Differential expression and activity of catechol-O-methyl transferase (COMT) in a generalist (Neotoma albigula) and juniper specialist (Neotoma stephensi) woodrat

Mammalian herbivores, particularly dietary specialists must have an efficient means to metabolize the high doses of plant secondary compounds they consume. We found previously that Neotoma stephensi, a juniper specialist, upregulated catechol-O-methyl transferase (COMT) mRNA almost seven fold in response to an ecologically relevant diet (70% juniper). To further investigate the relevance of this enzyme with respect to juniper metabolism, we compared the protein expression, activity and kinetics of the two forms of COMT, soluble (S-COMT) and membrane bound (MB-COMT), in the blood, kidneys and liver of N. stephensi on its natural juniper diet to that of N. stephensi fed an experimental diet of 70% juniper as well as a non-toxic control diet under laboratory conditions. In addition, we compared these results to that of Neotoma albigula, a generalist species, which consumes a diet of 25% juniper in the wild. The specialist consuming juniper under both field and laboratory conditions had increased S-COMT expression and activity in their livers and kidneys, and increased S-COMT activity in their blood compared to the specialist and generalist fed the control diet. The specialist showed expression and activity of S-COMT in their kidneys that was as high as or higher than that in their livers. The generalist had an elevated V_max for MB-COMT compared to the specialist that resulted in higher activity for MB-COMT than the specialist despite lower expression of MB-COMT in the generalist's livers and kidneys. This high activity MB-COMT may be in part responsible for differences in the behaviors of the generalist compared to the specialist. We conclude that S-COMT is important in the specialist's ability to consume high levels of juniper.     

Diet breadth of mammalian herbivores: nutrient versus detoxification constraints

Two hypotheses, nutrient constraints and detoxification limitation, have been proposed to explain the lack of specialists among mammalian herbivores. The nutrient constraint hypothesis proposes that dietary specialization in mammalian herbivores is rare because no one plant can provide all requisite nutrients. The detoxification limitation hypothesis suggests that the mammalian detoxification system is incapable of detoxifying high doses of similar secondary compounds present in a diet of a single plant species. We experimentally tested these hypotheses by comparing the performance of specialist and generalist woodrats (Neotoma) on a variety of dietary challenges. Neotoma stephensi is a narrow dietary specialist with a single species, one-seeded juniper, Juniperus monosperma, comprising 85–95% of its diet. Compared with other plants available in the habitat, juniper is low in nitrogen and high in fiber, phenolics, and monoterpenes. The generalist woodrat, N. albigula, also consumes one-seeded juniper, but to a lesser degree. The nutrient constraint hypothesis was examined by feeding both species of woodrats a low-nitrogen, high-fiber diet similar to that found in juniper. We found no differences in body mass change, or apparent digestibility of dry matter or nitrogen between the two species of woodrats after 35 days on this diet. Moreover, both species were in positive nitrogen balance. We tested the detoxification limitation hypothesis by comparing the performance of the generalist and specialist on diets with and without juniper leaves, the preferred foliage of the specialist, as well as on diets with and without α-pinene, the predominant monoterpene in juniper. We found that on the juniper diet, compared with the specialist, the generalist consumed less juniper and lost more mass. Urine pH, a general indicator of overall detoxification processes, declined in both groups on the juniper diet. The generalist consumed half the toxin load of the specialist yet its urine pH was slightly lower. Moreover, the generalist consumed significantly less of the treatment with high concentrations of α-pinene compared to the control treatment, while the specialist consumed the same amount of food regardless of α-pinene concentration. For both groups, urine pH declined as levels of α-pinene in the diet increased. The generalist produced a significantly more acidic urine than the specialist on the treatment with the highest α-pinene concentration. Our results suggest that in this system, specialists detoxify plant secondary compounds differently than generalists and plant secondary compounds may be more important than low nutrient levels in maintaining dietary diversity in generalist herbivores. Received: 5 May 1999 / Accepted: 14 November 1999     

