Geographic variation in performance of a widespread generalist insect herbivore

1. Generalist herbivores are often widespread and occur in a variety of environments. Due to their broad distribution, it is likely that some populations of generalists will encounter host plants with geographic variation in traits that could affect the herbivore's growth and survival (i.e. performance). However, the geographic pattern of performance has rarely been studied for generalists, especially across large geographic ranges. 2. This study used one of the most generalist herbivore species known, the fall webworm (Hyphantria cunea Drury 1773, Erebidae, Lepidoptera), to experimentally test how the performance of a local population of fall webworms varies with increasing geographic distance of the host plant population from the local herbivore population. Specifically, a transplant experiment was used to compare the performance of one fall webworm population feeding on its local host plants with its performance on host populations from two other locations, 1300 and 2600 km away. 3. It was found that fall webworms performed better on their local host plant populations than on populations from other regions, with performance at its lowest when reared on hosts of the same species from the farthest region. It was also found that local fall webworms do not perform well on hosts commonly used by fall webworms at the other two, more distant sites. 4. This study helps to elucidate how the performance of generalist herbivores varies along their geographic range and suggests possible local adaptation to different sets of hosts across sites.     

Local adaptation: simultaneously considering herbivores and their host plants

? Although a major expectation of coevolutionary theory between plants and herbivores is the occurrence of reciprocal local adaptation, this has remained almost untested. Thus, we evaluated the presence and variation in the patterns of reciprocal local adaptation between an herbivorous insect and its host plant. ? Two four-by-four cross-infestation experiments were performed under similar abiotic conditions. The first one was done under laboratory conditions to estimate herbivore individual performance while the second one was performed in a common garden to simultaneously estimate herbivore population growth rate as well as seed production and plant defenses (resistance and tolerance to herbivory). ? The patterns of population differentiation for the herbivore and the plant were not independent of each other, showing all the possible outcomes from locally adapted to maladapted populations. These results indicate differences in the magnitude of local adaptation. While an association between resistance and herbivore performance was observed, there was no clear pattern between tolerance and herbivore local adaptation. ? Our results demonstrated the occurrence of reciprocal local adaptation following the pattern expected by theory: when the herbivores or the plants were adapted, the other species was non-adapted or even maladapted.     

B型烟粉虱对23种寄主植物适应度的评估和聚类分析

本文利用前期开发的两个寄主植物适应度评估模型对B型烟粉虱能够完成发育的23种寄主进行了寄主适应度评估,并对评估结果进行了聚类分析,分析结果显示供试烟粉虱种群存在明显的寄主偏好性,黄瓜与甘蓝为嗜好寄主,繁殖力大,若虫成活率高,非常有利于烟粉虱的种群发育;而其它寄主在营养状况、物理性状及次生化合物的综合作用下,烟粉虱的寄主植物适应度变化较大且整体低于嗜好寄主,结果暗示烟粉虱的寄主生态位可能存在从核心到周缘的分层现象。比较了两个评估模型的分析结果,虽然在低层聚类中存在差异,但高层聚类的结果趋于一致。     

Host-associated fitness trade-offs do not limit the evolution of diet breadth in the small milkweed bug Lygaeus kalmii (Hemiptera: Lygaeidae)

Theoretical models of evolution in a temporally variable environment predict that genotypes with low variance in fitness across generations will be favored. When host use varies temporally and fitness trade-offs exist among hosts, such that an increase in performance on one host results in a correlated decrease on the other, selection for low variance in fitness across generations will favor genotypes which are generalists. Before predictions such as this can be extended to natural herbivore populations, however, it is necessary to understand the extent to which performance trade-offs limit simultaneous adaptation to multiple hosts. The experiment reported here compares two populations of the common milkweed bug, Lygaeus kalmii (Hemiptera: Lygaeidae) which differ in patterns of host usage. One population is largely restricted to milkweed (Asclepias spp.) when milkweed seeds are available, but becomes a scavenger on a large assortment of available seeds when milkweed seeds are unavailable. The second population is restricted largely to dandelion (Taraxacum officinale), without access to milkweed. We examine these populations to test for host-associated genetic trade-offs between specialization on dandelion (Taraxacum) and two species of milkweed, Asclepias fascicularis, which is low in cardiac glycoside content, and A. speciosa, which is high in cardiac glycoside content. Despite the difference in patterns of host use of the two L. kalmii populations, the populations did not differ in their performance on any of the host plants. Within each population, bugs performed nearly as well on each host, except that bugs had significantly lower survivorship on dandelion than on either milkweed species. Trade-offs in performance among hosts were not present in either population: estimated genetic correlations across hosts were strongly positive. The inability of this study to detect host-associated fitness trade-offs is consistent with most published data on this topic.     

