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Data from: Strong dispersal in a parasitoid wasp overwhelms habitat fragmentation and host population dynamics

The population dynamics of a parasite depend on species traits, host dynamics, and the environment. Those dynamics are reflected in the genetic structure of the population. Habitat fragmentation has a greater impact on parasites than on their hosts because resource distribution is increasingly fragmented for species at higher trophic levels. This could lead to either more or less genetic structure than the host, depending on the relative dispersal rates of species. We examined the spatial genetic structure of the parasitoid wasp Hyposoter horticola, and how it was influenced by dispersal, host population dynamics, and habitat fragmentation. The host, the Glanville fritillary butterfly, lives as a metapopulation in a fragmented landscape in the Åland islands, Finland. We collected wasps throughout the 50 by 70 km archipelago and determined the genetic diversity, spatial population structure, and genetic differentiation using 14 neutral DNA microsatellite loci. We compared genetic structure of the wasp with that of the host butterfly using published genetic data collected over the shared landscape. Using maternity assignment, we also identified full-siblings among the sampled parasitoids to estimate the dispersal range of individual females. We found that, because the parasitoid is dispersive, it has low genetic structure, is not very sensitive to habitat fragmentation, and has less spatial genetic structure than its butterfly host. The wasp is sensitive to regional rather than local host dynamics, and there is a geographic mosaic landscape for antagonistic coevolution of host resistance and parasite virulence.

Data from: Prudent behavior rather than chemical deception enables a parasite to exploit its ant host

Many parasites display complex strategies to evade host detection. The principal view is that parasites of social insects deceive their host by means of advanced chemical adaptations such as mimicking the cuticular host recognition cues, being chemically odorless, or emitting manipulative volatiles. Apart from these chemical adaptations, parasites of social insects may also use simpler behavioral strategies to evade host detection. As yet, such behavior has rarely been studied. Here we tested which chemical and behavioral strategies the unspecialized parasitic rove beetle Thiasophila angulata uses to avoid detection by its aggressive Formica rufa red wood ant host. Chemical comparisons of the beetle's and the host ants' cuticular hydrocarbons showed that the beetle carried an idiosyncratic cuticular profile that was clearly different from that of its host. Beetles that were isolated from their host or were placed in the nests of another Formica species perfectly retained their original cuticular profiles and provoked equal levels of aggression. These results suggest that the beetles do not avoid host detection through chemical deception. In contrast, the beetle adapted its behavior to avoid aggression by the ants. In the presence of ants, the beetle behaved much more prudently by hiding more frequently and engaging in less risky runs. Overall, these results highlight that for relatively unspecialized parasites, general strategies such as prudent behavior can be equally effective as more specialized deception strategies to evade host detection.

Data from: Melanin-based colouration and host-parasite interactions under global change

The role of parasites in shaping melanin-based colour polymorphism, and the consequences of colour polymorphism for disease resistance, remain debated. Here we review recent evidence of the links between melanin-based colouration and the behavioural and immunological defences of vertebrates against their parasites. First we propose that (1) differences between colour morphs can result in variable exposure to parasites, either directly (certain colours might be more or less attractive to parasites) or indirectly (variations in behaviour and encounter probability). Once infected, we propose that (2) immune variation between differently coloured individuals might result in different abilities to cope with parasite infection. We then discuss (3) how these different abilities could translate in variable sexual and natural selection in environments varying in parasite pressure. Finally, we address (4) the potential role of parasites in the maintenance of melanin-based colouration polymorphism, especially in the context of global change and multiple stressors in human-altered environments. Because global change will likely affect both colouration and the spread of parasitic diseases in the next decades, future studies should take into account melanin-based colouration to better predict the evolutionary responses of animals to changing disease risk in human-altered environments.

opencc-zeroDec 2013View details →

Data from: The jack-of-all-trades is master of none: a pathogen's ability to infect a greater number of host genotypes comes at a cost of delayed reproduction.