A specialist herbivore (Neotoma stephensi) absorbs fewer plant toxins than does a generalist (Neotoma albigula)

Detoxification capacity of enzymes in the liver is thought to be the primary factor governing dietary toxin intake by mammalian herbivores. Recently, toxin absorption in the gut was proposed as an alternative process that also influences toxin intake. We examined the role of the gut in regulating toxin absorption by quantifying excretion of a plant secondary compound in the feces. We hypothesized that specialists have a greater capacity to reduce intestinal absorption of toxins than do generalists. To test this hypothesis, we compared fecal excretion of alpha-pinene in specialist (Neotoma stephensi) and generalist (Neotoma albigula) woodrats. Alpha-pinene is the most abundant monoterpene in Juniperus monosperma, which occurs in the natural diet of both woodrat species. Woodrats were fed alpha-pinene in diets containing juniper foliage for 3 wk and, in a separate experiment, were given a single oral dose of alpha-pinene. Feces were collected from animals at the end of each experiment and analyzed for alpha-pinene concentration using gas chromatography. Both woodrat species excreted unchanged alpha-pinene in the feces. However, specialist woodrats excreted 40% more alpha-pinene per unit ingested from a juniper diet and excreted nearly four times a greater percentage of an oral dose of alpha-pinene compared with generalists.     

Xenobiotic metabolism of plant secondary compounds in juniper (Juniperus monosperma) by specialist and generalist woodrat herbivores, genus Neotoma

Mammalian herbivores routinely consume diets laden with often-toxic xenobiotics, yet the manner in which mammalian herbivores detoxify these plant secondary compounds (PSC) is largely unknown. Theory predicts that specialists rely more heavily on functionalization pathways whereas generalists rely on conjugation pathways to metabolize PSC in their diet. We took a pharmacological approach to determine how a specialist (Neotoma stephensi) of juniper foliage (Juniperus monosperma) and a generalist (N. albigula) may process the same dietary PSC. We investigated the xenobiotic metabolizing enzymes of the specialist and generalist on a control diet and a low (25%) juniper diet. We also examined enzyme activities in the specialist on a high (70%) juniper diet. We assayed for cytochrome P450 concentration and biotransformation activities of three specific cytochrome P450 isozymes (CYP1A, CYP2B, CYP3A), NAD(P)H:quinone oxidoreductase, glutathione conjugation, sulfation and glucuronidation. Results provide partial evidence for the hypothesis in that the specialist and generalist consuming juniper at a level similar to their natural diet, differ in the level of conjugation enzyme activity with generalists having higher activity overall than specialists.     

Detoxification rates of wild herbivorous woodrats (Neotoma)

The detoxification systems of mammalian herbivores are thought to have evolved in response to the ingestion of plant secondary compounds. Specialist herbivores consume high quantities of secondary compounds and are predicted to have faster rates of Phase 1 detoxification compared to generalist herbivores. We tested this hypothesis by comparing the performances of a specialist (Neotoma fuscipes) and generalist (Neotoma lepida) herbivore using hypnotic state assays. Herbivores foraging in nature were live trapped and injected with hexobarbital (100 mg/kg). We measured the length of time in the hypnotic state as the time in which the animal was unable to right itself twice in 30 s. The specialist metabolized hexobarbital 1.7 times faster than the generalist (F(1, 19) = 9.31, P = 0.007) as revealed by its significantly shorter time spent in the hypnotic state (56+/-9 min vs. 87+/-8 min, respectively). The results are consistent with the hypothesis that specialists have faster rates of Phase 1 detoxification. This is the first evaluation of the detoxification capability of mammalian herbivores foraging under natural conditions. Hypnotic state assays have broad potential applications to the study of vertebrate-plant interactions.     

