Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences

Plants and herbivores are thought to be engaged in a coevolutionary arms race: rising frequencies of plants with anti-herbivore defences exert pressure on herbivores to resist or circumvent these defences and vice versa. Owing to its frequency-dependent character, the arms race hypothesis predicts that herbivores exhibit genetic variation for traits that determine how they deal with the defences of a given host plant phenotype. Here, we show the existence of distinct variation within a single herbivore species, the spider mite Tetranychus urticae, in traits that lead to resistance or susceptibility to jasmonate (JA)-dependent defences of a host plant but also in traits responsible for induction or repression of JA defences. We characterized three distinct lines of T. urticae that differentially induced JA-related defence genes and metabolites while feeding on tomato plants (Solanum lycopersicum). These lines were also differently affected by induced JA defences. The first line, which induced JA-dependent tomato defences, was susceptible to those defences; the second line also induced JA defences but was resistant to them; and the third, although susceptible to JA defences, repressed induction. We hypothesize that such intraspecific variation is common among herbivores living in environments with a diversity of plants that impose diverse selection pressure.     

Effects of host plant on life‐history traits in the polyphagous spider mite Tetranychus urticae

Studying antagonistic coevolution between host plants and herbivores is particularly relevant for polyphagous species that can experience a great diversity of host plants with a large range of defenses. Here, we performed experimental evolution with the polyphagous spider mite Tetranychus urticae to detect how mites can exploit host plants. We thus compared on a same host the performance of replicated populations from an ancestral one reared for hundreds of generations on cucumber plants that were shifted to either tomato or cucumber plants. We controlled for maternal effects by rearing females from all replicated populations on either tomato or cucumber leaves, crossing this factor with the host plant in a factorial design. About 24 generations after the host shift and for all individual mites, we measured the following fitness components on tomato leaf fragments: survival at all stages, acceptance of the host plant by juvenile and adult mites, longevity, and female fecundity. The host plant on which mite populations had evolved did not affect the performance of the mites, but only affected their sex ratio. Females that lived on tomato plants for circa 24 generations produced a higher proportion of daughters than did females that lived on cucumber plants. In contrast, maternal effects influenced juvenile survival, acceptance of the host plant by adult mites and female fecundity. Independently of the host plant species on which their population had evolved, females reared on the tomato maternal environment produced offspring that survived better on tomato as juveniles, but accepted less this host plant as adults and had a lower fecundity than did females reared on the cucumber maternal environment. We also found that temporal blocks affected mite dispersal and both female longevity and fecundity. Taken together, our results show that the host plant species can affect critical parameters of population dynamics, and most importantly that maternal and environmental conditions can facilitate colonization and exploitation of a novel host in the polyphagous T. urticae, by affecting dispersal behavior (host acceptance) and female fecundity.     

Combining experimental evolution and field population assays to study the evolution of host range breadth

Adapting to specific hosts often involves trade‐offs that limit performance on other hosts. These constraints may either lead to narrow host ranges (i.e. specialists, able to exploit only one host type) or wide host ranges often leading to lower performance on each host (i.e. generalists). Here, we combined laboratory experiments on field populations with experimental evolution to investigate the impact of adaptation to the host on host range evolution and associated performance over this range. We used the two‐spotted spider mite, Tetranychus urticae, a model organism for studies on the evolution of specialization. Field mite populations were sampled on three host plant species: tomato, citrus tree and rosebay (Nerium oleander). Testing these populations in the laboratory revealed that tomato populations of mites could exploit tomato only, citrus populations could exploit citrus and tomato whereas Nerium populations could exploit all three hosts. Besides, the wider niche ranges of citrus and Nerium populations came at the cost of low performance on their non‐native hosts. Experimental lines selected to live on the same three host species exhibited similar patterns of host range and relative performance. This result suggests that adaptation to a new host species may lead to wider host ranges but at the expense of decreased performance on other hosts. We conclude that experimental evolution may reliably inform on evolution in the field.     

