Robert S. Fritz

Interspecific hybridization of plants and resistance to herbivores : hypotheses, genetics, and variable responses in a diverse herbivore community

We studied the morphology, molecular genetics, and hebivory of two species of willows (Salix sericea and S. eriocephala) and their interspecific hybrids to test four alternative hypotheses concerning the effects of hybridization on plant resistance. Individually marked plants were identified using morphological traits in the field and measurements of stipule and leaf pubescence were made and compared using Canonical Discriminant Function Analysis. DNA was extracted from the leaves of a sample of the marked plants and RAPD-PCR analysis was performed to establish the genetic status of parental and hybrid plants. RAPD band analysis generally verified the genetic status of parental plants. Hybrid plants were usually correctly identified in the field with a few exceptions. However, the hybrid plants were a heterogeneous group of plants made up of most plants that appear to be F1s and a few plants that appear to be backcrosses to S. sericea. Morphological variables were useful for distinguishing S. sericea from S. eriocephala and hybrids, but were not as dependable in distinguishing between S. eriocephala and hybrids. We compared the densities of 11 herbivore species and the infection by a leaf rust pathogen (Melampsora sp.) on the leaves and stems of two parents and the hybrids in the field. We found support for the Additive hypothesis (3 species), the Dominance hypothesis (2 species) and the Hybrid Susceptibility hypothesis (7 species, 6 herbivores and the Melampsora rust). We found no evidence for the Hybrid Resistance hypothesis. Guild membership was not a good predictor of similar responses of species to hybrid versus parental plants. A Canonical Discriminant Function Analysis showed discrete separation of the taxa based on herbivore densities, illustrating different community structures on hybrid and parental plants. This study demonstrates the diversity of responses of phytophages in response to interspecific hybridization.

Genetic Variation Among Plants and Insect Community Structure: Willows and Sawflies

The effects of both genotype and spatial position of host plants on density, proportion, and total community structure of herbivore species were experimentally tested for a guild of gall-forming sawflies on their host plant, the arroyo willow, Salix lasiolepis. Genetic differences among individually potted stem cuttings from 6 and 12 willow plants were found to have significant effects on the densities of each of the four sawfly species and on their proportional representation on willow clones. Analyses also showed that the total community structure (proportions of species) varied among clones. Proportional over- lap values showed that two of the willow clones differed markedly from the others regarding the predominant species on them. However, phenotypic correlations showed that the sawfly species were positively correlated among plants during 2 yr. Genotypic correlations were positive and mostly significant in 1985, but were mostly nonsignificant in 1986. Estimates of broad-sense heritability indicated that between 20 and 50% of variation in the density of two species, the stem galler (Euura lasiolepis) and the leaf folder (Phyllocolpa sp.), was due to clone genotype, whereas only 9-28% of variation in the density of the leaf galler (Pontania sp.) and the petiole galler (Euura sp.) was due to clone genotype. Environmental variation due to spatial position of plants contributed little to variation in density of species in experiments in 1985, but was an important source of variation in 1986 for three species. As a consequence species proportion for all species varied signifi- cantly among rack positions of the willow pots. In 1986, clone x position interactions were not significant for species density or for species proportion, with the exception of the leaf folder, which showed marginal significance. Thus, there was little evidence of geno- type x position interactions. These studies suggest that plant genetic variation may be an important variable influencing community structure of phytophagous insects on host plants within plant populations. Plant morphological traits that are important to sawfly oviposition in the field (e.g., mean shoot length) differed significantly among willow clones in both years and were correlated with the variation in density of three of the four sawfly species among all plants in both years. In 1985, correlations between shoot length and species density based on clone means were significant for all four species, but in 1986, none of the correlations was significant, although for three of the four species correlation coefficients were similar in magnitude to those from 1985. Species density of the leaf folder, stem gallery, and petiole galler were also correlated with leaf length among plants and clones in 1985. These data tentatively suggest that there are positive genetic correlations between plant characteristics and susceptibility to sawfly galling.

