Cris G. Hochwender

Evidence for Local Adaptation in Closely Adjacent Subpopulations of Northern Red Oak (Quercus rubra L.) Expressed as Resistance to Leaf Herbivores

Many studies of herbaceous plant populations have illustrated the potential of adjacent subpopulations to adapt to local ecological conditions. However, the extent to which local adaptation on a small geographical scale can occur in outcrossing tree populations is not well understood. In this study, we reciprocally transplanted acorns from adjacent subpopulations of northern red oak (Quercus rubra L.) occupying north-, southwest-, and west-facing slopes within a 4-ha plot in a Missouri oak-hickory forest. The quantitative character we measured was leaf damage by herbivores on first-year seedlings, because it reflects resistance to insect herbivores-a quantitative trait that could be under different selective pressures in dissimilar microhabitats. We found that seedlings showed the least damage when planted at the site of the maternal plant. This finding provides initial but strong evidence of local adaptation and illustrates that selection associated with leaf harbivory may have a strong impact on the genetic structure of local tree populations. Such a result is unexpected for a widely outcrossing species on such a small geographical scale but indicates that genetic structuring is possible within other plant populations occupying heterogeneous environments.

The potential for and constraints on the evolution of compensatory ability in Asclepias syriaca

Abstract To investigate the potential for and constraints on the evolution of compensatory ability, we performed a greenhouse experiment using Asclepias syriaca in which foliar damage and soil nutrient concentration were manipulated. Under low nutrient conditions, significant genetic variation was detected for allocation patterns and for compensatory ability. Furthermore, resource allocation to storage was positively, genetically correlated both with compensatory ability and biomass when damaged, the last two being positively, genetically correlated with each other. Thus, in the low nutrient environment, compensatory ability via resource allocation to storage provided greater biomass when damaged. A negative genetic correlation between compensatory ability and plant biomass when undamaged suggests that this mechanism entailed an allocation cost, which would constrain the evolution of greater compensatory ability when nutrients are limited. Under high nutrient conditions, neither compensatory ability nor allocation patterns predicted biomass when damaged, even though genetic variation in compensatory ability existed. Instead, plant biomass when undamaged predicted biomass when damaged. The differences in outcomes between the two nutrient treatments highlight the importance of considering the possible range of environmental conditions that a genotype may experience. Furthermore, traits that conferred compensatory ability did not necessarily contribute to biomass when damaged, demonstrating that it is critical to examine both compensatory ability and biomass when damaged to determine whether selection by herbivores can favor the evolution of increased compensation.

Plant genetic differences influence herbivore community structure: evidence from a hybrid willow system

To determine the influence of plant genetic variation on community structure of insect herbivores, we examined the abundances of 14 herbivore species among six genetic classes of willow: Salix eriocephala, S. sericea, their F1 and F2 interspecific hybrids, and backcross hybrids to each parental species. We placed 1-year-old plants, grown from seeds generated from controlled crosses, in a common garden. During the growing season, we censused gall-inducing flies and sawflies, leaf-mining insects, and leaf-folding Lepidoptera to determine the community structure of herbivorous insects on the six genetic classes. Our results provided convincing evidence that the community structure of insect herbivores in this hybrid willow system was shaped by genetic differences among the parental species and the hybrid genetic classes. Using MANOVA, we detected significant differences among genetic classes for both absolute and relative abundance of herbivores. Using canonical discriminant analysis, we found that centroid locations describing community structure of the insect herbivores differed for each genetic class. Moreover, the centroids for the four hybrid classes were located well outside of the range between the centroids for the parental species, suggesting that more than additive genetic effects of the two parental species influenced community formation on hybrid classes. Line-cross analysis suggested that plant genetic factors responsible for structuring the herbivore community involved epistatic effects, as well as additive and dominance effects. We discuss the ramifications of these results in regard to the structure of insect herbivore communities on plants and the implications of our findings for the evolution of interspecific interactions.

FLUCTUATING ASYMMETRY IN A SALIX HYBRID SYSTEM: THE IMPORTANCE OF GENETIC VERSUS ENVIRONMENTAL CAUSES

To examine the effects of hybridization and environmental stress on developmental instability, we examined fluctuating asymmetry (FA), the variance in random deviations from perfect symmetry in bilaterally symmetrical traits, for leaf symmetry in a Salix hybrid system. An abiotic environmental stress (water stress), an interspecific biotic stress (pathogen attack), and an intraspecific biotic stress (competition) were examined to determine which factors increase developmental instability. None of these three environmental stressors significantly increased FA. However, genetic stress through hybridization was detected; hybrid plants showed significantly higher levels of FA than parental species. In contrast to hybridization providing greater developmental stability through heterozygosity, these results suggest that complex, nonadditive interactions provided developmental stability and that developmental instability increased when coadapted gene complexes were disrupted through hybridization. In addition, plant biomass was significantly, negatively correlated with FA, suggesting that those individuals that were more able to buffer themselves against the disruptive effects of environmental stress may have a selective advantage over those that are less able to buffer themselves against these disruptive effects.