Interspecific competition counteracts negative effects of dispersal on adaptation of an arthropod herbivore to a new host

Dispersal and competition have both been suggested to drive variation in adaptability to a new environment, either positively or negatively. A simultaneous experimental test of both mechanisms is however lacking. Here, we experimentally investigate how population dynamics and local adaptation to a new host plant in a model species, the two‐spotted spider mite (Tetranychus urticae), are affected by dispersal from a stock population (no‐adapted) and competition with an already adapted spider mite species (Tetranychus evansi). For the population dynamics, we find that competition generally reduces population size and increases the risk of population extinction. However, these negative effects are counteracted by dispersal. For local adaptation, the roles of competition and dispersal are reversed. Without competition, dispersal exerts a negative effect on adaptation (measured as fecundity) to a novel host and females receiving the highest number of immigrants performed similarly to the stock population females. By contrast, with competition, adding more immigrants did not result in a lower fecundity. Females from populations with competition receiving the highest number of immigrants had a significantly higher fecundity than females from populations without competition (same dispersal treatment) and than the stock population females. We suggest that by exerting a stronger selection on the adapting populations, competition can counteract the migration load effect of dispersal. Interestingly, adaptation to the new host does not significantly reduce performance on the ancestral host, regardless of dispersal rate or competition. Our results highlight that assessments of how species can adapt to changing conditions need to jointly consider connectivity and the community context.     

Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway

The octadecanoid signaling pathway has been shown to play an important role in plant defense against various chewing insects and some pathogenic fungi. Here, we examined the interaction of a cell-content feeding arachnid herbivore, the two-spotted spider mite (Tetranychus urticae Koch), with cultivated tomato (Lycopersicon esculentum) and an isogenic mutant line (defenseless-1 [def-1]) that is deficient in the biosynthesis of the octadecanoid pathway-derived signal, jasmonic acid (JA). Spider mite feeding and fecundity on def-1 plants was significantly greater than on wild-type plants. Decreased resistance of def-1 plants was correlated with reduced JA accumulation and expression of defensive proteinase inhibitor (PI) genes, which were induced in mite-damaged wild-type leaves. Treatment of def-1 plants with methyl-JA restored resistance to spider mite feeding and reduced the fecundity of female mites. Plants expressing a 35S::prosystemin transgene that constitutively activates the octadecanoid pathway in a Def-1-dependent manner were highly resistant to attack by spider mites and western flower thrips (Frankliniella occidentalis), another cell-content feeder of economic importance. These findings indicate that activation of the octadecanoid signaling pathway promotes resistance of tomato to a broad spectrum of herbivores. The techniques of amplified fragment length polymorphism (AFLP) and bulk segregant analysis were used to map the Def-1 gene to a region on the long arm of chromosome 3 that is genetically separable from the map position of known JA biosynthetic genes. Tight linkage of Def-1 to a T-DNA insertion harboring the maize (Zea mays) Dissociation transposable element suggests a strategy for directed transposon tagging of the gene.     

Assessment of herbivore performance on host plants

Two models for assessing the performance of herbivores on a variety of host plants are developed by combining knowledge of population genetics and population ecology, especially that of the fixation probability of mutant genes. The absolute host performance model precisely assesses host performance for one herbivore population based on parameters of fecundity, larval survivorship, and selection pressure. The relative host performance model compares host performance for one population among different host plant species and for several populations on the same host species. Two herbivore populations, Bemisia tabaci (Gennadius) and Tetranychus truncates Ehara, were used to validate the absolute and relative host performance models. Results indicated that the assessment systems of host performance were reasonable and reliable. These models could be applied to a wide range of herbivore species for assessing their performance on host plants.     

Predators induce interspecific herbivore competition for food in refuge space

Resource competition among herbivorous arthropods has long been viewed as unimportant because herbivore populations are controlled by predators. Although recently resurrected as an organizing force in arthropod communities on plants, there is still general agreement that resource competition among herbivores is reduced by predators. Here we show the reverse: predators induce interspecific resource competi-tion among herbivores. We found that thrips larvae ( Frankliniella occidentalis ) use the web produced and inhabited by the spider mite Tetranychus urticae as a refuge from predation by the phytoseiid mite Neoseiulus cucumeris . Thrips larvae prefer clean plant parts, but move into the web upon perceiving volatile cues associated with thrips and predators. This behaviour leads to lower predation risk, but also to reduced developmental rate and lower production of thrips larvae due to competition with spider mites. In addition, thrips larvae consume spider-mite eggs. Thus, predators induce interspecific competition and intraguild predation among herbivores within refuge space, even when host plants have an overall green appearance.     