Local adaptation and ecological genetics of host-plant specialization in a leaf beetle

The tendency of insect species to evolve specialization to one or a few plant species is probably a major reason for the remarkable diversity of herbivorous insects. The suggested explanations for this general trend toward specialization include a range of evolutionary mechanisms, whose relative importance is debated. Here we address two potentially important mechanisms: (i) how variation in the geographic distribution of host use may lead to the evolution of local adaptation and specialization; (ii) how selection for specialization may lead to the evolution of trade‐offs in performance between different hosts. We performed a quantitative genetic experiment of larval performance in three different populations of the alpine leaf beetle Oreina elongata reared on two of its main host plants. Due to differences in host availability, each population represents a distinctly different selective regime in terms of host use including selection for specialization on one or the other host as well as selection for utilizing both hosts during the larval stage. The results suggest that selection for specialization has lead to some degree of local adaptations in host use: both single‐host population had higher larval growth rate on their respective native host plant genus, while there was no difference between plant treatments in the two‐host population. However, differences between host plant treatments within populations were generally small and the degree of local adaptation in performance traits seems to be relatively limited. Genetic correlations in performance traits between the hosts ranged from zero in the two‐host population to significantly positive in the single‐host populations. This suggests that selection for specialization in single host populations typically also increased performance on the alternative host that is not naturally encountered. Moreover, the lack of a positive genetic correlation in the two host‐population give support for the hypothesis that performance trade‐offs between two host plants may typically evolve when a population have adapted to both these plants. We conclude that although there is selection for specialization in larval performance traits it seems as if the genetic architecture of these traits have limited the divergence between populations in relative performance on the two hosts.     

Variation in plant quality and the population dynamics of herbivores: there is nothing average about aphids

In the attempt to use results from small-scale studies to make large-scale predictions, it is critical that we take into account the greater spatial heterogeneity encountered at larger spatial scales. An important component of this heterogeneity is variation in plant quality, which can have a profound influence on herbivore population dynamics. This influence is particularly relevant when we consider that the strength of density dependence can vary among host plants and that the strength of density dependence determines the difference between exponential and density- dependent growth. Here, we present some simple models and analyses designed to examine the impact of variable plant quality on the dynamics of insect herbivore populations, and specifically the consequences of variation in the strength of density dependence among host plants. We show that average values of herbivore population growth parameters, calculated from plants that vary in quality, do not predict overall population growth. Furthermore, we illustrate that the quality of a few individual plants within a larger plant population can dominate herbivore population growth. Our results demonstrate that ignoring spatial heterogeneity that exists in herbivore population growth on plants that differ in quality can lead to a misunderstanding of the mechanisms that underlie population dynamics.     

Reciprocal interactions between native and introduced populations of common milkweed,Asclepias syriaca,and the specialist aphid,Aphis nerii

