Arthur E. Weis

Rapid evolution of flowering time by an annual plant in response to a climate fluctuation

Ongoing climate change has affected the ecological dynamics of many species and is expected to impose natural selection on ecologically important traits. Droughts and other anticipated changes in precipitation may be particularly potent selective factors, especially in arid regions. Here we demonstrate the evolutionary response of an annual plant, Brassica rapa, to a recent climate fluctuation resulting in a multiyear drought. Ancestral (predrought) genotypes were recovered from stored seed and raised under a set of common environments with descendant (postdrought) genotypes and with ancestor×descendant hybrids. As predicted, the abbreviated growing seasons caused by drought led to the evolution of earlier onset of flowering. Descendants bloomed earlier than ancestors, advancing first flowering by 1.9 days in one study population and 8.6 days in another. The intermediate flowering time of ancestor×descendant hybrids supports an additive genetic basis for divergence. Experiments confirmed that summer drought selected for early flowering, that flowering time was heritable, and that selection intensities in the field were more than sufficient to account for the observed evolutionary change. Natural selection for drought escape thus appears to have caused adaptive evolution in just a few generations. A systematic effort to collect and store propagules from suitable species would provide biologists with materials to detect and elucidate the genetic basis of further evolutionary shifts driven by climate change.

THE CONSEQUENCES OF FLORAL HERBIVORY FOR POLLINATOR SERVICE TO ISOMERIS ARBOREA

Flower-feeding insects may reduce the reproductive success of their host plant in subtle ways that go beyond a direct reduction in gametes. Pollinators may respond to floral damage by visiting damaged plants at lower rates. Fewer visitations to the plant may result in fewer flowers that receive pollinator service and as a consequence lead to lower male and/or female reproductive success. In a two-year study, we examined the direct effect of flower predation by Meligethes rufimanus on the floral display of Isomeris arborea, and the indirect effect of herbivory on pollinator behavior. Plants exposed to herbivore attack produced fewer functional inflorescences than plants protected from herbivory. Undamaged flowers produced three times as much nectar per flower as damaged flowers. Likewise, protected plants had over twice as many anthers per flower as exposed plants. Pollinators responded by visiting damaged flowers less, and exposed plants had lower flower visitation rates than protected plants. Pollinators also visited patches of protected plants more frequently than exposed patches. These results show that floral herbivory reduces pollinator service and thus may reduce reproductive success indirectly, as well as through the direct consumption of viable gametes.

THE EFFECT OF FLORAL HERBIVORY ON MALE AND FEMALE REPRODUCTIVE SUCCESS IN ISOMERIS ARBOREA

Flower-feeding herbivores can directly reduce plant reproduction by consuming gametes. They may have additional indirect effects if their damage disrupts pollinator service and causes uneaten gametes to go unused. In a two-year study we investigated direct and indirect effects of florivory by a pollen beetle, Meligethes rufimanus, on the male and female reproductive success of the andromonoecious shrub, Isomeris arborea. We measured pollen export, pollen receipt, fruit set, and outcrossing rates on plants exposed to herbivores (most flowers damaged) and protected from herbivores (few flowers damaged) by systemic insecticide. Pollen export per undamaged flower was reduced by one-half in exposed plants, as estimated by pollinator transfer of florescent dye, which demonstrated indirect negative effects on male reproductive success. Damaged flowers on exposed plants had a lower stigmatic pollen load than undamaged flowers on either exposed or protected plants. Furthermore, exposed plants produced fewer fruits and seeds during the year than protected plants. Although damage reduces pollen receipt, hand pollination experiments showed that neither exposed nor protected plants were pollen limited, which suggests that floral herbivores primarily affect female function through their direct destruction of gametes. Outcrossing rates did not differ between exposed plants (ts = 0.920) and protected plants (ts = 0.806), suggesting that herbivory does not indirectly reduce plant reproductive success by inducing autogamy and subsequent inbreeding depression. Overall, floral herbivory has direct consequences for both male and female reproductive success, but indirect effects are limited to male function.