A trade-off between a pathogen's ability to infect many hosts and its reproductive capacity on each host genotype is predicted to limit the evolution of an expanded host range, yet few empirical results provide evidence for the magnitude of such trade-offs. Here, we test the hypothesis for a trade-off between the number of host genotypes that a fungal pathogen can infect (host genotype range) and its reproductive capacity on susceptible plant hosts. We utilized strains of the oat crown rust fungus that carried widely varying numbers of virulence (avr) alleles known to determine host genotype range. We quantified total spore production and the expression of four pathogen life history stages: infection efficiency, time until reproduction, pustule size, and spore production per pustule. In support of the trade-off hypothesis, we found that virulence level, the number of avr alleles per pathogen strain, was correlated with significant delays in the onset of reproduction and with smaller pustule sizes. Modeling from our results, we conclude that trade-offs have the capacity to constrain the evolution of host genotype range in local populations. In contrast, long term trends in virulence level suggests that the continued deployment of resistant host lines over wide regions of the USA has generated selection for increased host genotype range.

Data from: A host immune hormone modifies parasite species interactions and epidemics: insights from a field manipulation.

Parasite epidemics can depend on priority effects, and parasite priority effects can result from the host immune response to prior infection. Yet we lack experimental evidence that such immune-mediated priority effects influence epidemics. To address this research gap, we manipulated key host immune hormones, then measured the consequences for within-host parasite interactions, and ultimately parasite epidemics in the field. Specifically, we applied plant immune-signaling hormones to sentinel plants, embedded into a wild host population, and tracked foliar infections caused by two common fungal parasites. Within host individuals, priority effects were altered by the immune-signaling hormone, salicylic acid. Scaling up from within-host interactions, hosts treated with salicylic acid experienced lower prevalence of a less aggressive parasite, increased burden of infection by a more aggressive parasite, and experienced fewer coinfections. Together, these results indicate that by altering within-host priority effects, host immune hormones can drive parasite epidemics. This study therefore experimentally links host immune hormones to within-host priority effects and parasite epidemics, advancing a more mechanistic understanding of how interactions among parasites alter their epidemics.

Data from: Effects of host genetics and environment on egg-associated microbiotas in brown trout (Salmo trutta)

Recent studies found fish egg-specific bacterial communities that changed over the course of embryogenesis, suggesting an interaction between the developing host and its microbiota. Indeed, single-strain infections demonstrated that the virulence of opportunistic bacteria is influenced by environmental factors and host immune genes. However, the interplay between a fish embryo host and its microbiota has not been studied yet at the community level. To test whether host genetics affects the assemblage of egg-associated bacteria, adult brown trout (Salmo trutta) were sampled from a natural population. Their gametes were used for full-factorial in vitro fertilizations to separate sire from dam effects. In total, 2520 embryos were singly raised under experimental conditions that differently support microbial growth. High-throughput 16S rRNA amplicon sequencing was applied to characterize bacterial communities on milt and fertilized eggs across treatments. Dam and sire identity influenced embryo mortality, time until hatching and composition of egg-associated microbiotas, but no link between bacterial communities on milt and on fertilized eggs could be found. Elevated resources increased embryo mortality and modified bacterial communities with a shift in their putative functional potential. Resource availability did not significantly affect any parental effects on embryo performance. Sire identity affected bacterial diversity that turned out to be a significant predictor of hatching time: embryos associated with high bacterial diversity hatched later. We conclude that both host genetics and the availability of resources define diversity and composition of egg-associated bacterial communities that then affect the life history of their hosts.

opencc-zeroDec 2013View details →

Data from: Low host specificity among arctic root-assosiated fungi

In High Arctic ecosystems, plant growth and reproduction are limited by low soil moisture and nutrient availability, low soil and air temperatures, and a short growing season. Mycorrhizal associations facilitate plant nutrient acquisition and water uptake and may therefore be particularly ecologically important in nutrition-poor and dry environments, such as parts of the Arctic. Similarly, endophytic root associates are thought to play a protective role, increasing plants' stress tolerance, and likely have an important ecosystem function. Despite the importance of these root-associated fungi, little is known about their host specificity in the Arctic. We investigated the host specificity of root-associated fungi in the common, widely distributed arctic plant species Bistorta vivipara, Salix polaris and Dryas octopetala in the High Arctic archipelago Svalbard. High-throughput sequencing of the internal transcribed spacer 1 (ITS1) amplified from whole root systems generated no evidence of host specificity and no spatial autocorrelation within two 3 m × 3 m sample plots. The lack of spatial structure at small spatial scales indicates that Common Mycelial Networks (CMNs) are rare in marginal arctic environments. Moreover, no significant differences in fungal OTU richness were observed across the three plant species, although their root system characteristics (size, biomass) differed considerably. Reasons for lack of host specificity could be that association with generalist fungi may allow arctic plants to more rapidly and easily colonize newly available habitats, and it may be favourable to establish symbiotic relationships with fungi possessing different physiological attributes.