Following its introduction into Europe (EU), the common milkweed (Asclepias syriaca) has been free of most specialist herbivores that are present in its native North American (NA) range, except for the oleander aphid Aphis nerii. We compared EU and NA populations of A. nerii on EU and NA milkweed populations to test the hypothesis that plant–insect interactions differ on the two continents. First, we tested if herbivore performance is higher on EU plants than on NA plants, because the former have escaped most of their herbivores and have perhaps been selected for lower defence levels following introduction. Second, we compared two A. nerii lines (one from each continent) to test whether genotypic differences in the herbivore may influence species interactions in plant–herbivore communities in the context of species introductions. The NA population of A. nerii developed faster, had higher fecundity and attained higher population growth rates than the EU population. There was no overall significant continental difference in aphid resistance between the plants. However, milkweed plants from EU supported higher population growth rates and faster development of the NA line of A. nerii than plants from NA. In contrast, EU aphids showed similar (low) performance across plant populations from both continents. In a second experiment, we examined how chewing herbivores indirectly mediate interactions between milkweeds and aphids, and induced A. syriaca plants from each continent by monarch caterpillars (Danaus plexippus) to compare the resulting changes in plant quality on EU aphid performance. As specialist chewing herbivores of A. syriaca are only present in NA, we expected that plants from the two continents may affect aphid growth in different ways when they are challenged by a specialist chewing herbivore. Caterpillar induction decreased aphid developmental times on NA plants, but not on EU plants, whereas fecundity and population growth rates were unaffected by induction on both plant populations. The results show that genetic variation in the plants as well as in the herbivores can determine the outcome of plant–herbivore interactions.     

Symbiont-induced speciation

Speciation induced by parasitic or mutualistic symbionts has been suggested for taxa ranging from plants to insects to monkeys. Previous models for symbiont-induced speciation have been based upon hybrid inferiority and selection for reinforcement genes. Taken on their own, however, such models have severe theoretical limitations and little empirical support. Two conditions that may favour symbiont-induced speciation are presented here: (1) interaction norms in which the outcomes of host/symbiont interactions differ between environments and (2) differential coadaptation of host and symbiont populations between environments or along an environmental gradient. Symbiont-induced speciation can be considered as one form of 'mixed-process coevolution': reciprocal evolution in which adaptation of a population of one species to a population of a second species (or coadaptation of the populations) causes the population of the second species to become reproductively isolated from other populations.     

Colonization of a host tree by herbivorous insects under a changing climate

Climate warming has been predicted to increase the abundance of herbivorous insects. Together with concurrent poleward shifts in many insect species this may increase herbivore pressure on plants. However, the manner in which plants at higher latitudes become colonized by herbivorous insects in the future is unknown. We established a translocation experiment using 26 micropropagated silver birch Betula pendula genotypes from six populations originating from 60°N to 67°N, to study the susceptibility of the translocated birches to local herbivores. The birches were planted at three different latitudes in Finland (60°N, 62°N and 67°N). We studied the effect of source population and latitudinal translocation on herbivore density, species richness, and community composition among the genotypes growing in the same environmental conditions in two years; 2011 and 2012. The source population explained the variation in the herbivore density only in 2012, whereas latitudinal translocation did not affect herbivore density. Variation in species richness was not explained by the source population or by the latitudinal translocation. At two of the study sites, the similarity of the herbivore communities among the populations decreased with increasing latitudinal distance of the source populations, possibly because birch populations that grow geographically closer to each other are genetically more similar, and therefore support a more similar composition of the arthropod community. All birch genotypes were colonized by local herbivores, suggesting that as herbivores shift their ranges polewards, they are able to colonize novel host‐plant genotypes. This enables compositional changes in insect communities on their host plants in the future, which in turn, might affect total herbivory and eventually, plant growth.     

Geographical divergence in host use ability of a marine herbivore in alga–grazer interaction

When the selective environment differs geographically, local herbivore populations may diverge in their host use ability and adapt locally to exploit the sympatric host population. We tested whether populations of the marine generalist herbivore Idotea baltica have diverged in host us ability and whether they locally adapted to exploit the sympatric population of their main host species, the bladderwrack Fucus vesiculosus. We fed isopods from three local populations reciprocally with the sympatric and two allopatric populations of the host. The bladderwrack populations varied in their quality as food for isopods suggesting variation in the selective environment. The ability to exploit the main host showed considerable divergence among the isopod populations. There was no significant interaction between host and isopod origin, indicating that the patterns observed in the reciprocal feeding experiment could be explained by differences in overall suitability of the hosts and differences in overall performance of the isopod populations. Isopod population that was sympatric to a bladderwrack population with low phlorotannin content showed high performance on the algae from the sympatric but low performance on the algae from the two allopatric populations. Performance of isopods, especially in this population, decreased quickly with the increasing phlorotannin content of food algae. We therefore hypothesize that the isopods adapted to a low phlorotannin content were unable to utilize high-phlorotannin algae efficiently. Isopod populations sympatric to the high-phlorotannin bladderwrack populations may be generally better adapted to deal with phlorotannins, being thereby able to utilize a range of bladderwrack populations.     