EVOLUTION OF HOST-PLANT MANIPULATION BY GALL MAKERS: ECOLOGICAL AND GENETIC FACTORS IN THE SOLIDAGO-EUROSTA SYSTEM

Plant galls are growth deformities that feed and house the larvae of specialized insect species and other organisms (nematodes, bacteria, fungi, etc.). The benefits derived by the insect from its interaction with the host plant suggest that gall-making ability is an adaptive trait of the insect subject to modification by natural selection. Our findings, that variation in gall phenotype influences insect fitness and that gall phenotypic variation is affected by genetic variation in the insect population, support this interpretation. Our study of the goldenrod gall fly, Eurosta solidaginis, shows that gall size variation results from genetic variation among flies despite selective pressures by natural enemies. Eurosta larvae that produce small galls are vulnerable to the attack of parasitoid wasps, whereas those producing large galls are more prone to attack by avian predators. In this study population, parasitoid attack was more intense; hence, a net upward selective pressure was exerted. Quantitative-genetic methods were used in a greenhouse experiment to evaluate the contribution of insect genetic variance to phenotypic variation in gall size. Significant differences in gall diameter were found among full-sib families of gall makers. Gall dimensions were genetically correlated with one another at most developmental stages. Observations of galls growing on goldenrod clones in both the field and the greenhouse suggest that plant genotype also influences gall phenotype, and thus affects gall-maker vulnerability to natural enemies.

POTENTIAL SELECTIVE PRESSURES BY PARASITOIDS ON A PLANT-HERBIVORE INTERACTION'

The potential role of the third trophic level in the evolution of plant-herbivore rela- tionships was examined in the case of the goldenrod Solidago altissima, and the fly Eurosta solidaginis, which forms a round stem gall. Previous observation had shown that galls attacked by parasites are significantly smaller than those in which the gall maker survives. Two different mechanisms could cause such a pattern: parasite attack could occur before galls reach full size and the attacks could cause early cessation of growth, or attack could occur after galls reach their mature size, but with inherently small galls being more prone to attack. In the first instance, parasite attack would diminish the cost of the gall to the plant, and thus favor plant genotypes that facilitate parasites. In the second instance, parasites would exert selection pressure on the gall maker to induce larger galls. Monitoring of marked plants in the field, and field experiments in which parasites were excluded from gall-bearing plants except during controlled periods, showed that parasite attack does not stop gall growth. The parasitoid wasp Eurytoma gigantea is limited to attacking small galls because of the limited reach of its ovipositor. This created a selection intensity of 0.50, favoring Eurosta that induce larger galls. Evolutionary response to selection could be realized directly through change in the gall makers stimulus ability, or less directly through phenological changes. Plant reactivity to the gall maker declined with plant age, so that late-starting galls were more vulnerable to parasite attack.

Measuring selection on reaction norms : an exploration of the Eurosta-solidago system

The sensitivity of genotypic expression to the environment can be depicted as the reaction norm, which is defined as the array of phenotypes produced by a single genotype over a range of environments. We studied selection on reaction norms of the gall‐inducing insect Eurosta solidaginis (Diptera; Tephritidae), which attacks tall goldenrod Solidago altissima (Compositae). Gall size was treated as a component of insect phenotype and attributes of the host plant as environmental influences on gall development. Genetic differences in the response of gall size to plant lag time (the number of days before a plant responds to the gall maker) were examined. Reaction norms for full‐sib families of flies were quantified as linear functions; the elevation of the function denoted gall size produced by the family averaged across all plants, and the functions slope denoted family sensitivity to lag time. Expected fitness of each family was regressed over reaction norm elevation and slope to yield selection gradients on these reaction norm parameters.

Goldenrod Ball Gall Effects on Solidago altissima: 14C Translocation and Growth

The purpose of this investigation was to determine whether the effects of the goldenrod ball gall on carbon translocation and growth in ramets of Solidago altissima can account for changes in biomass allocation and total biomass observed in galled ramets. To do this, individual leaves of S. altissima were labeled with carbon—14 introduced as CO2. The 14C was introduced into ramets that had ball galls caused by the fly Eurosta solidaginis and into ungalled control ramets; gall size (large vs. small) and point of introduction of the label (above vs. below the gall) were experimental factors. After 5 d the ramets were harvested and their component organs were assayed for 14C using liquid scintillation. In addition, a field cohort of 359 galled and ungalled was followed during the period of gall growth to determine the effect of the gal on stem height growth. Gall size and labeling position had no effect on the percent of 14C translocated out of the labeled leaf but did affect the distribution of translocated 14C. Translocation to underground organs was reduced when the label was introduced above the gall, the reduction being related to gall size. Large galls reduced translocation to the apical bud when the label was introduced below the gall, but small galls did not. Translocation to underground organs was not affected by the gall when the label was introduced below the gall and translocation to the apical bud was not affected by the gall when the label was introduced above the gall; these results indicate that the goldenrod ball gall is a nonmobilizing gall. The presence of a gall did not significantly affect final stem height but did slow the growth of ramets during the period of most rapid gall growth. The observed effects of the gall probably explain changes in resource allocation shown by other studies but do not account for the overall decrease in biomass of galled ramets.