FITNESS AND GENETIC ARCHITECTURE OF PARENT AND HYBRID WILLOWS IN COMMON GARDENS

Abstract Models of hybrid zone dynamics incorporate different patterns of hybrid fitness relative to parental species fitness. An important but understudied source of variation underlying these fitness differences is the environment. We investigated the performance of two willow species and their F1, F2, and backcross hybrids using a common‐garden experiment with six replicated gardens that differed in soil moisture. Aboveground biomass, catkin production, seed production per catkin, and seed germination rate were significantly different among genetic classes. For aboveground biomass and catkin production, hybrids generally had intermediate or inferior performance compared to parent species. Salix eriocephala had the highest performance for all performance measures, but in two gardens F1 plants had superior or equal performance for aboveground biomass and female catkin production. Salix eriocephala and backcrosses to S. eriocephala had the highest numbers of filled seeds per catkin and the highest estimates of total fitness in all gardens. Measures of filled seeds per catkin and germination rate tend to support the model of endogenous hybrid unfitness, and these two measures had major effects on estimates of total seed production per catkin. We also estimated how the two willow species differ genetically in these fitness measures using line cross analysis. We found a complex genetic architecture underlying the fitness differences between species that involved additive, dominance, and epistatic genetic effects for all fitness measures. The environment was important in the expression of these genetic differences, because the type of epistasis differed among the gardens for aboveground biomass and for female catkin production. These findings suggest that fine‐scale environmental variation can have a significant impact on hybrid fitness in hybrid zones where parents and hybrids are widely interspersed.

Genetic architecture of susceptibility to herbivores in hybrid willows.

We performed a common garden experiment using parental, F1, F2, and backcross willow hybrids to test the hypothesis that hybrid willows experience breakdown of resistance to herbivores. After exposing plants to herbivores in the field, we measured the densities/damage caused by 13 insect herbivores and one herbivorous mite. Using joint‐scaling tests, we determined the contribution of additive, dominance, and epistasis to variation in susceptibility to herbivores (measured either as density or damage level) among the six genetic classes. We found the genetic architecture of susceptibility/resistance in the parental species to be complex, involving additive, dominance, and epistasis for each herbivore species. Although genic interactions altered plant susceptibility for each of the 14 herbivores, three distinct patterns of response of herbivores to hybrids were expressed. One pattern, observed in four herbivore species, supported the hypothesis of breakdown of resistance genes in recombinant hybrids. A second pattern, shown by six other herbivore species, supported the hypothesis of hybrid breakdown of host recognition genes. In other words, epistatic interactions for host recognition traits (probably oviposition/feeding stimulants or attractants) appeared to be important in determining herbivore abundance for those six species. The final patterns supported a structure of dominance, either for host recognition traits (in the case of three herbivore species) or for host resistance traits (for one herbivore species). The combination of differing responses of herbivore species, including members of the same genus and tribe, and the ubiquitous importance of epistasis suggests that many genes affect herbivore resistance in this hybrid willow system.

Fitness Consequences of Herbivory on Quercus alba

Abstract Leaf herbivores potentially reduce plant fitness by increasing fruit abortion. The impact of leaf herbivory on fruit abortion, however, may vary with branch height in trees because of differential investment in reproduction among branches, differences among branches in exposure to solar radiation and the mobility of resource movement among branches following defoliation. Here we describe spatial patterns in abundance of lepidopteran herbivores and resultant damage in the canopy of mature white oak trees, Quercus alba. The effect of foliar damage on fruit abortion for upper and lower canopy branches was also examined. A significant positive correlation occurred between foliar damage and spring herbivore abundance. Damage measured at the end of the season was unevenly distributed throughout the canopy, varying from 10–20% leaf area loss. A significant positive correlation between percent herbivore damage and percent fruit abortion also existed. Moreover, upper canopy branches had a higher percentage of fruit abortion for a given damage level than lower canopy branches, even though herbivore damage did not differ significantly with canopy height. These results suggest that early season leaf-chewing herbivores negatively affected fruit production, but the impact on fruit abortion depended upon the location of the damaged branch. Resources apparently did not move from lesser-damaged branches to more heavily damaged branches to reduce reproductive losses.

Using hybrid systems to explore the evolution of tolerance to damage.

Hybridization is common and important to the adaptive evolution of plants. Hybridization has resulted in the formation of new species and the introgression of traits between species. This paper discusses the advantages of using hybrid systems to explore the evolution of tolerance to herbivore damage (i.e., the ability to diminish the negative effects of damage on fitness). The major consequence of hybridization likely to make it influential for tolerance evolution is that hybridization generates broad variation in traits that can be selected for or against. In addition to generating greater variation in tolerance to damage and its putative traits (e.g., traits associated with allocation patterns and meristem production), hybridization can generate greater independence among tolerance traits and between tolerance and defense traits. Greater independence may provide a greater ability to discern mechanisms of tolerance, give a greater probability of detecting allocation costs of tolerance, and provide an effective means to evaluate tradeoffs between tolerance and defense. Interspecific hybrid systems can also be used to evaluate the importance of co-adaptation of tolerance traits. Moreover, recombinant hybrids can be used in selection studies focusing on tolerance to damage to discern whether parental combinations of tolerance traits are favored over novel combinations. Research in hybrid systems that investigate the selective importance of tolerance, the patterns of inheritance of tolerance traits, and the genetic architecture of plant species involved can be vital to our evaluation of the adaptive role of tolerance to damage.