants vary widely across populations. Heritable phenotypic differentiation is likely to be produced by genetic drift and spatially restricted gene flow between populations. However, spatially variable selection exerted by herbivores may also give rise to differences among populations. To explore to what extent these factors promote the among-population differentiation of plant resistance of 13 populations of Datura stramonium, we compared the degree of phenotypic differentiation (PST) of leaf resistance traits (trichome density, atropine and scopolamine concentration) against neutral genetic differentiation (FST) at microsatellite loci. Results showed that phenotypic differentiation in defensive traits among-population is not consistent with divergence promoted by genetic drift and restricted gene flow alone. Phenotypic differentiation in scopolamine concentration was significantly higher than FST across the range of trait heritability values. In contrast, genetic differentiation in trichome density was different from FST only when heritability was very low. On the other hand, differentiation in atropine concentration differed from the neutral expectation when heritability was less than or equal to 0.3. In addition, we did not find a significant correlation between pair-wise neutral genetic distances and distances of phenotypic resistance traits. Our findings reinforce previous evidence that divergent natural selection exerted by herbivores has promoted the among-population phenotypic differentiation of defensive traits in D. stramonium.

Natural selection drives chemical resistance of Datura stramonium

Plant resistance to herbivores involves physical and chemical plant traits that prevent or diminish damage by herbivores, and hence may promote coevolutionary arm-races between interacting species. Although Datura stramonium’s concentration of tropane alkaloids is under selection by leaf beetles, it is not known whether chemical defense reduces seed predation by the specialist weevil, Trichobaris soror, and if it is evolving by natural selection. We measured infestation by T. soror as well as the concentration of the plants’ two main tropane alkaloids in 278 D. stramonium plants belonging to 31 populations in central Mexico. We assessed whether the seed predator exerted preferences on the levels of both alkaloids and whether they affect plant fitness. Results show great variation across populations in the concentration of scopolamine and atropine in both leaves and seeds of plants of D. stramonium, as well as in the intensity of infestation and the proportion of infested fruits by T. soror. The concentration of scopolamine in seeds and leaves are negatively associated across populations. We found that scopolamine concentration increases plant fitness. Our major finding was the detection of a positive relationship between the population average concentrations of scopolamine with the selection differentials of scopolamine. Such spatial variation in the direction and intensity of selection on scopolamine may represent a coevolutionary selective mosaic. Our results support the view that variation in the concentration of scopolamine among-populations of D. stramonium in central Mexico is being driven, in part, by selection exerted by T. soror, pointing an adaptive role of tropane alkaloids in this plant species.