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Aims The spread of invasive weeds threatens biodiversity and stability of ecosystems. Jacobaea vulgaris is an invasive weed in some countries and an outbreak species in its native European range. Although biological control using specialist herbivores is available, controlling with soil microorganisms remains far less explored. Methods Twenty bacteria strains isolated from roots of J. vulgaris were used to examine bacterial effects on seed germination, root morphology and early plant growth. Moreover, we tested direct effects of the bacteria on a specialist herbivore of J. vulgaris , the leaf chewing caterpillar ( Tyria jacobaeae ), commonly used in biocontrol. We also tested indirect effects of bacteria, via the plant, on the performance of T. jacobaeae and the aphid species Aphis jacobaeae . Lastly, we examined the host specificity of two tested bacteria on three other forbs. Results Two Gammaproteobacteria, Pseudomonas brassicacearum and Serratia plymuthica , significantly reduced root growth of seedlings in-vitro, while seed germination was unaffected. However, these negative effects were observed across other forb species as well. Bacillus spp. injection led to the highest T. jacobaeae caterpillar mortality, while ingestion had no effect. Inoculation of the plants with bacteria did not affect aphid performance, but significantly affected T. jacobaeae preference. Specifically, P. syringae and one Bacillus sp. strain significantly increased T. jacobaeae preference. Conclusions Our results show that two root-associated bacteria inhibit J. vulgaris growth, but their lack of host specificity restricts their potential for biocontrol. Our study also highlights that belowground microorganisms can hamper or enhance the performance of aboveground insects.

1. Plant–soil feedback (PSF) effects on plant performance strongly depend on the plant species that conditioned the soil. Recent studies have shown that PSF can change above-ground plant–insect interactions via soil-mediated changes in plant quality, but whether these effects depend on species-specific soil conditioning is unknown. We examined how PSF effects of several plant species influence above-ground plant–aphid interactions. 2. We grew ragwort (Jacobaea vulgaris) in field soil conditioned specifically by 10 plant species, belonging to three functional groups (grasses, forbs and legumes), in a multispecies mixture of the conditioned soils and in control (unconditioned) field soil. We measured plant biomass, concentrations of primary (amino acids) and secondary (pyrrolizidine alkaloids) metabolites in phloem exudates, and performance of the generalist aphid Brachycaudus cardui and the specialist Aphis jacobaeae. 3. We observed that plant species, via species-specific effects on soil fungal communities, exerted unique plant–soil effects on J. vulgaris biomass, amino acid concentrations in phloem exudates and aphid performance. The direction and magnitude of the species-specific PSF effects on aphid performance differed between both aphid species. PSF effects on soil fungal communities, plant biomass and A. jacobaeae performance also differed between grasses, forbs and legumes, with soil conditioning by forbs resulting in lowest plant biomass and aphid performance. 4. Synthesis. Our study provides novel evidence that PSF effects on above-ground plant–insect interactions are highly species specific. Our results add a new dimension to the rapidly developing research fields of PSF and above-below-ground interactions, and highlights that these fields are tightly linked.

Plant–soil feedback (PSF) effects on plant performance can be influenced by the availability of nutrients in the soil. Recent studies have shown that PSF effects can also change aboveground plant–insect interactions via soil-mediated changes in plant quality, but whether this is influenced by soil nutrient availability is unknown. We examined how fertilisation influences PSF effects on aboveground plant-aphid interactions in ragwort Jacobaea vulgaris. We grew J. vulgaris in soil conditioned by conspecific plants and in unconditioned soil at two levels of fertilisation and measured soil fungal communities, plant biomass, concentrations of primary (amino acids) and secondary (pyrrolizidine alkaloids; PAs) metabolites in phloem exudates, performance of the specialist aphid Aphis jacobaeae and sequestration of PAs by the aphid. We observed a strong interaction between soil conditioning and fertilisation on amino acid and PA concentrations in phloem exudates of J. vulgaris and on aphid performance, with opposite effects of soil conditioning at the two fertilisation levels. Plant biomass was reduced by soil conditioning and increased by fertilisation. Aphids contained high PA concentrations, converted N-oxides into tertiary amines and preferentially sequestered certain PA compounds, but PA sequestration was not affected by any of the treatments. We conclude that effects of PSF and fertilisation on plant chemistry and aphid performance are interdependent. Our study highlights the need to consider the importance of abiotic soil conditions on the outcome of PSF effects on aboveground plant–insect interactions.