Butterfly–host plant synchrony determines patterns of host use across years and regions

Variation in the degree of synchrony among host plants and herbivores can disrupt or intensify species interactions, alter the strength of natural selection on traits associated with phenological timing, and drive novel host plant associations. We used field observations from three regions during four seasons to examine how timing of the butterfly herbivore Anthocharis cardamines relative to six host plant species (Arabis hirsuta, Cardamine pratensis, Arabis glabra, Arabidopsis thaliana, Thlaspi caerulescens and Capsella bursa‐pastoris) influenced host species use and the choice of host plant individuals within populations. Butterflies laid a larger fraction of their eggs on species that were closer to the butterfly's preferred stage of development than on other host species. Within host plant populations, butterflies showed a stronger preference for individuals with a late phenology when plants within the population were on average more developed at the time of butterfly flight. Our results suggest that changes in synchrony between herbivores and their host plants are associated with changes in both host species use and the choice of host plant individuals differing in phenology within populations. This is likely to be an important mechanism generating variation in interaction intensities and trait selection in the wild, and therefore also relevant for understanding how anthropogenic induced changes, such as global warming, will influence natural communities.     

Population differentiation related to climate of origin affects the intensity of plant–herbivore interactions in a clonal grass

With ongoing climate change, it is likely that shifts in species distribution ranges will lead to changes in the type and intensity of plant–herbivore interactions. Plants currently exposed to lower levels of herbivory could have less developed defensive mechanisms and therefore could suffer in case of increased herbivore pressure.We performed a common garden experiment using clones of Festuca rubra originating from four populations experiencing contrasting temperature and precipitation regimes. Clones of identical genotype were subjected to both the control and the herbivory treatment using larvae of the nymphalid butterfly Coenonympha pamphilus, a generalist herbivore feeding on several grass species. Various measures of constitutive and induced defence as well as growth response to herbivory were assessed, compared between populations of different climatic origin and related to herbivore performance (larval survival).The four F. rubra populations significantly differed in constitutive defence (content of Si and total phenols), nutritional quality (content of C) and inducibility of defence (change in total phenols), but not in growth response to herbivory. Herbivores survived better on populations from colder climate and better survival was generally related to lower Si content and lower initial plant size.We demonstrated population differentiation in both constitutive and induced defence against insect herbivory, which directly affected survival of a generalist herbivore. Our findings confirmed the expectation that plants from higher elevations are more prone to herbivory. Moreover, differences in various aspects of plant defence between populations from the same altitude stresses the need of considering multiple factors when assessing the effect of climate on plant–herbivore interactions.     

Simultaneous inbreeding modifies inbreeding depression in a plant–herbivore interaction

Because inbreeding is common in natural populations of plants and their herbivores, herbivore‐induced selection on plants, and vice versa, may be significantly modified by inbreeding and inbreeding depression. In a feeding assay with inbred and outbred lines of both the perennial herb, Vincetoxicum hirundinaria, and its specialist herbivore, Abrostola asclepiadis, we discovered that plant inbreeding increased inbreeding depression in herbivore performance in some populations. The effect of inbreeding on plant resistance varied among plant and herbivore populations. The among‐population variation is likely to be driven by variation in plant secondary compounds across populations. In addition, inbreeding depression in plant resistance was substantial when herbivores were outbred, but diminished when herbivores were inbred. These findings demonstrate that in plant–herbivore interactions expression of inbreeding depression can depend on the level of inbreeding of the interacting species. Furthermore, our results suggest that when herbivores are inbred, herbivore‐induced selection against self‐fertilisation in plants may diminish.     

