Specialized avian Haemosporida trade reduced host breadth for increased prevalence

Parasite specialization on one or a few host species leads to a reduction in the total number of available host individuals, which may decrease transmission. However, specialists are thought to be able to compensate by increased prevalence in the host population and increased success in each individual host. Here, we use variation in host breadth among a community of avian Haemosporida to investigate consequences of generalist and specialist strategies on prevalence across hosts. We show that specialist parasites are more prevalent than generalist parasites in host populations that are shared between them. Moreover, the total number of infections of generalist and specialist parasites within the study area did not vary significantly with host breadth. This suggests that specialists can infect a similar number of host individuals as generalists, thus compensating for a reduction in host availability by achieving higher prevalence in a single host species. Specialist parasites also tended to infect older hosts, whereas infections by generalists were biased towards younger hosts. We suggest that this reflects different abilities of generalists and specialists to persist in hosts following infection. Higher abundance and increased persistence in hosts suggest that specialists are more effective parasites than generalists, supporting the existence of a trade‐off between host breadth and average host use among these parasites.     

Landscape structure and agricultural intensification are weak predictors of host range and parasitism rate of cereal aphids

Proportions of specialist and generalist primary parasitoids have been described by the resource breadth and the trade-off hypothesis. These alternative hypotheses predict either decreased or increased, respectively, parasitism rate of shared aphid species by specialist parasitoids. We tested both hypotheses and the confounding effects of landscape structure and agricultural intensification (AI) using extensive samplings of aphids and their parasitoids in Polish agricultural landscapes. Abundances, species composition of aphids, primary parasitoids, and parasitism rate of aphids by specialists and generalist parasitoids were analysed. Contrary to our expectations we found equally decreased parasitism rates by both types of primary parasitoids at higher aphid densities and thus proportion of specialists to generalists did not change with increasing host density. In line with the resource breadth hypothesis, specialist parasitoids had always lower abundances and parasitism rates than generalist parasitoids. Landscape diversity and agricultural intensification did not influence the host-parasitoid population dynamics. We speculate that these contrasting results could be caused by the additional density effects of secondary parasitoids. We conclude that simplistic two-trophic-level population models are not able to fully describe the complex dynamics of trophic networks. We also argue that agricultural intensification has lower effects on abundance and effectiveness of parasitoids than predicted by respective predator–prey models and empirical studies performed in controlled and artificial conditions.     

Geography is more important than host plant use for the population genetic structure of a generalist insect herbivore

Population divergence can occur due to mechanisms associated with geographic isolation and/or due to selection associated with different ecological niches. Much of the evidence for selection‐driven speciation has come from studies of specialist insect herbivores that use different host plant species; however, the influence of host plant use on population divergence of generalist herbivores remains poorly understood. We tested how diet breadth, host plant species and geographic distance influence population divergence of the fall webworm (Hyphantria cunea; FW). FW is a broadly distributed, extreme generalist herbivore consisting of two morphotypes that have been argued to represent two different species: black‐headed and red‐headed. We characterized the differentiation of FW populations at two geographic scales. We first analysed the influence of host plant and geographic distance on genetic divergence across a broad continental scale for both colour types. We further analysed the influence of host plant, diet breadth and geographic distance on divergence at a finer geographic scale focusing on red‐headed FW in Colorado. We found clear genetic and morphological distinction between red‐ and black‐headed FW, and Colorado FW formed a genetic cluster distinct from other locations. Although both geographic distance and host plant use were correlated with genetic distance, geographic distance accounted for up to 3× more variation in genetic distance than did host plant use. As a rare study investigating the genetic structure of a widespread generalist herbivore over a broad geographic range (up to 3,000 km), our study supports a strong role for geographic isolation in divergence in this system.     

Specialists make faster decisions than generalists: experiments with aphids

Theoretical studies and a few recent experimental reports suggest that the evolution of diet breadth in herbivorous insects is constrained by a limited neural ability to efficiently process large amounts of information in short periods of time. This neural-constraints hypothesis predicts that generalist herbivores should make slower or poorer decisions than specialists when selecting plants, because generalists must discriminate and decide among stimuli from a wider variety of potential hosts. The present study compares the speed with which host-associated decisions are made in specialist versus generalist populations of the aphid Uroleucon ambrosiae. Populations of U. ambrosiae from eastern North America are highly specific to the host plant Ambrosia trifida (Asteraceae), whereas those from the American southwest also feed on a variety of other taxa from the Asteraceae. Experiments with winged (alate) and wingless (apterous) individuals showed that host-finding, host-selection, host-acceptance, host-sampling and host-settling were more efficiently performed by the eastern specialists. These very consistent results provide evidence that strongly supports the neural-constraints hypothesis.     