Strategies in herbivory by mammals revisited: The role of liver metabolism in a juniper specialist (Neotoma stephensi) and a generalist (Neotoma albigula)

Although herbivory is widespread among mammals, few species have adopted a strategy of dietary specialization. Feeding on a single plant species often exposes herbivores to high doses of plant secondary metabolites (PSMs), which may exceed the animal's detoxification capacities. Theory predicts that specialists will have unique detoxification mechanisms to process high levels of dietary toxins. To evaluate this hypothesis, we compared liver microsomal metabolism of a juniper specialist, Neotoma stephensi (diet >85% juniper), to a generalist, N. albigula (diet ≤30% juniper). Specifically, we quantified the concentration of a key detoxification enzyme, cytochrome P450 2B (CYP2B) in liver microsomes, and the metabolism of α‐pinene, the most abundant terpene in the juniper species consumed by the specialist woodrat. In both species, a 30% juniper diet increased the total CYP2B concentration (2–3×) in microsomes and microsomal α‐pinene metabolism rates (4‐fold). In N. stephensi, higher levels of dietary juniper (60% and 100%) further induced CYP2B and increased metabolism rates of α‐pinene. Although no species‐specific differences in metabolism rates were observed at 30% dietary juniper, total microsomal CYP2B concentration was 1.7× higher in N. stephensi than in N. albigula (p < .01), suggesting N. stephensi produces one or more variant of CYP2B that is less efficient at processing α‐pinene. In N. stephensi, the rates of α‐pinene metabolism increased with dietary juniper and were positively correlated with CYP2B concentration. The ability of N. stephensi to elevate CYP2B concentration and rate of α‐pinene metabolism with increasing levels of juniper in the diet may facilitate juniper specialization in this species.     

Role of cytochrome P450 2B sequence variation and gene copy number in facilitating dietary specialization in mammalian herbivores

Theory postulates that dietary specialization in mammalian herbivores is enabled by a specialized set of liver enzymes that process the high concentrations of similar plant secondary metabolites (PSMs) in the diets of specialists. To investigate whether qualitative and quantitative differences in detoxification mechanisms distinguish dietary specialists from generalists, we compared the sequence diversity and gene copy number of detoxification enzymes in two woodrat species: a generalist, the white‐throated woodrat (Neotoma albigula) and a juniper specialist, Stephens’ woodrat (N. stephensi). We focused on enzymes in the cytochrome P450 subfamily 2B (CYP2B), because previous research suggests this subfamily plays a key role in the processing of PSMs. For both woodrat species, we obtained and sequenced CYP2B cDNA, generated CYP2B phylogenies, estimated CYP2B gene copy number and created a homology model of the active site. We found that the specialist possessed on average ~5 more CYP2B gene copies than the generalist, but the specialist's CYP2B sequences were less diverse. Phylogenetic analysis of putative CYP2B homologs resolved woodrat species as reciprocally monophyletic and suggested evolutionary convergence of distinct homologs on similar key amino acid residues in both species. Homology modelling of the CYP2B enzyme suggests that interspecific differences in substrate preference and function likely result from amino acid differences in the enzyme active site. The characteristics of CYP2B in the specialist, that is greater gene copy number coupled with less sequence variation, are consistent with specialization to a narrow range of dietary toxins.     

Testing the diet-breadth trade-off hypothesis: differential regulation of novel plant secondary compounds by a specialist and a generalist herbivore