Density dependent population growth of the two-spotted spider mite, Tetranychus urticae, on the host plant Leonurus cardiaca

We observed Tetranychus urticae (Koch), a polyphagous spider mite herbivore, on Leonurus cardiaca (L.) at several sites in eastern North America at variable density, ranging from extremely dense to sparse. To understand the nature of T. urticae 's population dynamics we experimentally manipulated population densities on L. cardiaca and assessed per capita growth after 1 to 2 generations in laboratory and field experiments. In particular, we took a 'bottom-up' approach, manipulating both plant size and quality to examine effects on mite dynamics. Per capita growth was strongly dependent on the initial density of the mite population. Spider mite populations grew (1) in a negatively density dependent manner on small plants and (2) unhindered by density dependence on large plants. Mean per capita growth was 59% higher on small plants compared to large plants, irrespective of mite density. We also found evidence for density dependent induced susceptibility to spider mites in small plants and density dependent induced resistance in large plants. Hence, spider mite populations grew at a relatively fast rate on small plants, and this was associated with negative density dependence due to factors that depress population growth, such as food deterioration or limitation. On large plants, spider mite populations grew at a relatively slow rate, apparently resulting in herbivore densities that may not have been high enough to cause intraspecific competition or other forms of negative density dependence.     

Interactions between white mealybugs and red spider mites sequentially colonizing coffee plants

Plants under herbivore attack often respond defensively by mounting chemical and physical defences. However, some herbivores can manipulate plant defences to their own benefit by suppressing the expression of induced defences. These herbivore‐induced changes specific to the attacking herbivore can either facilitate or impede the colonization and establishment of a second herbivore. Although recent studies have focused on the effect of multiple herbivory on plant induced response and the third trophic level, few have examined the ecological relevance of multiple herbivores sharing the host. Here, we investigated whether herbivory by the white mealybug Planococcus minor (Maskell) (Hemiptera: Pseudococcidae) or the red spider mite Olygonychus ilicis (McGregor) (Acari: Tetranychidae), two herbivores that peak in coffee plantations during the dry season, may facilitate the colonization and establishment of the other species in coffee plants. Dual‐choice arena tests showed that white mealybugs preferred mite‐infested over uninfested coffee plants as hosts. Fifteen days after the release of 50 first‐instar P. minor nymphs, greater numbers of nymphs and adults were found on mite‐infested than uninfested plants, indicating superior performance on mite‐infested plants. On the other hand, female red spider mites did not show clear preference between uninfested and mealybug‐infested plants and deposited similar numbers of eggs on both treatments. In a no‐choice test, red spider mites performed poorly on mealybug‐infested plants with a smaller number of eggs, nymphs, females and males found in mealybug‐infested plants relative to uninfested plants. Thus, our results indicate that coffee plants are more likely to be infested by the red spider mite before white mealybug, rather than the inverse sequence (i.e. mealybug infestation followed by red spider mites). Our findings are discussed in the context of plant manipulation reported for pseudococcid mealybugs and spider mites.     

Host plant resistance among tomato accessions to the spider mite <Emphasis Type="Italic">Tetranychus evansi</Emphasis> in Kenya

The spider mite Tetranychus evansi has a broad range of host plants. Control of T. evansi has been a big challenge to tomato farmers due to its fast rate of reproduction, development of resistance to chemical pesticides and its ability to use weeds as alternative hosts when the tomato plants are not available. The aim of the current study was to determine the host plant acceptance and the relative contributions of trichomes in the control of the red spider mite by comparing the survival, development and oviposition rates of the red spider mite on eight tomato accessions. Leaflets from eight tomato varieties were assayed with the spider mites to determine the egg laying capacity and developmental time of the spider mites on the tomato accessions as well as the trichome densities. Densities of trichome types I, IV, V and VI varied among the tomato accessions. Variation in types I, IV and VI accounted for most of the variation in mite responses. The varieties with high densities of types IV and VI had the highest fecundity and mite development did not go beyond the larval stage. The developmental time varied significantly among the tomato accessions. The results indicated that the higher the density of trichome type I the lower the adult survival. The findings indicated possible resistance of some of the tested tomato accessions against T. evansi which is partially associated with trichomes types and density.     