Pyrrolizidine alkaloids (PAs) are the major defense compounds of plants in the Senecio genus. Here I will review the effects of PAs in Senecio on the preference and performance of specialist and generalist insect herbivores. Specialist herbivores have evolved adaptation to PAs in their host plant. They can use the alkaloids as cue to find their host plant and often they sequester PAs for their own defense against predators. Generalists, on the other hand, can be deterred by PAs. PAs can also affect survival of generalist herbivores. Usually generalist insects avoid feeding on young Senecio leaves, which contain a high concentration of alkaloids. Structurally related PAs can differ in their effects on insect herbivores, some are more toxic than others. The differences in effects of PAs on specialist and generalists could lead to opposing selection on PAs, which may maintain the genetic diversity in PA concentration and composition in Senecio species.

Background Insect-associated microorganisms can provide a wide range of benefits to their host, but insect dependency on these microbes varies greatly. The origin and functionality of insect microbiomes is not well understood. Many caterpillars can harbor symbionts in their gut that impact host metabolism, nutrient uptake and pathogen protection. Despite our lack of knowledge on the ecological factors driving microbiome assemblages of wild caterpillars, they seem to be highly variable and influenced by diet and environment. Several recent studies have shown that shoot-feeding caterpillars acquire part of their microbiome from the soil. Here, we examine microbiomes of a monophagous caterpillar ( Tyria jacobaeae ) collected from their natural host plant ( Jacobaea vulgaris ) growing in three different environments: coastal dunes, natural inland grasslands and riverine grasslands, and compare the bacterial communities of the wild caterpillars to those of soil samples collected from underneath each of the host plants from which the caterpillars were collected. Results The microbiomes of the caterpillars were dominated by Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes. Only 5% of the total bacterial diversity represented 86.2% of the total caterpillar’s microbiome. Interestingly, we found a high consistency of dominant bacteria within the family Burkholderiaceae in all caterpillar samples across the three habitats. There was one amplicon sequence variant belonging to the genus Ralstonia that represented on average 53% of total community composition across all caterpillars. On average, one quarter of the caterpillar microbiome was shared with the soil. Conclusions We found that the monophagous caterpillars collected from fields located more than 100 km apart were all dominated by a single Ralstonia . The remainder of the bacterial communities that were present resembled the local microbial communities in the soil in which the host plant was growing. Our findings provide an example of a caterpillar that has just a few key associated bacteria, but that also contains a community of low abundant bacteria characteristic of soil communities.

Plants produce a variety of secondary metabolites (PSMs) that may be selective against herbivores. Yet, specialist herbivores may use PSMs as cues for host recognition, oviposition, and feeding stimulation, or for their own defense against parasites and predators. This summarizes a dual role of PSMs: deter generalists but attract specialists. It is not clear yet whether specialist herbivores are a selective force in the evolution of PSM diversity. A prerequisite for such a selective force would be that the preference and/or performance of specialists is influenced by PSMs. To investigate these questions, we conducted an oviposition experiment with cinnabar moths ( Tyria jacobaeae ) and plants from an artificial hybrid family of Jacobaea vulgaris and Jacobaea aquatica . The cinnabar moth is a specialist herbivore of J . vulgaris and is adapted to pyrrolizidine alkaloids (PAs), defensive PSMs of these plants. The number of eggs and egg batches oviposited by the moths were dependent on plant genotype and positively correlated to concentrations of tertiary amines of jacobine-like PAs and some otosenine-like PAs. The other PAs did not correlate with oviposition preference. Results suggest that host plant PAs influence cinnabar moth oviposition preference, and that this insect is a potential selective factor against a high concentration of some individual PAs, especially those that are also involved in resistance against generalist herbivores.

• Hybridization can lead to novel qualitative or quantitative variation of secondary metabolite (SM) expression that can have ecological and evolutionary consequences. • We measured pyrrolizidine alkaloid (PA) expression in the shoots and roots of a family including one Jacobaea vulgaris genotype and one Jacobaea aquatica genotype (parental genotypes), two F1 hybrid genotypes, and 102 F2 hybrid genotypes using liquid chromatography–tandem mass spectrometry (LC‐MS/MS). • We detected 37 PAs in the roots and shoots of J. vulgaris, J. aquatica and the hybrids. PA concentrations and compositions differed between genotypes, and between roots and shoots. Three otosenine‐like PAs that only occurred in the shoots of parental genotypes were present in the roots of F2 hybrids; PA compositions were sometimes novel in F2 hybrids compared with parental genotypes, and in some cases transgressive PA expression occurred. We also found that PAs from within structural groups covaried both in the roots and in the shoots, and that PA expression was correlated between shoots and roots. • Considerable and novel variation present among F2 hybrids indicates that hybridization has a potential role in the evolution of PA diversity in the genus Jacobaea, and this hybrid system is useful for studying the genetic control of PA expression.