Specialist herbivores are predicted to have evolved biotransformation pathways that can process large doses of secondary compounds from the plant species on which they specialize. It is hypothesized that this physiological specialization results in a trade-off such that specialists may be limited in ability to ingest novel plant secondary compounds (PSCs). In contrast, the generalist foraging strategy requires that herbivores alternate consumption of plant species and PSC types to reduce the possibility of over-ingestion of any particular PSC. The ability to behaviorally regulate is a key component of this strategy. These ideas underpin the prediction that in the face of novel PSCs, generalists should be better able to maintain body mass and avoid toxic consequences compared to specialists. We explored these predictions by comparing the feeding behavior of two herbivorous rodents: a juniper specialist, Neotoma stephensi, and a generalist, Neotoma albigula, fed diets with increasing concentrations of phenolic resin extracted from the creosote bush (Larrea tridentata), which produces a suite of PSCs novel to both species. The specialist lost more mass than the generalist during the 15-day trial. In addition, although the specialist and generalist both regulated phenolic resin intake by reducing meal size while on the highest resin concentration (4%), the generalist began to regulate intake on the 2% diet. The ability of the generalist to regulate intake at a lower PSC concentration may be the source of the generalist’s performance advantage over the specialist. These data provide evidence for the hypothesis that the specialist’s foraging strategy may result in behavioral as well as physiological trade-offs in the ability to consume novel PSCs.     

Liver biotransforming enzymes in woodrats Neotoma stephensi (Muridae)

Mammalian herbivores are exposed to extremely high levels of plant secondary compounds naturally present in their diet. It has been speculated that specialist herbivores should express a unique pattern of biotransforming enzymes to permit the consumption of a single species of toxic plant. Specifically, specialists should rely on pathways that effectively biotransform the toxins they routinely encounter in their diet. We examined the hepatic mRNA expression and activity or content of biotransforming enzymes in the specialist herbivorous woodrat, Neotoma stephensi, and compared results to those of laboratory rats (Sprague-Dawley strain Rattus norvegicus). In addition, we investigated the role of alpha-pinene, a specific plant toxin present in the diet of N. stephensi on the mRNA expression pattern and activity or content of biotransforming enzymes in Sprague-Dawley rats. Overall, the levels of functionalization enzyme activity and mRNA were found to be higher in specialists, while glucuronidation enzyme activity and mRNA were lower. These results support predictions that specialist herbivores rely more on functionalization biotransformation pathways rather than glucuronidation pathways.     

Evidence for local specialization in a generalist mammalian herbivore, Neotoma fuscipes

Herbivores with very plastic dietary requirements, or so-called generalist species, can include individuals that develop specialized feeding habits through their experience with local chemically-defended plants. Local specialization has important implications for understanding a variety of ecological and evolutionary dynamics. However, the extent to which individuals within a generalist species specialize on local plants and the consequences of such specialization remain poorly understood, especially in non-insect herbivores. To better understand this phenomenon, we determined the diet and food preferences of a generalist mammalian herbivore, the dusky-footed woodrat ( Neotoma fuscipes ), in two adjacent but distinct plant communities. Based on a combination of cafeteria trials and stable isotope analyses (δ¹³C and δ¹⁵N), our results indicate that woodrats display preferences for local plants and tend to avoid novel chemically-defended plants. Moreover, both methodologies support the conclusion that individual woodrats are dietary specialists restricting their diets to only a few (2-3) of the available plant species. In juniper woodland, woodrats prefer western juniper ( Juniperus occidentalis ), while less than one km away in mixed-coniferous forest, woodrats prefer incense cedar ( Calocedrus decurrens ). Both plants contain high levels of plant secondary compounds that require detoxification mechanisms within consumers. Therefore, preferences are likely indicative of underlying physiological adaptations that could promote further behavioral, physiological and ultimately genetic differences between woodrats in different habitats. This study provides additional evidence for local specialization and urges caution when using the term generalist to characterize feeding behaviors at the individual level.     