Data from: Going undercover: increasing canopy cover around a host tree drives associational resistance to an insect pest

Neighbouring heterospecific plants are often observed to reduce the probability of herbivore attack on a given focal plant. While this pattern of associational resistance is frequently reported, experimental evidence for underlying mechanisms is rare particularly for potential plant species diversity effects on focal host plants and their physical environment. Here, we used an established forest diversity experiment to determine whether tree diversity effects on an important insect pest are driven by concomitant changes in host tree growth or the light environment. We examined the effects of tree species richness, canopy cover and tree growth on the probability of occurrence, the abundance, and volume of galls caused by the pineapple gall adelgid Adelges abietis on Norway spruce. Although tree diversity had no effect on gall abundance, we observed that both the probability of gall presence and gall volume (an indicator of maternal fecundity) decreased with tree species richness and canopy cover around host spruce trees. Structural equation models revealed that effects of tree species richness on gall presence and volume were mediated by concurrent increases in canopy cover rather than changes in tree growth or host tree density. As canopy cover did not influence tree or shoot growth, patterns of associational resistance appear to be driven by improved host tree quality or more favourable microclimatic conditions in monocultures compared to mixed-stands. Our study therefore demonstrates that changes in forest structure may be critical to understanding the responses of herbivores to plant diversity and may underpin associational effects in forest ecosystems.

Data from: Seasonally dependent relationship between insect herbivores and host plant density in Jatropha nana, a tropical perennial herb

The fact that plant spatial aggregation patterns shape insect herbivore communities in a variety of ways has resulted in a large body of literature on the subject. The landmark resource concentration hypothesis predicts that density of insect-herbivores per plant will increase as host plant density increases. I examined this prediction across temporal samplings using Jatropha nana and the associated specialist insect-herbivores as a system. Through 12 field samplings, I modelled the effect of host plant density on insect-herbivore loads. The initial samplings (2-3) provided evidence for the resource concentration hypothesis with insect loads increasing with increasing host plant density, whereas the later samplings (4-5, 7-11) showed the opposite- a resource dilution pattern with decline of insect loads with increasing host plant density. These patterns also depend on the biology of the herbivores and have important implications on J. nana population dynamics.

Data from: Host phenology and potential saprotrophism of ectomycorrhizal fungi in the boreal forest

Phenology-induced changes in carbon assimilation by trees may affect carbon stored in fine roots and as a consequence, alter carbon allocated to ectomycorrhizal fungi. Two competing models exist to explain carbon mobilization by ectomycorrhizal fungi. Under the 'saprotrophy model', decreased allocation of carbon may induce saprotrophic behaviour in ectomycorrhizal fungi, resulting in the decomposition of organic matter to mobilize carbon. Alternatively, under the 'nutrient acquisition model', decomposition may instead be driven by the acquisition of nutrients locked within soil organic matter compounds, with carbon mobilization a secondary process. We tested whether phenology-induced shifts in carbon reserves of fine roots of aspen (Populus tremuloides) affect potential activity of four carbon-compound degrading enzymes, β-glucuronidase, β-glucosidase, N-acetylglucosaminidase and laccase, by ectomycorrhizal fungi. Ectomycorrhizal roots from mature aspen were collected across eight stands in north-eastern Alberta, Canada, and analysed during tree dormancy, leaf flush, full leaf expansion and leaf abscission. We predicted potential extracellular enzyme activity to be highest when root carbon reserves were lowest, should host phenology induce saprotrophism. Further, we anticipated enzyme activity to be mediated by invertase, a plant-derived enzyme which makes carbon available to fungal symbionts in the plant–fungus interface. Root carbon reserves were positively correlated with invertase, suggesting phenology may affect carbon allocation to ectomycorrhizal fungi. However, of the four enzymes, host phenology had the largest effect on β-glucuronidase, but activity of this enzyme was not correlated with root carbon reserves or invertase. Low-biomass ectomycorrhizas had greater potential laccase activity than high-biomass ectomycorrhizas, highlighting discrete functional traits in fungi for litter decomposition. Our results suggest that the decomposition of organic matter may be driven by foraging by fungi for nutrients locked within organic compounds rather than for mobilizing carbon. Furthermore, the potential ability to degrade lignin was more common in low-biomass ectomycorrhizas when compared to high-biomass ectomycorrhizas.