Induction of preference and performance after acclimation to novel hosts in a phytophagous spider mite: adaptive plasticity?

We examined induction of preference and performance on novel host plants for two laboratory populations of the polyphagous spider mite Tetranychus urticae, with one population adapted to bean and the other population adapted to tomato. We bred four isofemale lines of the bean population only and used them in all the assays. The bean population had a 30% lower fecundity on tomato than on bean, while the tomato population had equal fecundity on both host plants. Acclimation of adult females to the novel host plant for both populations increased acceptability of that novel host but did not increase rejection of the original host. The bean population experienced a 60% benefit and a 30% cost in terms of egg production for acclimating to tomato, thus exemplifying adaptive plasticity. The tomato population showed a 23% benefit for acclimating to bean but no cost. Mites from the bean population that were acclimated to tomato fed more on tomato than did mites that were not acclimated to tomato. When these mites were fed inhibitors of cytochrome P-450 detoxification enzymes, their performance was severely depressed (84%) on tomato but not on bean. However, mites that were fed inhibitors of P-450 enzymes did not reduce their acceptance of tomato as a host. Thus, performance on novel hosts (but not preference) in this species is likely correlated with the induction of detoxifying enzymes. Spider mites are known to form host races rapidly on novel hosts. Induction of preference and physiological acclimation via detoxification enzymes may enhance performance and, thus, strongly contribute to initial stages of host race formation.     

Rapid specialization of counter defenses enables two-spotted spider mite to adapt to novel plant hosts

Genetic adaptation, occurring over a long evolutionary time, enables host-specialized herbivores to develop novel resistance traits and to efficiently counteract the defenses of a narrow range of host plants. In contrast, physiological acclimation, leading to the suppression and/or detoxification of host defenses, is hypothesized to enable broad generalists to shift between plant hosts. However, the host adaptation mechanisms used by generalists composed of host-adapted populations are not known. Two-spotted spider mite (TSSM; Tetranychus urticae) is an extreme generalist herbivore whose individual populations perform well only on a subset of potential hosts. We combined experimental evolution, Arabidopsis thaliana genetics, mite reverse genetics, and pharmacological approaches to examine mite host adaptation upon the shift of a bean (Phaseolus vulgaris)-adapted population to Arabidopsis. We showed that cytochrome P450 monooxygenases are required for mite adaptation to Arabidopsis. We identified activities of two tiers of P450s: general xenobiotic-responsive P450s that have a limited contribution to mite adaptation to Arabidopsis and adaptation-associated P450s that efficiently counteract Arabidopsis defenses. In approximately 25 generations of mite selection on Arabidopsis plants, mites evolved highly efficient detoxification-based adaptation, characteristic of specialist herbivores. This demonstrates that specialization to plant resistance traits can occur within the ecological timescale, enabling the TSSM to shift to novel plant hosts.

Mites can evolve highly efficient detoxification-based adaptation in approximately 25 generations on an initially unfavorable plant host, revealing that specialization can occur within the ecological timescale.     

Adaptation in a spider mite population after long-term evolution on a single host plant

Evolution in a single environment is expected to erode genetic variability, thereby precluding adaptation to novel environments. To test this, a large population of spider mites kept on cucumber for approximately 300 generations was used to establish populations on novel host plants (tomato or pepper), and changes in traits associated to adaptation were measured after 15 generations. Using a half-sib design, we investigated whether trait changes were related to genetic variation in the base population. Juvenile survival and fecundity exhibited genetic variation and increased in experimental populations on novel hosts. Conversely, no variation was detected for host choice and developmental time and these traits did not evolve. Longevity remained unchanged on novel hosts despite the presence of genetic variation, suggesting weak selection for this trait. Hence, patterns of evolutionary changes generally matched those of genetic variation, and changes in some traits were not hindered by long-term evolution in a constant environment.     