Elimination of plant toxins by herbivorous woodrats: revisiting an explanation for dietary specialization in mammalian herbivores

Constraints on rates of detoxification and elimination of plant toxins are thought to be responsible for limiting dietary specialization in mammalian herbivores. This hypothesis, known as the detoxification limitations hypothesis, suggests that most mammalian herbivores are generalists to avoid overdosing on toxins from a single plant species. The hypothesis also predicts that the few mammalian specialists that exist should have adaptations for rapid detoxification and elimination of plant secondary compounds. We took a pharmacological approach to test whether specialists eliminate toxins from the bloodstream faster than generalists. We compared elimination rate and total exposure of alpha-pinene in closely related dietary specialist and generalist woodrats, Neotoma stephensi and N. albigula, respectively. Animals were orally gavaged with alpha-pinene, a plant secondary compound present in the natural diets of both woodrat species. We collected venous blood at 3, 6, 10, 15, and 20 min post-ingestion of alpha-pinene. Blood was analyzed for alpha-pinene concentration using gas chromatography. We found that specialist and generalist woodrats did not differ in elimination rates of alpha-pinene. However, specialists had lower exposure levels of alpha-pinene than generalists due to lower initial delivery of alpha-pinene to the general circulation. The levels of alpha-pinene detected in the bloodstream of specialists were 4.7-5.3x lower over all time intervals than generalists. Thus, specialists encounter a functionally lower dose of toxin than generalists. We suggest that the lower exposure level of specialist woodrats may be due to mechanisms in the gut that decrease toxin absorption. Regardless of mechanism, lower exposure to plant toxins may allow specialists to forage on diets with high toxin concentrations thereby facilitating dietary specialization.     

An oak (Quercus agrifolia) specialist (Neotoma macrotis) and a sympatric generalist (Neotoma lepida) show similar intakes and digestibilities of oak

Dietary specialization is thought to be rare in mammalian herbivores as a result of either a limitation in their detoxification system to metabolize higher doses of plant secondary compounds or deficiencies in nutrients present in a diet composed of a single species of plant. Neotoma macrotis is an oak specialist, whereas Neotoma lepida is a dietary generalist when sympatric with N. macrotis. We hypothesized that N. macrotis would have a higher tolerance for and digestibility of oak. We determined the two species' tolerances for oak by feeding them increasing concentrations of ground oak leaves until they could no longer maintain body mass. The highest concentration on which both species maintained body mass was 75% oak. There were no differences between the species in their abilities to digest dry matter, nitrogen, or fiber in the oak diets. The species' similar tolerances for oak were probably due to their similar abilities to digest and potentially assimilate the ground oak leaves.     

Woodrat (<Emphasis Type="Italic">Neotoma</Emphasis>) herbivores maintain nitrogen balance on a low-nitrogen,high-phenolic forage, <Emphasis Type="Italic">Juniperus monosperma</Emphasis>

The acquisition of adequate quantities of nitrogen is a challenge for herbivorous vertebrates because many plants are in low nitrogen and contain secondary metabolites that reduce nitrogen digestibility. To investigate whether herbivores maintain nitrogen balance on plant diets low in nitrogen and high in secondary compounds, we studied the effect of juniper (Juniperus monosperma) ingestion on the nitrogen balance of two species of herbivorous woodrats (Neotoma stephensi and N. albigula). These woodrat species feed on the foliage of juniper: N. stephensi is a juniper specialist, whereas N. albigula is a generalist that incorporates some juniper in its diet. Based on the nitrogen contents of the natural diets of these woodrats, we predicted that the generalist would be in negative nitrogen balance on a juniper diet whereas the specialist would not be affected. We found that both species of woodrat had low-nitrogen requirements (334.2 mg N/kg^0.75/day) and that a diet of 50% juniper did not result in negative nitrogen balance for either species. However, excretion patterns of nitrogen were altered; on the 50% juniper diet, fecal nitrogen losses increased ~38% and urinary nitrogen losses were half that of the control diet. The results suggest that absorption and detoxification of juniper secondary compounds may be more important for restricting juniper intake by the generalist than nitrogen imbalance.     