Data from: Malagasy bats shelter a considerable genetic diversity of pathogenic Leptospira suggesting notable host-specificity patterns

Pathogenic Leptospira are the causative agents of leptospirosis, a disease of global concern with major impact in tropical regions. Despite the importance of this zoonosis for human health, the evolutionary and ecological drivers shaping bacterial communities in host reservoirs remain poorly investigated. Here, we describe Leptospira communities hosted by Malagasy bats, composed of mostly endemic species, in order to characterize host–pathogen associations and investigate their evolutionary histories. We screened 947 individual bats (representing 31 species, 18 genera and seven families) for Leptospira infection and subsequently genotyped positive samples using three different bacterial loci. Molecular identification showed that these Leptospira are notably diverse and include several distinct lineages mostly belonging to Leptospira borgpetersenii and L. kirschneri. The exploration of the most probable host-pathogen evolutionary scenarios suggests that bacterial genetic diversity results from a combination of events related to the ecology and the evolutionary history of their hosts. Importantly, based on the data set presented herein, the notable host-specificity we have uncovered, together with a lack of geographical structuration of bacterial genetic diversity, indicates that the Leptospira community at a given site depends on the co-occurring bat species assemblage. The implications of such tight host-specificity on the epidemiology of leptospirosis are discussed.

opencc-zeroDec 2016View details →

Data from: Genetic divergence with ongoing gene flow is maintained by the use of different hosts in phytophagous ladybird beetles genus Henosepilachna

Adaptation to different environments can promote population divergence via natural selection even in the presence of gene flow–a phenomenon that typically occurs during ecological speciation. To elucidate how natural selection promotes and maintains population divergence during speciation, we investigated the population genetic structure, degree of gene flow and heterogeneous genomic divergence in three closely related Japanese phytophagous ladybird beetles: Henosepilachna pustulosa, H. niponica and H. yasutomii. These species act as a generalist, a wild thistle (Cirsium spp.) specialist and a blue cohosh (Caulophyllum robustum) specialist, respectively, and their ranges differ accordingly. The two specialist species widely co-occur but are reproductively isolated solely due to their high specialisation to a particular host plant. Genome-wide amplified fragment-length polymorphism (AFLP) markers and mitochondrial cytochrome c oxidase subunit I (COI) gene sequences demonstrated obvious genome-wide divergence associated with both geographic distance and ecological divergence. However, a hybridisation assessment for both AFLP loci and the mitochondrial sequences revealed a certain degree of unidirectional gene flow between the two sympatric specialist species. Principal coordinates analysis (PCoA) based on all of the variable AFLP loci demonstrated that there are genetic similarities between populations from adjacent localities irrespective of the species (i.e. host range). However, a further comparative genome scan identified a few fractions of loci representing approximately 1% of all loci as different-host associated outliers. These results suggest that these three species had a complex origin, which could be obscured by current gene flow, and that ecological divergence can be maintained with only a small fraction of the genome is related to different host use even when there is a certain degree of gene flow between sympatric species pairs.

Data from: Host cues mediate growth and establishment of oak mistletoe (Phoradendron leucarpum, Viscaceae), an aerial parasitic plant.

The oak mistletoe (Phoradendron leucarpum, Viscaceae) is well-documented to exhibit preference for a few potential host species in a given locality, even when many potential host species are present. In trying to explain this distribution, we examined the mechanisms by which mistletoe seedlings recognize potentially suitable hosts in the Piney Woods ecoregion of east Texas. An initial survey of patterns of infection on the campus of Sam Houston State University revealed that water oak (Quercus nigra) was host to nearly half of the mistletoes observed, despite comprising less than 15% of trees surveyed. Field experiments demonstrated that light, host physiochemistry, and volatiles released from potential host trees serve as cues affecting the viability and establishment of mistletoe seedlings. These results provoked further study in controlled laboratory settings, in which it was demonstrated that chemical compounds in the bark of local host trees (compared to trees that serve as hosts elsewhere, but not in our survey) induce significantly although slightly greater seedling viability. Establishment of haustoria depended only on the presence of these chemicals, regardless of host species. Importantly, we demonstrated that three common monoterpenes, limonene, β-myrcene, and β-phellandrene induce a positive growth response of mistletoe radicles. These results taken together suggest a model to explain local host preference in P. leucarpum, in which covariation between mistletoe fruit maturity and monoterpene production by hosts determines the distribution of successful haustorial establishment.