GENETIC COVARIANCE BETWEEN OVIPOSITION PREFERENCE AND LARVAL PERFORMANCE IN AN INSECT HERBIVORE

An experimental study determined that females of the herbivorous fly species Liriomyza sativae (Diptera: Agromyzidae) preferentially oviposit on the plant species on which their female progeny attain the greatest pupal weight. A modified parent/offspring regression was used to quantify this relationship as an additive genetic covariance between host-plant preference and relative performance of female larvae on different plant species. The implications of a genetic covariance between preference and performance on the course of evolution in herbivores are discussed. Several females from one population refused to oviposit on one of the plant species; this population also suffered the only significant larval mortality on this plant. These results corroborate the avoidance of unsuitable host plants seen in the genetic analyses of individuals, but relative to the genetic data, such population-level data are of limited usefulness in the study of evolutionary mechanisms by which insect populations become adapted to their host plants.     

The Role of Adaptation to Host Plants in the Evolution of Reproductive Isolation: Negative Evidence from Tetranychus Urticae Koch

Reproductive isolation between demes of a phytophagous arthropod population that use different host plant species could evolve in two different ways. First, adaptation to different host species might result in reproductive isolation as a pleiotropic by-product. Second, if adaptation to one host species strongly reduces fitness on others, selection could favour mechanisms, such as host fidelity and assortative mating, that restrict gene flow between host-adapted demes. A laboratory selection experiment on the broadly polyphagous spider mite Tetranychus urticae gave information on these possibilities. A population allowed to adapt to tomato plants showed increased survival, development rate and fecundity on tomato relative to the base population from which it was derived. In spite of the large difference between the tomato-adapted and base populations in performance on tomato plants, the two populations showed no evidence of reproductive isolation, as measured by the hatching rate of eggs laid by F1 hybrids between the lines. Furthermore, a genetically variable population formed by hybridizing the tomato-adapted and base populations did not show evidence for a decline in ability to survive on tomato after more than ten generations of mass rearing on lima bean, indicating that tomato-adapted genotypes suffered little or no selective disadvantage on bean. These results give no support for the role of host plants in the evolution of reproductive isolation in T. urticae.     

Host‐plant genotypic diversity and community genetic interactions mediate aphid spatial distribution

Genetic variation in plants can influence the community structure of associated species, through both direct and indirect interactions. Herbivorous insects are known to feed on a restricted range of plants, and herbivore preference and performance can vary among host plants within a species due to genetically based traits of the plant (e.g., defensive compounds). In a natural system, we expect to find genetic variation within both plant and herbivore communities and we expect this variation to influence species interactions. Using a three‐species plant‐aphid model system, we investigated the effect of genetic diversity on genetic interactions among the community members. Our system involved a host plant (Hordeum vulgare) that was shared by an aphid (Sitobion avenae) and a hemi‐parasitic plant (Rhinanthus minor). We showed that aphids cluster more tightly in a genetically diverse host‐plant community than in a genetic monoculture, with host‐plant genetic diversity explaining up to 24% of the variation in aphid distribution. This is driven by differing preferences of the aphids to the different plant genotypes and their resulting performance on these plants. Within the two host‐plant diversity levels, aphid spatial distribution was influenced by an interaction among the aphid's own genotype, the genotype of a competing aphid, the origin of the parasitic plant population, and the host‐plant genotype. Thus, the overall outcome involves both direct (i.e., host plant to aphid) and indirect (i.e., parasitic plant to aphid) interactions across all these species. These results show that a complex genetic environment influences the distribution of herbivores among host plants. Thus, in genetically diverse systems, interspecific genetic interactions between the host plant and herbivore can influence the population dynamics of the system and could also structure local communities. We suggest that direct and indirect genotypic interactions among species can influence community structure and processes.     

