Rodney Mauricio

EXPERIMENTAL MANIPULATION OF PUTATIVE SELECTIVE AGENTS PROVIDES EVIDENCE FOR THE ROLE OF NATURAL ENEMIES IN THE EVOLUTION OF PLANT DEFENSE

Although biologists have long assumed that plant resistance characters evolved under selection exerted by such natural enemies as herbivores and pathogens, experimental evidence for this assumption is sparse. We present evidence that natural enemies exert selection on particular plant resistance characters. Specifically, we demonstrate that elimination of natural enemies from an experimental field population of Arabidopsis thaliana alters the pattern of selection on genetic variation in two characters that have been shown to reduce herbivore damage in the field: total glucosinolate concentration and trichome density. The change in pattern of selection reveals that natural enemies imposed selection favoring increased glucosinolate concentration and increased trichome density, and thus, supports one of the major assumptions of the coevolution hypothesis. We also demonstrate that a pattern of stabilizing selection on glucosinolate concentration results from a balance between the costs and benefits associated with increasing levels of this resistance character. This result provides direct confirmation of the appropriateness of cost‐benefit models for characterizing the evolution of plant defenses.

VARIATION IN THE DEFENSE STRATEGIES OF PLANTS: ARE RESISTANCE AND TOLERANCE MUTUALLY EXCLUSIVE?

Plants can employ two general strategies to defend themselves against herbivory: they can either reduce the amount of damage they experience (resistance), or they can tolerate herbivore damage. Theoretical considerations suggest that, in many cases, tolerance and resistance are redundant strategies, and may therefore be mutually exclusive adaptations. In this investigation of natural populations of the annual plant Arabidopsis thaliana we examine whether the pattern of selection acting on resistance and tolerance favors the evolution of one defense strategy, or the other, but not both. We found that the joint pattern of selection acting on tolerance and two resistance traits, trichome density and total glucosinolate concentration, indicated that there were not alternate peaks in the fitness landscape favoring either resistance or tolerance. Rather, selection favored the retention of both tolerance and resistance. One reason for the absence of mutually exclusive alternative resistance/tolerance strategies is the absence of a negative genetic correlation between resistance and tolerance. An unexpected result is the detection of disruptive selection acting on tolerance, which seems to result from a nonlinear relationship between tolerance and its costs.

Costs of Resistance to Natural Enemies in Field Populations of the Annual Plant Arabidopsis thaliana

The annual plant Arabidopsis thaliana is widely used as a model system in molecular genetics, but little is known about populations in the field. In this experimental field study of natural populations of Arabidopsis, I tested the assumption that plant resistance has fitness costs. Models of the evolution of resistance assume a cost, which is envisioned as a reduction in fitness in the absence of natural enemies, such as insect herbivores and pathogens. The presumed basis of this cost is the diversion of limiting resources away from present and future growth and reproduction. Recent failures to detect allocation costs of resistance to herbivores have raised questions about whether costs exist and, thus, about the appropriateness of theories that postulate such costs. I found genetic variation for two traits commonly thought to function as resistance characters: trichome density and total glucosinolate concentration. Under field conditions, these characters both reduced damage by the natural assemblage of herbivores and exhibited significant fitness costs.

Mapping quantitative trait loci in plants: uses and caveats for evolutionary biology

Gregor Mendel was either clever or lucky enough to study traits of simple inheritance in his pea plants; however, many plant characters of interest to modern geneticists are decidedly complex. Understanding the genetic basis of such complex, or quantitative, traits requires a combination of modern molecular genetic techniques and powerful statistical methods. These approaches have begun to give us insight into understanding the evolution of complex traits both in crops and in wild plants.

Testing for Environmentally Induced Bias in Phenotypic Estimates of Natural Selection: Theory and Practice

Measuring natural selection has been a fundamental goal of evolutionary biology for more than a century, and techniques developed in the last 20 yr have provided relatively simple means for biologists to do so. Many of these techniques, however, share a common limitation: when applied to phenotypic data, environmentally induced covariances between traits and fitness can lead to biased estimates of selection and misleading predictions about evolutionary change. Utilizing estimates of breeding values instead of phenotypic data with these methods can eliminate environmentally induced bias, although this approach is more difficult to implement. Despite this potential limitation to phenotypic methods and the availability of a potential solution, little empirical evidence exists on the extent of environmentally induced bias in phenotypic estimates of selection. In this article, we present a method for detecting bias in phenotypic estimates of selection and demonstrate its use with three independent data sets. Nearly 25% of the phenotypic selection gradients estimated from our data are biased by environmental covariances. We find that bias caused by environmental covariances appears mainly to affect quantitative estimates of the strength of selection based on phenotypic data and that the magnitude of these biases is large. As our estimates of selection are based on data from spatially replicated field experiments, we suggest that our findings on the prevalence of bias caused by environmental covariances are likely to be conservative.