Host race formation inTetranychus urticae: genetic differentiation, host plant preference, and mate choice in a tomato and a cucumber strain

The two-spotted spider mite,Tetranychus urticae Koch, occurs in two colour forms in greenhouses in the Netherlands: a red form on tomato and a green form on cucumber. The evolutionary status of these strains was analysed by studying genetic differentiation, host plant preference, and mate choice. Males of the tomato strain preferred the female (30 h-old) teleiochrysales from the same strain to those of the cucumber strain, independent of the host plants (tomato, cucumber, bean) on which the teleiochrysales were placed. In contrast, males of the cucumber strain were not selective. In a Y-tube olfactometer, females of the cucumber strain were not responsive to host plant volatiles alone. However, in two-choice disc experiments, where females were exposed to both volatile and contact cues, they settled on cucumber leaves in preference to tomato leaves. Females of the tomato strain preferred the odour of tomato leaves and settled on tomato leaves in preference to cucumber leaves. These experimental results provide the first evidence for (1) host-plant independent mate selection in male spider mites and (2) olfactory discrimination between host plants in female spider mites. Electrophoretic analysis showed much genetic differentiation at the phosphoglucose isomerase locus. The cucumber strain showed large variation with 5 alleles, whereas the tomato strain was fixed for the most common allele of the cucumber strain. The results suggest that the two strains represent host races. We hypothesize that the tomato strain has originated from the cucumber strain because (1) tomato represents a more hostile host plant to spider mites (due to toxic compounds and glandular hairs) and (2) the tomato strain is genetically impoverished suggesting that it passed through one or more bottlenecks.     

Interactions in a tritrophic acarine predator-prey metapopulation system III: effects of Tetranychus urticae (Acari: Tetranychidae) on host plant condition

Spider mites are serious pests on many economically important plant species, because they may reduce plant productivity and, at high mite densities, overexploit and even kill the host plants. We have conducted a series of greenhouse experiments to quantify the effects of two-spotted spider mites (Tetranychus urticae) on host plants (Phaseolusvulgaris). The average amount of chlorophyll per cm² leaf area was used as a measure of plant condition. It was shown that chlorophyll concentration decreases with plant age and intensity of spider mite feeding. Damage caused by spider mites was assessed visually, using the Leaf Damage Index (LDI) defined by, and a mathematical relationship between the visual measurements and the amount of chlorophyll/cm² was fitted to data. The relationship may serve as a short-cut to estimate overall plant injury, expressed as the relative loss of chlorophyll/cm² leaf area caused by spider mites (D). D takes values between 0 (no injury) and 1 (all leaves dead). A highly significant positive relationship between the instantaneous spider mite density and D was found, even though D is expected to reflect the cumulated density of mites (mite-days). A model of plant growth incorporating information about plant age and D predicts that plant area has a maximum when plant age is about 60 days, and that plant area decreases exponentially with an increase in D. This revised version was published online in July 2006 with corrections to the Cover Date.     

Evolutionary adaptation to host plants in a laboratory population of the phytophagous mite Tetranychus urticae Koch

Summary For evolutionary expansion of host range to occur in an herbivore population, genetic variation in ability to survive on and/or accept new hosts must be present. To determine whether a population of the phytophagous mite Tetranychus urticae contained such variation, I established lines from the population on two hosts on which mites initially showed both high juvenile mortality and low acceptance, tomato and broccoli. In less than ten generations, mites from the line kept on each host showed both lower mortality and greater acceptance on it than mites from a control line kept on lima bean, a favorable host for T. urticae. Host acceptance was measured by the proportion of mites attempting to disperse from leaves of the host. The line kept on tomato but not the one kept on broccoli also increased in development rate on its host. These results and those of a similar previous experiment on cucumber indicate that T. urticae populations can adapt to a diversity of initially unfavorable hosts. T. urticae populations therefore should be able to respond to temporal and spatial variation in host availability by adapting to the most abundant hosts.     