Expression of biotransformation genes in woodrat (Neotoma) herbivores on novel and ancestral diets: identification of candidate genes responsible for dietary shifts

The ability of herbivores to switch diets is thought to be governed by biotransformation enzymes. To identify potential biotransformation enzymes, we conducted a large-scale study on the expression of biotransformation enzymes in herbivorous woodrats ( Neotoma lepida ). We compared gene expression in a woodrat population from the Great Basin that feeds on the ancestral diet of juniper to one from the Mojave Desert that putatively switched from feeding on juniper to feeding on creosote. Juniper and creosote have notable differences in secondary chemistry, and thus, should require different biotransformation enzymes for detoxification. Individuals from each population were fed juniper and creosote diets separately. After the feeding trials, hepatic mRNA was extracted and hybridized to laboratory rat microarrays. Hybridization of woodrat samples to biotransformation probes on the array was 87%, resulting in a total of 224 biotransformation genes that met quality control standards. Overall, we found large differences in expression of biotransformation genes when woodrats were fed juniper vs. creosote. Mojave woodrats had greater expression of 10× as many biotransformation genes as did Great Basin woodrats on a creosote diet. We identified 24 candidate genes that may be critical in the biotransformation of creosote toxins. Superoxide dismutase, a free radical scavenger, was also expressed to a greater extent by the Mojave woodrats and may be important in controlling oxidative damage during biotransformation. The results are consistent with the hypothesis that biotransformation enzymes limit diet switching and that woodrats in the Mojave have evolved a unique strategy for the biotransformation of creosote toxins.     

Ingestion of juniper foliage reduces metabolic rates in woodrat (Neotoma) herbivores

Ingestion of plant secondary compounds by herbivores is predicted to increase resting or basal metabolic rates. We tested this hypothesis with two species of woodrat herbivores, Neotoma stephensi and Neotoma albigula, consuming diets of juniper (Juniperus monosperma), which is rich in plant secondary compounds. In nature, N. stephensi specializes on juniper, whereas N. albigula consumes a variety of plant species including juniper. We measured resting metabolic rates (RMR) of woodrats on control, 25% juniper and a treatment containing the maximum tolerable dose of juniper (50% juniper for N. albigula and 70% juniper for N. stephensi). Ingestion of a juniper diet resulted in decreased RMR in both species of woodrats. We propose several potential mechanisms for metabolic depression of Neotoma on juniper diets. Our novel results underscore the need for more studies utilizing plant-based diets to determine the general effect of plant secondary compounds on metabolic rates of herbivores.     

Intestinal capacity of P-glycoprotein is higher in the juniper specialist, Neotoma stephensi, than the sympatric generalist, Neotoma albigula

Permeability-glycoprotein (Pgp) is a membrane-bound, ATP-dependent, transport protein that excludes many cytotoxic compounds including plant metabolites and pollutants from the barrier epithelia of many tissues including the small intestine. We hypothesized that intestinal Pgp capacity would be higher in Neotoma stephensi, a specialist on Juniperus monosperma known to be high in plant toxins, than the sympatric generalist, Neotoma albigula, which consumes juniper in the field, but is unable to tolerate a high juniper diet. We measured Pgp activity as the difference in accumulation of a known Pgp substrate, digoxin, between everted sections of small intestine exposed to ethanol vehicle control and a maximal level of a known competitive inhibitor of Pgp, cyclosporin A. We estimated intestinal capacity by averaging Pgp activity along the intestine and multiplying by total small intestine mass. These first measures of Pgp in wild mammals show a significant difference among species with the juniper specialist, N. stephensi, exhibiting a 2.4 fold higher capacity than the generalist, N. albigula. This result suggests that Pgp may play a role in the ability of N. stephensi to tolerate juniper.     