Specialist versus generalist life histories and nucleotide diversity in Caenorhabditis nematodes

Species with broad ecological amplitudes with respect to a key focal resource, niche generalists, should maintain larger and more connected populations than niche specialists, leading to the prediction that nucleotide diversity will be lower and more subdivided in specialists relative to their generalist relatives. This logic describes the specialist-generalist variation hypothesis (SGVH). Some outbreeding species of Caenorhabditis nematodes use a variety of invertebrate dispersal vectors and have high molecular diversity. By contrast, Caenorhabditis japonica lives in a strict association and synchronized life cycle with its dispersal host, the shield bug Parastrachia japonensis, itself a diet specialist. Here, we characterize sequence variation for 20 nuclear loci to investigate how C. japonica''s life history shapes nucleotide diversity. We find that C. japonica has more than threefold lower polymorphism than other outbreeding Caenorhabditis species, but that local populations are not genetically disconnected. Coupled with its restricted range, we propose that its specialist host association contributes to a smaller effective population size and lower genetic variation than host generalist Caenorhabditis species with outbreeding reproductive modes. A literature survey of diverse organisms provides broader support for the SGVH. These findings encourage further testing of ecological and evolutionary hypotheses with comparative population genetics in Caenorhabditis and other taxa.     

Do body size and diet breadth affect partitioning of species diversity? A test with forest Lepidoptera

Two of the major themes resulting from recent macroecological research are the central roles that body size and niche breadth may play as determinants of species geographical distribution. Unanswered questions, however, linger regarding how similarities in body size or niche breadth affect the allocation of α‐ and β‐diversity across spatial scales. Using data on moth diversity in the eastern deciduous forest of North America, we tested the predictions that smaller‐bodied and diet‐restricted species would have lower levels of α‐diversity within forest stands and greater β‐diversity at higher sampling scales compared to larger or more generalist species. Moths were sampled using a nested sampling design consisting of three hierarchical levels: 20 forest stands, 5 sites and 3 ecoregions. Body size for 492 species was estimated as mean forewing length, and diet breadth was assessed from the published literature. Moth species were then classified according to body size (small or large) or diet breadth (generalist or restricted), and partitioning was conducted on each group. Diversity partitions for large‐ and small‐bodied species yielded similar patterns. When observed diversity components differed from those derived from our null model, a consistent pattern was observed: α‐diversity was greater than expected, β‐diversity among forest stands was less than expected, and β‐diversity among sites and ecoregions was higher than expected. In contrast, diet‐restricted moths contributed significantly less to stand‐level α‐diversity than generalist feeders. Furthermore, specialists contributed to a greater proportion of β‐diversity across scales compared to generalist moths. Because absolute measures of β‐diversity among stands were greater for generalists than for restricted feeders, we suggest that regional β‐diversity of forest moths may be influenced by several possible factors: intraspecific aggregation of diet‐restricted species, local fluctuations in population size of eruptive generalists and small geographical distributions of generalist moths than predicted by the geographical extent of putative host plants     

Use of novel pollen species by specialist and generalist solitary bees (Hymenoptera: Megachilidae)

If trade-offs between flexibility to use a range of host species and efficiency on a limited set underlie the evolution of diet breadth, one resulting prediction is that specialists ought to be more restricted than generalists in their ability to use novel resource species. I used foraging tests and feeding trials to compare the ability of a generalist and a specialist solitary mason bee species to collect and develop on two pollen species that are not normally used in natural populations (novel pollens). Osmia lignaria (Hymenoptera: Megachilidae) is a generalist pollen feeder; O. californica, is more specialized. Adults of the specialist were more limited in use of novel hosts, but only in some contexts. Both bee species refused to collect one novel pollen. The specialist accepted a second novel pollen only when it was presented along with its normal pollen, whereas the generalist collected novel pollen whether presented alone or with normal pollen. Surprisingly, larvae of the specialist were more flexible than were generalists. The specialist grew well on mixtures of normal and novel pollen species, in some cases better than on its normal host alone. Larvae of the generalist grew more poorly on all diets containing novel pollens than on their normal host. Data on these two species of bees suggest that specialization by itself need not reduce flexibility on novel hosts. The findings also provide information about mechanisms of specialization in bees. Similar to some folivores, specific cues of the pollen host and the bee's interpretation of these contribute, along with foraging economics, to pollen choice by adults. The ability of the larvae to cope with specific components of one pollen species need not interfere with its ability to use others.     