Morphological and molecular evidence for hybridization and introgression in a willow ( Salix ) hybrid zone

Hybrid zones provide biologists with the opportunity to examine genetic and ecological interactions between differentiated populations. Accurate identification of hybrid genealogies is considered a necessary prerequisite to understanding observed patterns of hybridization–related phenomena. We analysed molecular and morphological data from individuals in a hybrid zone between two species of willows (Salix sericea Marshall and S. eriocephala Michaux) and report the use of randomly amplified polymorphic DNA (RAPD), chloroplast DNA (cpDNA), and ribosomal DNA (rDNA) markers, as well as vegetative morphology and foliar chemistry data to identify individuals in terms of hybrid genealogy and to infer the direction and extent of backcrossing and introgression within the hybrid zone. A novel version of a maximum likelihood estimate approach (developed for this study) was used to calculate hybrid index scores from RAPD marker data; this method produced results similar to those obtained using traditional arithmetic methods. Distribution of rDNA, cpDNA, and chemistry data were examined within the graphical context of RAPD–based hybrid index score histograms and principal component analyses (PCA) on RAPD and morphology data. Seven of the 21 plants classified as S. eriocephala in the field were possible introgressants. Another plant presented an unequivocal example of backcrossed S. sericea chemistry and RAPD markers. Inter– and intraspecific chloroplast diversity found within the hybrid zone suggests both historic introgression (perhaps in a glacial refugium), and contemporary hybridization. Patterns of inheritance and expression within the hybrid zone suggest that morphological characters are often not expressed in a simple additive fashion, and problems associated with both morphological and molecular data are considered.

RESISTANCE OF HYBRID PLANTS TO HERBIVORES: GENES, ENVIRONMENT, OR BOTH?

Analyses of resistance of hybrid plants to herbivores in natural populations have revealed a diversity of patterns, including hybrid susceptibility, hybrid dominance, and hybrid intermediacy. But because many of these studies are conducted on unknown genotypes of hybrid plants in natural habitats, the genetic and environmental causes of the patterns cannot be distinguished. Predicted patterns and models of underlying genetic and environmental causes of these patterns are presented for F1, F2, and BC hybrid genotypes. It is argued that progress in resolving the causal relationships in hybrid plant–herbivore interactions will require experimentation that compares known hybrid genotypes in a combination of common garden and reciprocal transplant experiments. Such experiments will also permit tests of genotype-by-environment interactions in hybrid resistance that parallel hypotheses of hybrid plant fitness in hybrid zones.

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.

Reproductive success and foraging of the crab spider Misumena vatia

SummaryReproductive success and growth rate data were collected for individually marked crab spiders Misumena vatia (Clerck) in 1980, 1981, and 1982. All measures of reproductive success were found to be quite variable between individuals within years, but did not differ between years. Reproductive effort (mass of clutch/prereproductive mass of female) was the least variable measurement and was not correlated with female weight at reproduction. Clutch weight and number of eggs per clutch were highly correlated with female reproductive weight. Egg weight was not correlated with the number of eggs per clutch. Hatching success did not vary with clutch size and averaged 94.5%. Growth rates of spiders were highly variable, indicating large variation in feeding rate. In 1981 and 1982, approximately 20% of female spiders were unable to capture enough prey to grow and reproduce. Primary prey species differed in weight and in their contribution to spider egg production. Spiders attacked a larger percentage of bumblebees but captured a larger percentage of honeybees. There was no simple relationship between diet choice and reproductive success. Spiders which selected suboptimal umbels to forage on some or all of the time, however, had significantly lower reproductive success than spiders choosing the best umbels.