Selection Mosaic Exerted by Specialist and Generalist Herbivores on Chemical and Physical Defense of Datura stramonium

Selection exerted by herbivores is a major force driving the evolution of plant defensive characters such as leaf trichomes or secondary metabolites. However, plant defense expression is highly variable among populations and identifying the sources of this variation remains a major challenge. Plant populations are often distributed across broad geographic ranges and are exposed to different herbivore communities, ranging from generalists (that feed on diverse plant species) to specialists (that feed on a restricted group of plants). We studied eight populations of the plant Datura stramonium usually eaten by specialist or generalist herbivores, in order to examine whether the pattern of phenotypic selection on secondary compounds (atropine and scopolamine) and a physical defense (trichome density) can explain geographic variation in these traits. Following co-evolutionary theory, we evaluated whether a more derived alkaloid (scopolamine) confers higher fitness benefits than its precursor (atropine), and whether this effect differs between specialist and generalist herbivores. Our results showed consistent directional selection in almost all populations and herbivores to reduce the concentration of atropine. The most derived alkaloid (scopolamine) was favored in only one of the populations, which is dominated by a generalist herbivore. In general, the patterns of selection support the existence of a selection mosaic and accounts for the positive correlation observed between atropine concentration and plant damage by herbivores recorded in previous studies.     

Response of pest control by generalist predators to local‐scale plant diversity: a meta‐analysis

Disentangling the effects of plant diversity on the control of herbivores is important for understanding agricultural sustainability. Recent studies have investigated the relationships between plant diversity and arthropod communities at the landscape scale, but few have done so at the local scale. We conducted a meta‐analysis of 32 papers containing 175 independent measures of the relationship between plant diversity and arthropod communities. We found that generalist predators had a strong positive response to plant diversity, that is, their abundance increased as plant diversity increased. Herbivores, in contrast, had an overall weak and negative response to plant diversity. However, specialist and generalist herbivores differed in their response to plant diversity, that is, the response was negative for specialists and not significant for generalists. While the effects of scale remain unclear, the response to plant diversity tended to increase for specialist herbivores, but decrease for generalist herbivores as the scale increased. There was no clear effect of scale on the response of generalist predators to plant diversity. Our results suggest that the response of herbivores to plant diversity at the local scale is a balance between habitat and trophic effects that vary according to arthropod specialization and habitat type. Synthesis and applications. Positive effects of plant diversity on generalist predators confirm that, at the local scale, plant diversification of agroecosystems is a credible and promising option for increasing pest regulation. Results from our meta‐analysis suggest that natural control in plant‐diversified systems is more likely to occur for specialist than for generalist herbivores. In terms of pest management, our results indicate that small‐scale plant diversification (via the planting of cover crops or intercrops and reduced weed management) is likely to increase the control of specialist herbivores by generalist predators.     

Increased resistance to generalist herbivores in invasive populations of the California poppy (Eschscholzia californica)

Escape from enemies in the native range is often assumed to contribute to the successful invasion of exotic species. Following optimal defence theory, which assumes a trade‐off between herbivore resistance and plant growth, some have predicted that the success of invasive species could be the result of the evolution of lower resistance to herbivores and increased allocation of resources to growth and reproduction. Lack of evidence for ubiquitous costs of producing plant toxins, and the recognition that invasive species may escape specialist, but not generalist enemies, has led to a new prediction: invasive species may escape ecological trade‐offs associated with specialist herbivores, and evolve increased, rather than decreased, production of defensive compounds that are effective at deterring generalist herbivores in the introduced range. We tested the performance of two generalist lepidopteran herbivores, Trichoplusia ni and Orgyia vetusta, when raised on diets of native and invasive populations of the California poppy, Eschscholzia californica. Pupae of T. ni were significantly larger when reared on native populations. Similarly, caterpillars of O. vetusta performed significantly better when raised on native populations, indicating that invasive populations of the California poppy are more resistant to herbivores than native populations. The chance of successful establishment of some non‐indigenous plant species may be increased by retaining resistance to generalist herbivores, and in some cases, invasive species may be able to escape ecological trade‐offs in their new range and evolve, as we observed, even greater resistance to generalist herbivores than native plants.