Increased genetic differentiation in a specialist versus a generalist bee: implications for conservation

Oligolectic bees are specialists that collect pollen from one or a few closely related species of plants, while polylectic bees are generalists that collect pollen from both related and unrelated species of plants. Because of their more restricted range of floral hosts, it is expected that specialists persist in more isolated populations than do generalists. We present data on the population structure of two closely related bee species sampled from a super abundant floral host in the southern Atacama Desert. Pairwise comparisons of population subdivision over identical distances revealed that the specialist bee had significantly more differentiated populations in comparison to the generalist. Further, populations of the specialist had significantly less genetic variation, measured as observed and expected heterozgyosity, than those of the generalist. Our data support the hypothesis of decreased gene flow among populations of the specialist bee even at equivalent geographic distances. The resulting reductions in effective population size for specialists make them particularly prone to extinction due to both demographic and genetic reasons. Our findings have important implications for the conservation of bees and other specialist insects. Deceased     

Host specialization in habitat specialists and generalists

Generalists and specialists use different cues to find their habitat and essential resources. While generalists have the advantage of exploiting a wider range of resources, they are predicted to be less efficient in using one particular resource compared to specialists. The level of specialization of parasitoids can be either at the habitat or at the host level; strategies used by either type are expected to differ. We examined interactions between three aphid parasitoid species that are a habitat specialist Aphidius rhopalosiphi, a habitat generalist Aphidius ervi, and a host generalist Praon volucre on three cereal aphids, Sitobion avenae, Metopolophium dirhodum and Rhopalosiphum padi. We compared total parasitism rate across behavioral and physiological variation in a non-choice test. Next, we addressed total parasitism in two phases to examine: (1) the response of parasitoids to different hosts through the behavioral sequence from antennation through oviposition, and (2) the physiological suitability of different hosts for oviposition and larval development. Parasitization typically involved the following behavioral steps: (1) antennal contact, (2) abdominal bending, and (3) ovipositor insertion (acceptance). A. rhopalosiphi had the same number of antennal contacts with the three aphids but showed fewer instances of abdominal bending towards R. padi. Pre-contact host preference was found for A. ervi but it did not correspond to the level of acceptance. The number of antennal contacts by P. volucre corresponded to the parasitization level of the aphid species but more mummies were produced on M. dirhodum than on R. padi. These results suggest that parasitoid species that are habitat specialists react similarly to the different host species present in the same habitat, whereas generalist species exhibit clear preferences during host selection. Preferences were, however, not always related to host suitability.     

Diet characterisation of solitary bees on farmland: dietary specialisation predicts rarity

Changes in agricultural practice across Europe and North America have been associated with declines in wild bee populations. Bee diet breadth has been associated with sensitivity to agricultural intensification, but much of this analysis has been conducted at the categorical level of generalist or specialist, and it is not clear to what extent the level of generalisation within generalist species is also associated with species persistence. We used pollen load analysis to quantify the pollen diets of wild solitary bees on 19 farms across southern England, UK. A total of 72 species of solitary bees were recorded, but only 31 species were abundant enough to allow for formal diet characterisation. The results broadly conformed to existing literature with the majority of species polylectic and collecting pollen from a wide range of plants. Pollen load analysis consistently identified pollens from more plant species and families from each bee species than direct observation of their foraging behaviour. After rarefaction to standardise pollen load sample sizes, diet breadth was significantly associated with frequency of occurrence, with more generalist bees present on more farms than less generalist bees. Our results show that the majority of bee species present on farmland in reasonable numbers are widely variable in their pollen choices, but that those with the broadest diet were present on the greatest number of farms. Increasing the diversity of plants included in agri-environment schemes may be necessary to provide a wider range of pollen resources in order to support a diverse bee community on farmland.     