Tree hybridization and genotypic variation drive cryptic speciation of a specialist mite herbivore

Few studies have investigated the roles that plant hybridization and individual plant genotype play in promoting population divergence within arthropod species. Using nrDNA sequence information and reciprocal transfer experiments, we examined how tree cross type (i.e., pure Populus angustifolia and P. angustifolia x P. fremontii F(1) type hybrids) and individual tree genotype influence host race formation in the bud-galling mite Aceria parapopuli. Three main findings emerged: (1) Strong genetic differentiation of mite populations found on pure P. angustifolia and F(1) type hybrids indicates that these mites represent morphologically cryptic species. (2) Within the F(1) type hybrids, population genetic analyses indicate migration among individual trees; however, (3) transfer experiments show that the mites found on heavily infested F(1) type trees perform best on their natal host genotype, suggesting that genetic interactions between mites and their host trees drive population structure, local adaptation, and host race formation. These findings argue that hybridization and genotypic differences in foundation tree species may drive herbivore population structure, and have evolutionary consequences for dependent arthropod species.     

Adaptive learning in arthropods: spider mites learn to distinguish food quality

Many herbivorous arthropods have been shown to possess learning capabilities, yet fitness effects of learning are largely unknown. In this paper, we test whether two-spotted spider mites (Tetranychus urticae) learn to distinguish food quality in choice tests, and whether this results in fitness benefits. Food consisted of cucumber plants with one of three degrees of feeding damage: undamaged (no mites), mildly damaged (infested by a mite strain adapted to tomato) and heavily damaged (infested by a mite strain adapted to cucumber). Mites were subjected to one choice test in a greenhouse and three sequential choice tests on leaf disks. Thereafter, individual mite performance was measured as oviposition rate over four days. In the course of the three small-scale choice tests, preference shifted towards less damaged food. The performance tests showed that learning was adaptive: mites learned to prefer the food type that yielded the higher oviposition rate. Interestingly, innate preferences in the greenhouse tests were close to those shown after learning in the small-scale tests. Given that both strains of mites had not experienced cucumber for several years, we hypothesize that the preference in the greenhouse was due to avoidance of mite odours rather than odours of damaged plants. Through its effect on foraging behaviour, adaptive learning may promote the evolution of host plant specialization in herbivorous arthropods.     

Attraction of the specialist parasitoid Cotesia rubecula to Arabidopsis thaliana infested by host or non-host herbivore species

In this study we investigated whether in a two‐choice set‐up the parasitoid Cotesia rubecula (Marshall) (Hymenoptera, Braconidae) distinguishes between volatiles emitted by Arabidopsis thaliana (L.) Heynh. (Brassicaceae) infested with its host, Pieris rapae (L.) (Lepidoptera: Pieridae) and Arabidopsis infested with non‐host herbivores. Four non‐host herbivore species were tested: the caterpillars Plutella xylostella (L.) (Lepidoptera: Plutellidae) and Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae), both chewing insects, the spider mite Tetranychus urticae (Koch) (Acari: Tetranychidae), which punctures parenchymal cells, and the aphid Myzus persicae (Sulzer) (Hemiptera: Aphidoidea), which is a phloem‐feeder. Compared with undamaged plants, C. rubecula females were more attracted to Arabidopsis plants infested by P. rapae, P. xylostella, S. exigua, or T. urticae, but not to plants infested by M. persicae. The parasitoids preferred host‐infested plants to spider mite‐ or aphid‐infested plants, but not to plants infested with non‐host caterpillars (P. xylostella or S. exigua). The data show that when Arabidopsis plants are infested with a leaf tissue‐damaging herbivore they emit a volatile blend that attracts C. rubecula females and the wasps only discriminate between a host and non‐host herbivore when the type of damage is different (chewing vs. piercing). When Arabidopsis is infested with a herbivore that hardly damages leaf tissue, C. rubecula females are not attracted. These results may be explained by differences in the amount of damage and in the relative importance of different signal‐transduction pathways induced by different types of herbivores.