opencc-zeroDec 2018View details →

Data from: Annual environmental variation influences host tolerance to parasites

When confronted with a parasite or pathogen, hosts can defend themselves by resisting or tolerating the attack. While resistance can be diminished when resources are limited, it is unclear how robust tolerance is to changes in environmental conditions. Here we investigate the sensitivity of tolerance in a single host population living in a highly variable environment. We manipulated the abundance of an invasive parasitic fly, Philornis downsi, in nests of Galápagos mockingbirds (Mimus parvulus) over four field seasons and measured host fitness in response to parasitism. Mockingbird tolerance to P. downsi varied significantly among years and decreased when rainfall was limited. Video observations indicate that parental provisioning of nestlings appears key to tolerance: in drought years, mockingbirds likely do not have sufficient resources to compensate for the effects of P. downsi. These results indicate that host tolerance is a labile trait and suggest that environmental variation plays a major role in mediating the consequences of host-parasite interactions.

opencc-zeroDec 2010View details →

Data from: Mountain pine beetle host-range expansion threatens the boreal forest

The current epidemic of the mountain pine beetle (MPB), an indigenous pest of western North American pine, has resulted in significant losses of lodgepole pine. The leading edge has reached Alberta where forest composition shifts from lodgepole to jack pine through a hybrid zone. The susceptibility of jack pine to MPB is a major concern, but there has been no evidence of host-range expansion, in part due to the difficulty in distinguishing the parentals and their hybrids. We tested the utility of a panel of microsatellite loci optimized for both species to classify lodgepole pine, jack pine and their hybrids using simulated data. We were able to accurately classify simulated individuals, and hence applied these markers to identify the ancestry of attacked trees. Here we show for the first time successful MPB attack in natural jack pine stands at the leading edge of the epidemic. This once unsuitable habitat is now a novel environment for MPB to exploit, a potential risk which could be exacerbated by further climate change. The consequences of host-range expansion for the vast boreal ecosystem could be significant.

Data from: Generalist haemosporidian parasites are better adapted to a subset of host species in a multiple host community

Parasites that can infect multiple host species are considered to be host generalists with low host specificity. However, whether generalist parasites are better adapted to a subset of their host species remains unknown. To elucidate this possibility, we compared the variation in prevalence and infection intensity among host species of three generalist parasite lineages belonging to the morphological species Haemoproteus majoris, in a natural bird community in southern Sweden. Prevalence in each host species was confirmed by nested PCR and DNA sequencing and infection intensities were quantified using lineage-specific real-time qPCR. For two of the three lineages, we detected positive correlations between prevalence and infection intensity, indicating that these generalist parasites are better adapted to a subset of host species, which may have been more frequently encountered during the evolution of the parasite; we refer to these as main host species. For both lineages, the main host species were more phylogenetically related than expected by chance as revealed by strong phylogenetic signal in prevalence among hosts. By comparing our results with previous records of these parasites, we found that the host range of a generalist parasite can vary among different communities and may partly be shaped by the presence of other parasites. Our study reveals that generalist parasites may be specialized on a subset of their host species and it highlights the importance of considering infection intensity and host phylogeny when determining the host specificity of a parasite.

opencc-zeroDec 2012View details →

Data from: Specificity, rank preference and the colonization of a non-native host plant by the Melissa blue butterfly

Animals often express behavioral preferences for different types of food or other resources, and these preferences can evolve or shift following association with novel food types. Shifts in preference can involve at least two phenomena: a change in rank preference or a change in specificity. The former corresponds to a change in the order in which hosts are preferred, while a shift in specificity can be an increase in the tendency to utilize multiple hosts. These possibilities have been examined in relatively few systems that include extensive population-level replication. The Melissa blue butterfly, Lycaeides melissa, has colonized exotic alfalfa, Medicago sativa, throughout western North America. We assayed host preferences of 229 females from 10 populations associated with novel and native hosts. In four out of five native-associated populations, a native host was preferred over the exotic host, while preference for a native host characterized only two out of five of the alfalfa-associated populations. Across all individuals from alfalfa-associated populations, there appears to have been a decrease in specificity: females from these populations lay fewer eggs on the native host and more eggs on the exotic relative to females from native-host populations. However, females from alfalfa-associated populations did not lay more eggs on a third plant species, which suggests that preferences for specific hosts in this system can potentially be gained and lost independently. Geographic variation in oviposition preference in L. melissa highlights the value of surveying a large number of populations when studying the evolution of a complex behavioral trait.