Contrasting effects of habitat discontinuity on three closely related fungivorous beetle species with diverging host‐use patterns and dispersal ability

Understanding how landscape structure influences biodiversity patterns and ecological processes are essential in ecological research and conservation practices. Forest discontinuity is a primary driver affecting the population persistence and genetic structure of forest‐dwelling species. However, the actual impacts on populations are highly species‐specific. In this study, we tested whether dispersal capability and host specialization are associated with susceptibility to forest discontinuity using three closely related, sympatric fungivorous ciid beetle species (two host specialists, Octotemnus assimilis and O. crassus; one host generalist, O. kawanabei). Landscape genetic analyses and the estimation of effective migration surfaces (EEMS) method consistently demonstrated contrasting differences in the relationships between genetic structure and configuration of forest land cover. Octotemnus assimilis, one of the specialists with a presumably higher dispersal capability due to lower wing loading, lacked a definite spatial genetic structure in our study landscape. The remaining two species showed clear spatial genetic structure, but the results of landscape genetic analyses differed between the two species: while landscape resistance appeared to describe the spatial genetic structure of the specialist O. crassus, genetic differentiation of the generalist O. kawanabei was explained by geographic distance alone. This finding is consistent with the prediction that nonforest areas act more strongly as barriers between specialist populations. Our results suggest that differences in host range can influence the species‐specific resistance to habitat discontinuity among closely related species inhabiting the same landscape.     

Optimal foraging predicts the ecology but not the evolution of host specialization in bacteriophages

We explore the ability of optimal foraging theory to explain the observation among marine bacteriophages that host range appears to be negatively correlated with host abundance in the local marine environment. We modified Charnov's classic diet composition model to describe the ecological dynamics of the related generalist and specialist bacteriophages phiX174 and G4, and confirmed that specialist phages are ecologically favored only at high host densities. Our modified model accurately predicted the ecological dynamics of phage populations in laboratory microcosms, but had only limited success predicting evolutionary dynamics. We monitored evolution of attachment rate, the phenotype that governs diet breadth, in phage populations adapting to both low and high host density microcosms. Although generalist phiX174 populations evolved even broader diets at low host density, they did not show a tendency to evolve the predicted specialist foraging strategy at high host density. Similarly, specialist G4 populations were unable to evolve the predicted generalist foraging strategy at low host density. These results demonstrate that optimal foraging models developed to explain the behaviorally determined diets of predators may have only limited success predicting the genetically determined diets of bacteriophage, and that optimal foraging probably plays a smaller role than genetic constraints in the evolution of host specialization in bacteriophages.     

On the role of sinigrin (mustard oil) in a tritrophic context: plant–aphid–aphidophagous hoverfly

1. Plant secondary metabolites can govern prey–predator interactions by altering the diet breadth of predators and sometimes provide an ecological refuge to prey. Brassicaceae plants and their specialist pests can be used as a model system for understanding the role of chemically mediated effects restricting the diet breadth of natural enemies, and consequently the occurrence of enemy‐free space for the specialist pest. 2. The objective of the present study was to test the performance of the generalist predator Episyrphus balteatus De Geer (Diptera: Syrphidae) fed on the specialist herbivore Brevicoryne brassicae L.(Homoptera: Aphididae), reared on two different brassica species: black mustard (Brassica nigra), a wild species with high levels of sinigrin; and canola (Brassica napus), a cultivated species without sinigrin. 3. The preference and performance of the predator and the performance of the prey were measured. Sinigrin was quantified by high‐performance liquid chromatography in both leaf samples and aphids reared on the two host plants. 4. The cabbage aphid performed better on canola than on black mustard. The performance of the predator on this aphid when reared on canola was clearly better than when reared on black mustard. Females had a higher overall preference for cabbage aphids reared on canola than on black mustard. 5. The ability of aphids reared on plants with high glucosinolate content to reduce the performance of their generalist predators indicates that the presence of B. nigra may provide enemy‐free space for the cabbage aphid from its predator, a concept that has useful application in the context of biological control for agricultural systems.     

Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes

Adaptive radiation is recognized by a rapid burst of phenotypic, ecological and species diversification. However, it is unknown whether different species within an adaptive radiation evolve reproductive isolation at different rates. We compared patterns of genetic differentiation between nascent species within an adaptive radiation of Cyprinodon pupfishes using genotyping by sequencing. Similar to classic adaptive radiations, this clade exhibits rapid morphological diversification rates and two species are novel trophic specialists, a scale‐eater and hard‐shelled prey specialist (durophage), yet the radiation is <10 000 years old. Both specialists and an abundant generalist species all coexist in the benthic zone of lakes on San Salvador Island, Bahamas. Based on 13 912 single‐nucleotide polymorphisms (SNPs), we found consistent differences in genetic differentiation between each specialist species and the generalist across seven lakes. The scale‐eater showed the greatest genetic differentiation and clustered by species across lakes, whereas durophage populations often clustered with sympatric generalist populations, consistent with parallel speciation across lakes. However, we found strong evidence of admixture between durophage populations in different lakes, supporting a single origin of this species and genome‐wide introgression with sympatric generalist populations. We conclude that the scale‐eater is further along the speciation‐with‐gene‐flow continuum than the durophage and suggest that different adaptive landscapes underlying these two niche environments drive variable progress towards speciation within the same habitat. Our previous measurements of fitness surfaces in these lakes support this conclusion: the scale‐eating fitness peak may be more distant than the durophage peak on the complex adaptive landscape driving adaptive radiation.     

Host selection by the generalist aphid Myzus persicae (Hemiptera: Aphididae) and its subspecies specialized on tobacco, after being reared on the same host

Decision-making during host selection by phytophagous insects has proved to be related to host range, with specialists taking faster decisions than generalists; however, this pattern fails to materialize in some host selection studies performed with aphids. Differences found in testing designs point to rearing effects on aphid host selection. To test whether specialization patterns derive from the nature of the aphid or as a consequence of rearing environment, host selection behaviours were compared between the generalist Myzus persicae (Sulzer) s.s. and its subspecies specialized on tobacco when reared on a common host and offered the choice of an alternative host and a non-host plant. Pre-alighting (host finding and attraction towards host volatiles) and post-alighting (leaf surface exploration and probing) behaviours did not differ between the generalist and the tobacco-specialist, except in the allocation of time to probing behaviour; furthermore, all specialists chose the host on which they performed best. Thus, although the specialist was not faster than the generalist, it showed a higher level of commitment to its preferred host plant.     

Microbial generalist or specialist: Intraspecific variation and dormancy potential matter

Microbial generalists and specialists coexist in the soil environment while having distinctive impacts on microbial community dynamics. In microbial ecology, the underlying mechanisms as to why a species is a generalist or a specialist remain ambiguous. Herein, we collected soils across a national scale and identified bacterial generalists and specialists according to niche breadth at the species level (OTU level), and the single-nucleotide differences in each species were measured to investigate intraspecific variation (at zero-radius OTU level). Compared with that of the specialists, the intraspecific variation of the generalists was much higher, which ensured their wider niche breadth and lower variability. The higher asynchrony and different niche preferences of conspecific individuals and the higher dormancy potential within the generalists further contributed to their stability in varying environments. Besides, generalists were less controlled by environmental filtering, which was indicated by the stronger signature of stochastic processes in their assembly, and had higher diversification and transition rates that allowed them to adapt to environmental changes to a greater extent than specialists. Overall, this study provides a new comprehensive understanding of the rules of assembly and the evolutionary roles of bacterial generalists and specialists. It also highlights the importance of intraspecific variation and the dormancy potential in the stability of species.     

Partitioning of herbivore hosts across time and food plants promotes diversification in the Megastigmus dorsalis oak gall parasitoid complex

Communities of insect herbivores and their natural enemies are rich and ecologically crucial components of terrestrial biodiversity. Understanding the processes that promote their origin and maintenance is thus of considerable interest. One major proposed mechanism is ecological speciation through host‐associated differentiation (HAD), the divergence of a polyphagous species first into ecological host races and eventually into more specialized daughter species. The rich chalcid parasitoid communities attacking cynipid oak gall wasp hosts are structured by multiple host traits, including food plant taxon, host gall phenology, and gall structure. Here, we ask whether the same traits structure genetic diversity within supposedly generalist parasitoid morphospecies. We use mitochondrial DNA sequences and microsatellite genotypes to quantify HAD for Megastigmus (Bootanomyia) dorsalis, a complex of two apparently generalist cryptic parasitoid species attacking oak galls. Ancient Balkan refugial populations showed phenological separation between the cryptic species, one primarily attacking spring galls, and the other mainly attacking autumn galls. The spring species also contained host races specializing on galls developing on different host‐plant lineages (sections Cerris vs. Quercus) within the oak genus Quercus. These results indicate more significant host‐associated structuring within oak gall parasitoid communities than previously thought and support ecological theory predicting the evolution of specialist lineages within generalist parasitoids. In contrast, UK populations of the autumn cryptic species associated with both native and recently invading oak gall wasps showed no evidence of population differentiation, implying rapid recruitment of native parasitoid populations onto invading hosts, and hence potential for natural biological control. This is of significance given recent rapid range expansion of the economically damaging chestnut gall wasp, Dryocosmus kuriphilus, in Europe.     