Plants produce a diversity of secondary metabolites (SMs) to protect them from generalist herbivores. On the other hand, specialist herbivores use SMs for host plant recognition, feeding and oviposition cues, and even sequester SMs for their own defense. Therefore, plants are assumed to face an evolutionary dilemma stemming from the contrasting effects of generalist and specialist herbivores on SMs. To test this hypothesis, bioassays were performed with F2 hybrids from Jacobaea species segregating for their pyrrolizidine alkaloids (PAs), using a specialist flea beetle (Longitarsus jacobaeae) and a generalist slug (Deroceras invadens). Our study demonstrated that while slug feeding damage was negatively correlated with the concentration of total PAs and that of senecionine-like PAs, flea beetle feeding damage was not affected by PAs. It was positively correlated though, with leaf fresh weight. The generalist slug was deterred by senecionine-like PAs but the specialist flea beetle was adapted to PAs in its host plant. Testing other herbivores in the same plant system, it was observed that the egg number of the specialist cinnabar moth was positively correlated with jacobine-like PAs, while the silver damage of generalist thrips was negatively correlated with senecionine- and jacobine-like PAs, and the pupae number of generalist leaf miner was negatively correlated with otosenine-like PAs. Therefore, while the specialist herbivores showed no correlation whatsoever with PA concentration, the generalist herbivores all showed a negative correlation with at least one type of PA. We concluded that the generalist herbivores were deterred by different structural groups of PAs while the specialist herbivores were attracted or adapted to PAs in its host plants.

We report evidence of adaptive evolution in juvenile development time on a decadal timescale for the cinnabar moth Tyria jacobaeae (Lepidoptera: Arctiidae) colonizing new habitats and hosts from the Willamette Valley to the Coast Range and Cascades Mountains in Oregon. Four lines of evidence reveal shorter egg to pupa juvenile development times evolved in the mountains, where cooler temperatures shorten the growing season: (i) field observations showed that the mountain populations have shorter phenological development; (ii) a common garden experiment revealed genetic determination of phenotypic differences in juvenile development time between Willamette Valley and mountain populations correlated with the growing season; (iii) a laboratory experiment rearing offspring from parental crosses within and between Willamette Valley and Cascades populations demonstrated polygenic inheritance, high heritability, and genetic determination of phenotypic differences in development times; and (iv) statistical tests that exclude random processes (founder effect, genetic drift) in favor of natural selection as explanations for observed differences in phenology. These results support the hypothesis that rapid adaptation to the cooler mountain climate occurred in populations established from populations in the warmer valley climate. Our findings should motivate regulators to require evaluation of evolutionary potential of candidate biological control organisms prior to release.

Insects experience a wide array of chemical pressures from plant allelochemicals and pesticides and have developed several effective counterstrategies to cope with such toxins. Among these, cytochrome P450 monooxygenases are crucial in plant-insect interactions. Flavin-dependent monooxygenases (FMOs) seem not to play a central role in xenobiotic detoxification in insects, in contrast to mammals. However, the previously identified senecionine N-oxygenase of the arctiid moth Tyria jacobaeae (Lepidoptera) indicates that FMOs have been recruited during the adaptation of this insect to plants that accumulate toxic pyrrolizidine alkaloids. Identification of related FMO-like sequences of various arctiids and other Lepidoptera and their combination with expressed sequence tag (EST) data and sequences emerging from the Bombyx mori genome project show that FMOs in Lepidoptera form a gene family with three members (FMO1 to FMO3). Phylogenetic analyses suggest that FMO3 is only distantly related to lepidopteran FMO1 and FMO2 that originated from a more recent gene duplication event. Within the FMO1 gene cluster, an additional gene duplication early in the arctiid lineage provided the basis for the evolution of the highly specific biochemical, physiological, and behavioral adaptations of these butterflies to pyrrolizidine-alkaloid-producing plants. The genes encoding pyrrolizidine-alkaloid-N-oxygenizing enzymes (PNOs) are transcribed in the fat body and the head of the larvae. An N-terminal signal peptide mediates the transport of the soluble proteins into the hemolymph where PNOs efficiently convert pro-toxic pyrrolizidine alkaloids into their non-toxic N-oxide derivatives. Heterologous expression of a PNO of the generalist arctiid Grammia geneura produced an N-oxygenizing enzyme that shows noticeably expanded substrate specificity compared with the related enzyme of the specialist Tyria jacobaeae. The data about the evolution of FMOs within lepidopteran insects and the functional characterization of a further member of this enzyme family shed light on this almost uncharacterized detoxification system in insects.