Tests of associational defence provided by hairy plants for glabrous plants of Arabidopsis halleri subsp. gemmifera against insect herbivores

1. Trichome‐producing (hairy) and trichomeless (glabrous) plants of Arabidopsis halleri subsp. gemmifera were investigated to test whether plant resistance to herbivory depends on the plants' phenotypes and/or the phenotypes of neighbouring plants (associational effects). 2. A common garden experiment was conducted in which the relative frequency of hairy and glabrous plants was manipulated. Two species of leaf‐chewing insects (larvae of a white butterfly and a cabbage sawfly) were found less often on hairy plants than on glabrous plants. By contrast, the numbers of aphids and flea beetles did not differ significantly between hairy and glabrous plants. For none of these insects did abundance depend on the frequency of the two plant morphs. 3. A field survey was conducted in two natural populations of A. halleri. In the first population, a species of white butterfly was the dominant herbivore, and hairy plants incurred less leaf damage than glabrous plants across 2 years. By contrast, in the other population, where flea beetles were dominant, there were no consistent differences in leaf damage between the two types of plants. In neither of the two populations was any evidence found of associational effects. 4. This study did not provide any conclusive evidence of associational effects of anti‐herbivore resistance, but it was discovered that trichomes can confer resistance to certain herbivores. Given the results of previous work by the authors on associational effects against a flightless leaf beetle, such associational effects of the trichome dimorphism of A. halleri were herbivore‐specific.     

Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Scrophulariaceae)

Previous studies have demonstrated genetic variation for resistance to insect herbivores and host plant quality. The effect of plant mating system, an important determinant of the distribution of genetic variation, on host plant characteristics has received almost no attention. This study used a controlled greenhouse experiment to examine the effect of self- and cross-pollination in Mimulus guttatus (Scrophulariaceae) on resistance to and host plant quality for the xylem-feeding spittlebug Philaenus spumarius (Homoptera: Cercopidae). Spittlebugs were found to have a negative effect on two important fitness components in M. guttatus, flower production and above ground biomass. One of two M. guttatus populations examined showed a significant interaction between the pollination and herbivore treatments. In this case, the detrimental effects of herbivores on biomass and flower production were much more pronounced in inbred (self) plants. The presence of spittlebug nymphs increased inbreeding depression by as much as three times. Pollination treatments also had significant effects on important components of herbivore fitness, but these effects were in opposite directions in our two host plant populations. Spittlebug nymphs maturing on self plants emerged as significantly larger adults in one of our host plant populations, indicating that inbreeding increased host plant quality. In our second host plant population, spittlebug nymphs took significantly longer to develop to adulthood on self plants, indicating that inbreeding decreased host plant quality. Taken together these results suggest that the degree of inbreeding in host plant populations can have important and perhaps complex effects on the dynamics of plant-herbivore interactions and on mating-system evolution in the host.     

Effect of population size on the prospect of species survival

Many recent studies have demonstrated a negative effect of small population size on single plant traits. However, not much is known about the actual consequences of reduced plant performance on the long-term prospect of species survival. I studied the effect of population size on population growth rate and survival probability in the rare perennial herbScorzonera hispanica occurring in fragmented grasslands. Its performance was measured using several traits related to reproduction in 21 populations ranging in size from 3 to 2475 plants. These data were then connected with data on full demography of the species from three of the studied populations. Two different matrix models differing in the number of transitions based on measurements in the populations differing in size were used to explore the relationship between population size and population growth rate. Both matrix models showed that despite the decline in seed production in small populations, population growth rate is never significantly different from one, and the populations could thus be expected to survive in the long run. Calculations of extinction probabilities that take into account demographic and environmental stochasticity, however, showed that populations below 100 flowering individuals have a high probability to become extinct. This demonstrates that demographic and environmental stochasticity is an important driver of the fate of small populations in this system. This study demonstrates that estimation of population growth rate can provide new insights into the effect of population size on population growth and survival. It also shows how matrix models enable the combination various pieces of information about the single populations into one overall measure, and may provide a useful tool for the standardization of studies on the effects of population size on population performance.