Ant Protection of a Host Plant's Defoliator: Consequence of an Ant‐Membracid Mutualism

Black locust (Robinia pseudoacacia) is extensively defoliated by the locust leaf-mining beetle (Odontota dorsalis) in western Maryland. This plant is also the host of Vanduzea arquata (Membracidae), a gregarious, sap-feeding treehopper, which is tended by the ant Formica subsericea. Aggression by F. subsericea reduced adult density and density of egg masses of 0. dorsalis on branches with Vanduzea tended by Formica (ant branches) compared to non-ant branches. Obser- vations and staged encounters also showed that Formica ants excluded Nabicula subcoleoptrata, an important predator of 0. dorsalis larvae, from branches with Formica and Vanduzea. Thus, ants indirectly protected the beetle larvae from this predator. In both 1980 and 1981 survivorship of beetle larvae was significantly higher in the presence of ants. In 1980 this resulted in nearly twice as many beetle larvae surviving on ant branches even when egg mass density was initially lower. In 1981 beetle survivorship was higher on branches with ants, although numbers of larvae remained higher on non- ant branches compared to ant branches. There was no apparent net benefit or harm to black locust in having Formica ants and Vanduzea treehoppers, although these results suggest a mechanism by which ant attendance could harm the plant indirectly. These results are contrary to previous studies of ant-Homoptera-plant associations.

The ecology and evolution of host-plant resistance to insects

Genetic techniques have yielded new insights into plant-herbivore coevolution. Quantitative genetic tests of herbivory theory reveal that in some cases insect herbivores impose selection on resistance traits. Also, some resistance traits are costly while others appear not to be, and genetic models can explain these results. Genetic variation in plant resistance influences insect community structure by modifying interactions of herbivores with competitors and natural enemies. Therefore, models of multispecies coevolution are more realistic than pairwise coevolutionary models. Ecological genetics will facilitate further theoretical and empirical exploration of multispecies coevolution of plants and herbivores.

SELECTION FOR HOST MODIFICATION BY INSECT PARASITOIDS

The ability of parasites to influence the behavior of their hosts is an important aspect of parasite-host biology (Price, 1980). Holmes and Bethel (1972) review an extensive literature that documents the influence of parasites on the behavior of their intermediate hosts. They argue that these effects by parasites on their hosts are adaptations of the parasites to increase transmission to subsequent hosts. Holmes and Bethel suggest that parasites affect intermediate host behavior by reducing stamina, increasing conspicuousness, causing disorientation, and altering responses so that hosts are more susceptible to predation by the definitive host of their parasites. Modification of insect hosts by their parasitoids, however, has received little attention. Insect parasitoids, unlike parasites, are of relatively large size, they possess a freeliving stage, and their development kills the hosts; therefore their effect on host population dynamics resembles that of predators (Doutt, 1959). Parasitoids, other than insects, and parasitic castrators show similar characteristics (Kuris, 1974; Trail, 1980). Most insect species are attacked by one or more parasitoid species during their development. The growth, development, and survival of parasitized hosts are of direct consequence to the parasitoids; if the host dies before the parasitoid emerges, so does the parasitoid. Vinson (1975) developed the concept that host regulation is necessary for the parasitoids success. He stated that growth and development of parasitoids were enhanced by physiological regulation of the host through venoms, hormones and parasitoid feeding. Parasitized hosts may behave differently from unparasitized hosts in predator avoidance responses, microhabitat selection, and developmental and growth rates. Some of these modifications may be adaptively significant, and promote the coevolution between the host and its parasitoid. Here I propose a hypothesis that extends Vinsons host regulation concept to explain the evolution of host modification by insect parasitoids. This hypothesis leads to predictions of the characteristics of hosts that should influence how parasitoids should modify their hosts.

Secondary chemistry of hybrid and parental willows: Phenolic glycosides and condensed tannins inSalix sericea, S. eriocephala, and their hybrids

Salix sericea andS. eriocephala differ markedly in secondary chemistry.S. sericea produces phenolic glycosides, salicortin and 2′-cinnamoylsalicortin, and low concentrations of condensed tannin. In contrast,S. eriocephala produces no phenolic glycosides, but high concentrations of condensed tannins. Hybrid chemistry is intermediate for both types of chemicals, suggesting predominantly additive inheritance of these two defensive chemical systems from the parental species. However, there is extensive variation among hybrids. This variation may be due to genetic variation among parental genotypes, which genes were passed on, or to subsequent back-crossing. The differences in chemistry are likely to exert a strong effect on the relative susceptibility of hybrid and parental willows to herbivores.