Mark D. Rausher

THE MEASUREMENT OF SELECTION ON QUANTITATIVE TRAITS: BIASES DUE TO ENVIRONMENTAL COVARIANCES BETWEEN TRAITS AND FITNESS

The use of regression techniques for estimating the direction and magnitude of selection from measurements on phenotypes has become widespread in field studies. A potential problem with these techniques is that environmental correlations between fitness and the traits examined may produce biased estimates of selection gradients. This report demonstrates that the phenotypic covariance between fitness and a trait, used as an estimate of the selection differential in estimating selection gradients, has two components: a component induced by selection itself and a component due to the effect of environmental factors on fitness. The second component is shown to be responsible for biases in estimates of selection gradients. The use of regressions involving genotypic and breeding values instead of phenotypic values can yield estimates of selection gradients that are not biased by environmental covariances. Statistical methods for estimating the coefficients of such regressions, and for testing for biases in regressions involving phenotypic values, are described.

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.

Co-evolution and plant resistance to natural enemies

Co-evolution between plants and their natural enemies is generally believed to have generated much of the Earths biological diversity. A process analogous to co-evolution occurs in agricultural systems, in which natural enemies adapt to crop resistance introduced by breeding or genetic engineering. Because of this similarity, the investigation of resistance mechanisms in crops is helping to elucidate the workings of co-evolution in nature, while evolutionary principles, including those derived from investigation of co-evolution in nature, are being applied in the management of resistance in genetically engineered crops.

Costs and Benefits of Plant Resistance to Herbivory

The cost-benefit theory of the evolution of plant resistance to herbivory assumes that the allocation of plant resources to defense against herbivores is costly. We present a graphical model, which states that allocation of plant resources to defense against herbivores evolves so as to maximize the difference between benefits and costs associated with resistance. A method for quantification of such costs, using genetic regression coefficients between fitness and defense, is described. This technique was applied to measure the cost to tall morning glory. (Ipomoea purpurea) of resistance to the sweet potato flea beetle (Chaetocnema confinis). The morning glory population studied exhibited significant amounts of heritable variation in resistance in flea beetles. However, there was no evidence for costs of resistance to plants in this population.

Search Image for Leaf Shape in a Butterfly

The butterfly Battus philenor forms search images for leaf shape when searching for its two larval host plants in southeast Texas. This behavior increases the rate of discovery of host plants and permits females to track changes in relative host plant suitability for larval growth. Apostatic selection resulting from search image formation is a likely explanation for divergence in leaf shape by the two host plants.

Escape from adaptive conflict after duplication in an anthocyanin pathway gene

Gene duplications have been recognized as an important source of evolutionary innovation and adaptation since at least Haldane, and their varying fates may partly explain the vast disparity in observed genome sizes. The expected fates of most gene duplications involve primarily non-adaptive substitutions leading to either non-functionalization of one duplicate copy or subfunctionalization, neither of which yields novel function. A significant evolutionary problem is thus elucidating the mechanisms of adaptive evolutionary change leading to evolutionary novelty. Currently, the most widely recognized adaptive process involving gene duplication is neo-functionalization (NEO-F), in which one copy undergoes directional selection to perform a novel function after duplication. An alternative, but understudied, adaptive fate that has been proposed is escape from adaptive conflict (EAC), in which a single-copy gene is selected to perform a novel function while maintaining its ancestral function. This gene is constrained from improving either novel or ancestral function because of detrimental pleiotropic effects on the other function. After duplication, one copy is free to improve novel function, whereas the other is selected to improve ancestral function. Here we first present two criteria that can be used to distinguish NEO-F from EAC. Using both tests for positive selection and assays of enzyme function, we then demonstrate that adaptive evolutionary change in a duplicated gene of the anthocyanin biosynthetic pathway in morning glories (Ipomoea) is best interpreted as EAC. Finally, we argue that this phenomenon likely occurs more often than has been previously believed and may thus represent an important mechanism in generating evolutionary novelty.

Evolutionary Transitions in Floral Color

The tremendous diversity in flower color among angiosperms implies that there have been numerous evolutionary transitions in this character. The conventional wisdom is that a large proportion of these transitions reflect adaptation to novel pollinator regimes. By contrast, recent research suggests that many of these transitions may instead have been driven by selection imposed by nonpollinator agents of selection acting on pleiotropic effects of flower color genes. I evaluate the evidence for these alternative hypotheses and find that while there is circumstantial evidence consistent with each hypothesis, there are no definitive examples of flower color evolution conforming to either hypothesis. I also document four macroevolutionary trends in flower color evolution: color transitions rates are often asymmetrical; biases favoring loss of pigmentation or favoring gain of pigmentation are both observed, but bias favoring transition from blue to red flowers seems more common than the reverse bias; transitions from blue to red often involve inactivation of branches of the anthocyanin pathway; and color transitions often involve loss‐of‐function mutations. Finally, I discuss how these trends may be related to one another.

Larval Habitat Suitability and Oviposition Preference in Three Related Butterflies

A simple hypothesis about habitat choice by ovipositing butterflies is that females prefer to lay their eggs on plants in habitats where juvenile growth and survival are best. This hypothesis was evaluated by studying 3 Aristolochia—feeding swallowtail butterflies (Papilionidae: Troidini). Results show that the eggs and larvae of all 3 butterfly species survive significantly better in shady habitats than in sunny habitats. Pupal survival is similar in the 2 habitats for at least 1 species. Larval growth rates were similar in the 2 habitats for all 3 species. Thus, for all 3 species shady habitats appear to be more suitable for juvenile development and survival than sunny habitats. Only Parides montezuma lays most of its eggs in shady habitats, however; Battus philenor and B. polydamus females lay most of their eggs in sunny habitats. The original hypothesis is therefore not upheld by this study. Three alternative explanations for the discrepancy between the relative suitability of habitats for the juvenil...

Genetic Constraints and Selection Acting on Tolerance to Herbivory in the Common Morning Glory Ipomoea purpurea

Tolerance to herbivory minimizes the effects of herbivory on plant fitness. In the presence of herbivores, maximal levels of tolerance may be expected to evolve. In many plant species, however, tolerance is found at an intermediate level. Tolerance may be prevented from evolving to a maximal level by genetic constraints or stabilizing selection. We report on a field study of Ipomoea purpurea, the common morning glory, in which we measured three types of costs that may be associated with tolerance and the pattern of selection acting on tolerance to two types of herbivore damage: apical meristem damage and folivory. We used genetic correlations to test for the presence of three types of costs: a trade‐off between tolerance and fitness in the absence of herbivore damage, a trade‐off between tolerance and resistance, and genetic covariances among tolerance to different types of damage. We found no evidence that tolerance to apical meristem damage or tolerance to folivory was correlated with resistance, although these two types of tolerance were positively correlated with one another. Tolerance to both types of damage involved costs of lower fitness in the absence of herbivory. Selection acting on tolerance to either type of herbivory was not detected at natural levels of herbivory. Selection is expected to act against tolerance at reduced levels of herbivory and favor tolerance at elevated levels of herbivory. In addition, significant correlational selection gradients indicate that the pattern of selection acting on tolerance depends on values of resistance. Although we found no evidence for stabilizing selection, fluctuating selection resulting from fluctuating herbivore loads may be responsible for maintaining tolerance at an intermediate level.