Genetic variation in flowering time induces phenological assortative mating: quantitative genetic methods applied to Brassica rapa

It has been argued from first principles that plants mate assortatively by flowering time. However, there have been very few studies of phenological assortative mating, perhaps because current methods to infer paternal phenotype are difficult to apply to natural populations. Two methods are presented to estimate the phenotypic correlation between mates-the quantitative genetic metric for assortative mating-for phenological traits. The first method uses individual flowering schedules to estimate mating probabilities for every potential pairing in a sample. These probabilities are then incorporated into a weighted phenotypic correlation between all potential mates and thus yield a prospective estimate based on mating opportunities. The correlation between mates can also be estimated retrospectively by comparing the regression of offspring phenotype over one parent, which is inflated by assortative mating, to the regression over mid-parent, which is not. In a demonstration experiment with Brassica rapa, the prospective correlation between flowering times (days from germination to anthesis) of pollen recipients and their potential donors was 0.58. The retrospective estimate of this correlation strongly agreed with the prospective estimate. The prospective method is easily employed in field studies that explore the effect of phenological assortative mating on selection response and population differentiation.

A change in climate causes rapid evolution of multiple life-history traits and their interactions in an annual plant.

Climate change is likely to spur rapid evolution, potentially altering integrated suites of life‐history traits. We examined evolutionary change in multiple life‐history traits of the annual plant Brassica rapa collected before and after a recent 5‐year drought in southern California. We used a direct approach to examining evolutionary change by comparing ancestors and descendants. Collections were made from two populations varying in average soil moisture levels, and lines propagated from the collected seeds were grown in a greenhouse and experimentally subjected to conditions simulating either drought (short growing season) or high precipitation (long growing season) years. Comparing ancestors and descendants, we found that the drought caused many changes in life‐history traits, including a shift to earlier flowering, longer duration of flowering, reduced peak flowering and greater skew of the flowering schedule. Descendants had thinner stems and fewer leaf nodes at the time of flowering than ancestors, indicating that the drought selected for plants that flowered at a smaller size and earlier ontogenetic stage rather than selecting for plants to develop more rapidly. Thus, there was not evidence for absolute developmental constraints to flowering time evolution. Common principal component analyses showed substantial differences in the matrix of trait covariances both between short and long growing season treatments and between populations. Although the covariances matrices were generally similar between ancestors and descendants, there was evidence for complex evolutionary changes in the relationships among the traits, and these changes depended on the population and treatment. These results show that a full appreciation of the impacts of global change on phenotypic evolution will entail an understanding of how changes in climatic conditions affect trait values and the structure of relationships among traits.

VARIABLE SELECTION ON EUROSTA'S GALL SIZE, I: THE EXTENT AND NATURE OF VARIATION IN PHENOTYPIC SELECTION

Natural fluctuations in environmental conditions are likely to induce variation in the intensity or direction of natural selection. A long‐term study of the insect, Eurosta solidaginins Fitch (Diptera; Tephritidae), which induces stem galls on the perennial herb Solidago altissima (Asteraceae) was performed to explore the patterns of variation in phenotypic selection. The intensity of selection imposed by parasitoids and predators on gallmaking larvae, for gall size, was measured across 16 populations over the course of 4 generations, for a total of 64 population‐generations. Directional selection was quantified by i, the selection intensity, and variance selection by j‘, a measure of the intensity of selection on phenotypic variance. Size‐dependent attack by parasitoids caused upward directional selection (mean ip = 0.42; SE = 0.023), while size‐dependent bird attack favored larvae that induced smaller galls (mean ib = ‐0.07; SE = 0.013. The mean net directional selection intensity was 0.35 (SE = 0.030), which indicates that insects inducing larger galls are generally favored by selection. The opposing patterns of size‐dependent attack resulted in stabilizing selection in half the population generations, with an overall average. j‘ of ‐0.11 (SE = 0.078). The magnitude of directional selection was strongly influenced by the population mean gall size and weakly by the optimal gall size. The intensity of variance selection was strongly influenced by the shape of the fitness function, with sigmoidal and Gaussian‐like shapes causing greater depletion of phenotypic variance.