Epistasis for fitness-related quantitative traits in Arabidopsis thaliana grown in the field and in the greenhouse

The extent to which epistasis contributes to adaptation, population differentiation, and speciation is a long-standing and important problem in evolutionary genetics. Using recombinant inbred (RI) lines of Arabidopsis thaliana grown under natural field conditions, we have examined the genetic architecture of fitness-correlated traits with respect to epistasis; we identified both single-locus additive and two-locus epistatic QTL for natural variation in fruit number, germination, and seed length and width. For fruit number, we found seven significant epistatic interactions, but only two additive QTL. For seed germination, length, and width, there were from two to four additive QTL and from five to eight epistatic interactions. The epistatic interactions were both positive and negative. In each case, the magnitude of the epistatic effects was roughly double that of the effects of the additive QTL, varying from −41% to +29% for fruit number and from −5% to +4% for seed germination, length, and width. A number of the QTL that we describe participate in more than one epistatic interaction, and some loci identified as additive also may participate in an epistatic interaction; the genetic architecture for fitness traits may be a network of additive and epistatic effects. We compared the map positions of the additive and epistatic QTL for germination, seed width, and seed length from plants grown in both the field and the greenhouse. While the total number of significant additive and epistatic QTL was similar under the two growth conditions, the map locations were largely different. We found a small number of significant epistatic QTL × environment effects when we tested directly for them. Our results support the idea that epistatic interactions are an important part of natural genetic variation and reinforce the need for caution in comparing results from greenhouse-grown and field-grown plants.

Pattern of Leaf Damage Affects Fitness of the Annual Plant Raphanus Sativus (Brassicaceae)

We investigated how the pattern of leaf damage influences reproduction, growth, and allocation in the wild radish, Raphanus sativus (Brassicaceae). We removed an equivalent leaf area from plants with four leaves in five treatments ranging from con- centrated to dispersed damage: one entire mature leaf removed, one entire new leaf re- moved, 50% of two mature leaves removed, 50% of two new leaves removed, and 25% of all four leaves removed. Plants in a control group were undamaged. Reproduction, growth, and allocation were not affected by the age of the damaged leaf. However, the pattern of leaf damage significantly affected our three measures of plant fitness: the number of flowers produced, the reproductive biomass, and the total biomass. Plants in the treatment in which the damage was most dispersed had significantly higher flower number, reproductive biomass, and total biomass than an intermediate damage treatment and significantly more reproductive biomass than the concentrated damage treatment. There were no significant differences between the concentrated and intermediate damage treatments and no differ- ences between the dispersed damage treatment and the undamaged control. Our data indicate that more dispersed damage is less detrimental to the plant than more concentrated damage. Therefore, the pattern of leaf damage must be considered in determining the impact of herbivores on plant performance.

Natural selection and the joint evolution of toleranceand resistance as plant defenses

Plants can defend themselves against the damaging effects of herbivory in at least two ways. Resistant plants avoid or deter herbivores and are therefore fed upon less than susceptible plants. Tolerant plants are not eaten less than plants with little tolerance, but the effects of herbivore damage are not so detrimental to a tolerant plant as they are to a less tolerant plant. Biologists have suggested that these two strategies might represent two alternative and redundant defenses against herbivory since they appear to serve the same function for plants. I explore the relationship between resistance and tolerance, particularly with regards to how the joint evolution of these two traits will influence the evolution of plant defense. Although I briefly review some of the contributions of theory to the study of tolerance, I concentrate on an empirical, ecological genetic approach to the study of the evolution of these characters and the coevolution of tolerance and herbivores. In order to understand the evolution of any trait, we must understand the evolutionary forces acting on the trait. Specifically, we must understand how natural selection acts on tolerance. I review several studies that have specifically measured the form of selection acting on tolerance and tested the hypothesis that resistance and tolerance are alternative strategies. I also present a statistical analysis that does not support the hypothesis that herbivores are selective agents on tolerance. Finally, I consider a variety of constraints that possibly restrict the evolution of tolerance.

QTL-based evidence for the role of epistasis in evolution

The extent to which epistasis contributes to adaptation and speciation has been a controversial topic in evolutionary genetics. One experimental approach to study epistasis is based on quantitative trait locus (QTL) mapping using molecular markers. Comparisons can be made among all possible pair-wise combinations of the markers, irrespective of whether an additive QTL is associated with a marker; several software packages have been developed that facilitate this. We review several examples of using this approach to identify epistatic QTLs for traits of evolutionary or ecological interest. While there is variability in the results, the number of epistatic QTL interactions is often greater than or equal to the number of additive QTLs. The magnitude of epistatic effects can be larger than the additive effects. Thus, epistatic interactions seem to be an important part of natural genetic variation. Future studies of epistatic QTLs could lead to descriptions of the genetic networks underlying variation for fitness-related traits.

CONSTRAINTS ON THE EVOLUTION OF TOLERANCE TO HERBICIDE IN THE COMMON MORNING GLORY : RESISTANCE AND TOLERANCE ARE MUTUALLY EXCLUSIVE

Abstract Evolutionary biologists explain the maintenance of intermediate levels of defense in plant populations as being due to trade-offs, or negative genetic covariances among ecologically important traits. Attempts at detecting trade-offs as constraints on the evolution of defense have not always been successful, leading some to conclude that such trade-offs rarely explain current levels of defense in the population. Using the agricultural pest Ipomoea purpurea, we measured correlations between traits involved in defense to glyphosate, the active ingredient in Roundup, a widely used herbicide. We found significant allocation costs of tolerance, as well as trade-offs between resistance and two measures of tolerance to glyphosate. Selection on resistance and tolerance exhibited differing patterns: tolerance to leaf damage was under negative directional selection, whereas resistance was under positive directional selection. The joint pattern of selection on resistance and tolerance to leaf damage indicated the presence of alternate peaks in the fitness landscape such that a combination of either high tolerance and low resistance, or high resistance and low tolerance was favored. The widespread use of this herbicide suggests that it is likely an important selective agent on weed populations. Understanding the evolutionary dynamics of herbicide defense traits is thus of increasing importance in the context of human-mediated evolution.