Larval feeding induced defensive responses in tobacco: comparison of two sibling species of <Emphasis Type="Italic">Helicoverpa</Emphasis> with different diet breadths

Plants respond differently to damage by different herbivorous insects. We speculated that sibling herbivorous species with different host ranges might also influence plant responses differently. Such differences may be associated with the diet breadth (specialization) of herbivores within a feeding guild, and the specialist may cause less intensive plant responses than the generalist. The tobacco Nicotinana tabacum L. is the common host plant of a generalist Helicoverpa armigera (Hübner) and a specialist H. assulta Guenée (Lepidoptera, Noctuidae). The induced responses of tobacco to feeding of these two noctuid herbivores and mechanical wounding were compared. The results showed that the feeding of the specialist H. assulta and the generalist H. armigera resulted in the same inducible defensive system, but response intensity of plants was different to these two species. Inductions of jasmonic acid (JA), lipoxygenase (LOX), and proteinase inhibitors (PIs) were not significantly different concerning these two species, but H. assulta caused the less intensive foliar polyphenol oxidase (PPO) increase, more intensive nicotine and peroxidase (POD) increases in tobacco than H. armigera. The defensive response of plant to herbivores with different diet breadth seems to be more complicated than we expected, and the specialist does not necessarily cause less intensive plant responses than the generalist.     

Coevolution and the adaptive value of autumn tree colours: colour preference and growth rates of a southern beech aphid

The evolutionary explanation for the change in leaf colour during autumn is still debated. Autumn colours could be a signal of defensive commitment towards insects (coevolution) or an adaptation against physical damage because of light at low temperatures (photoprotection). These two hypotheses have different predictions: (1) under the coevolution hypothesis, insects should not prefer red leaves in autumn and grow better in spring on trees with green autumn leaves; and (2) under the photoprotection hypothesis, insects should prefer and grow better on trees with red leaves because they provide better nutrition. Studying colour preference in autumn and growth rates in spring of a southern beech aphid species (Neuquenaphis staryi) on Nothofagus alessandrii, we found preference for green leaves in autumn but no differential performance of aphids in spring. We suggest that aphid preference for green might have evolved to exploit better their host during the autumn rather than to improve their performance in spring.     

The tri-trophic interactions hypothesis: interactive effects of host plant quality, diet breadth and natural enemies on herbivores

Several influential hypotheses in plant-herbivore and herbivore-predator interactions consider the interactive effects of plant quality, herbivore diet breadth, and predation on herbivore performance. Yet individually and collectively, these hypotheses fail to address the simultaneous influence of all three factors. Here we review existing hypotheses, and propose the tri-trophic interactions (TTI) hypothesis to consolidate and integrate their predictions. The TTI hypothesis predicts that dietary specialist herbivores (as compared to generalists) should escape predators and be competitively dominant due to faster growth rates, and that such differences should be greater on low quality (as compared to high quality) host plants. To provide a preliminary test of these predictions, we conducted an empirical study comparing the effects of plant (Baccharis salicifolia) quality and predators between a specialist (Uroleucon macolai) and a generalist (Aphis gossypii) aphid herbivore. Consistent with predictions, these three factors interactively determine herbivore performance in ways not addressed by existing hypotheses. Compared to the specialist, the generalist was less fecund, competitively inferior, and more sensitive to low plant quality. Correspondingly, predator effects were contingent upon plant quality only for the generalist. Contrary to predictions, predator effects were weaker for the generalist and on low-quality plants, likely due to density-dependent benefits provided to the generalist by mutualist ants. Because the TTI hypothesis predicts the superior performance of specialists, mutualist ants may be critical to A. gossypii persistence under competition from U. macolai. In summary, the integrative nature of the TTI hypothesis offers novel insight into the determinants of plant-herbivore and herbivore-predator interactions and the coexistence of specialist and generalist herbivores.