Data from: Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila

High-throughput transcriptome studies are breaking new ground to investigate the responses that organisms deploy in alternative environments. Nevertheless, much remains to be understood about the genetic basis of host plant adaptation. Here, we investigate genome-wide expression in the fly Drosophila buzzatii raised in different conditions. This species uses decaying tissues of cactus of the genus Opuntia as primary rearing substrate and secondarily, the necrotic tissues of the columnar cactus Trichocereus terscheckii. The latter constitutes a harmful host, rich in mescaline and other related phenylethylamine alkaloids. We assessed the transcriptomic responses of larvae reared in Opuntia sulphurea and T. terscheckii, with and without the addition of alkaloids extracted from the latter. Whole-genome expression profiles were massively modulated by the rearing environment, mainly by the presence of T. terscheckii alkaloids. Differentially expressed genes were mainly related to detoxification, oxidation–reduction and stress response; however, we also found genes involved in development and neurobiological processes. In conclusion, our study contributes new data onto the role of transcriptional plasticity in response to alternative rearing environments.

opencc-zeroDec 2016View details →

Data from: Host nest site choice depends on risk of cuckoo parasitism in magpie hosts

Avian brood parasites impose large fitness costs on their hosts and, thus, brood parasitism has selected for an array of host defensive mechanisms to avoid them. So far most studies have focused on antiparasite defenses operating at the egg and chick stages and neglected defenses that may work prior to parasite egg deposition. Here, we experimentally explore the possibility that hosts, as part of a front-line defense, might minimize parasitism costs through informed nest site choice based on perceived risk of cuckoo parasitism. We conducted a large-scale manipulation of visual and auditory cues potentially informing on the risk of great spotted cuckoo Clamator glandarius parasitism during the nest site choice period of the magpie Pica pica host to investigate its effect on host's nest settlement and individual year to year site fidelity. Early breeding magpies preferentially placed their nests in safe areas (i.e., in sites of low perceived risk of parasitism), and, this effect diluted with time elapsed since risk of parasitism was manipulated. Site fidelity of individual magpies decreased with risk of cuckoo parasitism, for those that were not parasitized in the previous year. Our results constitute the first strong evidence showing that hosts can minimize the costs of cuckoo parasitism through informed nest-site choice, calling for future consideration of defenses potentially operating prior to parasite egg deposition to achieve a better understanding of cuckoo-host coevolution.

Data from: Differential aphid toxicity to ladybeetles is not a function of host plant or facultative bacterial symbionts

Herbivores often defend themselves from predation by transmitting toxic plant-produced chemicals to their enemies. Polyphagous herbivores sometimes exhibit differential toxicity when found on various host plant species, which is generally assumed to reflect variation in plant chemistry. Here, however, we provide evidence that host-associated herbivore lineages can intrinsically differ in their toxic properties. Lineages of Aphis craccivora originating from black locust (Robinia pseudoacacia) are unsuitable food for the ladybeetle Harmonia axyridis, resulting in death of both larvae and adults, whereas aphid lineages originating from alfalfa (Medicago sativa) support larval development and adult reproduction. We show that locust-origin aphids remain toxic and alfalfa-origin aphids remain non-toxic when reared on any of three legume plants (fava, alfalfa or locust). Furthermore, toxicity is not a function of the facultative bacterial symbiont Arsenophonus, which is naturally present in locust-origin aphid lineages and facilitates aphid use of locust. Experimentally cured locust-origin lineages remain toxic, and an experimentally transinfected alfalfa-origin lineage remains non-toxic to H. axyridis. Instead, Arsenophonus plays an indirect role in the distribution of toxic aphid lineages by facilitating aphid use of locust. It is the parthenogenetic coinheritance of Arsenophonus and the toxic trait that observationally correlates locust-feeding with toxicity in A. craccivora, rather than host plant chemistry per se. Our results clearly demonstrate that aphid lineages intrinsically vary in their toxic properties in a way that neither plant chemistry nor bacterial symbionts can explain. A more inclusive paradigm is needed for understanding variation in herbivore defence against predators.