The genetics of indirect ecological effects-plant parasites and aphid herbivores.

When parasitic plants and aphid herbivores share a host, both direct and indirect ecological effects (IEEs) can influence evolutionary processes. We used a hemiparasitic plant (Rhinanthus minor), a grass host (Hordeum vulgare) and a cereal aphid (Sitobion avenae) to investigate the genetics of IEEs between the aphid and the parasitic plant, and looked to see how these might affect or be influenced by the genetic diversity of the host plants. Survival of R. minor depended on the parasite's population of origin, the genotypes of the aphids sharing the host and the genetic diversity in the host plant community. Hence the indirect effects of the aphids on the parasitic plants depended on the genetic environment of the system. Here, we show that genetic variation can be important in determining the outcome of IEEs. Therefore, IEEs have the potential to influence evolutionary processes and the continuity of species interactions over time

Coexistence through mutualist-dependent reversal of competitive hierarchies

Mechanisms that allow for the coexistence of two competing species that share a trophic level can be broadly divided into those that prevent competitive exclusion of one species within a local area, and those that allow for coexistence only at a regional level. While the presence of aphid-tending ants can change the distribution of aphids among host plants, the role of mutualistic ants has not been fully explored to understand coexistence of multiple aphid species in a community. The tansy plant (Tanacetum vulgare) hosts three common and specialized aphid species, with only one being tended by ants. Often, these aphids species will not coexist on the same plant but will coexist across multiple plant hosts in a field. In this study, we aim to understand how interactions with mutualistic ants and predators affect the coexistence of multiple species of aphid herbivores on tansy. We show that the presence of ants drives community assembly at the level of individual plant, that is, the local community, by favoring one ant-tended species, Metopeurum fuscoviride, while preying on the untended Macrosiphoniella tanacetaria and, to a lesser extent, Uroleucon tanaceti. Competitive hierarchies without ants were very different from those with ants. At the regional level, multiple tansy plants provide a habitat across which all aphid species can coexist at the larger spatial scale, while being competitively excluded at the local scale. In this case, ant mutualist-dependent reversal of the competitive hierarchy can drive community dynamics in a plant-aphid system

Chemotypic variation in terpenes emitted from storage pools influences early aphid colonisation on tansy

Tansy plants (Tanacetum vulgare L.) exhibit high chemical variation, particularly in mono- and sesquiterpenes that are stored in specialised glands on the plant surface. In the present work we investigated the effects of terpene chemotypes on Metopeurum fuscoviride, an aphid species specialised on tansy, and their tending ants, at the field scale. Previous studies have chemotyped tansy by assessing dominant compounds; here we propose a method of chemotyping using all volatile compounds that are likely emitted from the storage glands. The analysis is based on two extraction methods: GC-MS analysis of leaf hexane extracts and SBSE analysis of headspace emissions. In an initial screening we identified the subset of compounds present in both chemical patterns, labelled as ‘compounds likely emitted from storage’. In a large field survey we could show that the putative chemotypic emission pattern from storage pools significantly affected the early aphid colonisation of tansy. Moreover, the statistical analyses revealed that minor compounds exerted a stronger influence on aphid and tending-ant presence than dominant compounds. Overall we demonstrated that within the enormous chemotypic variation of terpenes in tansy plants, chemical signatures of volatile terpenes can be related to the occurrence of insects on individual plants in the field

Effect of plant chemical variation and mutualistic ants on the local population genetic structure of an aphid herbivore

Plants exhibit impressive genetic and chemical diversity, not just between species but also within species, and the importance of plant intraspecific variation for structuring ecological communities is well known. When there is variation at the local population level, this can create a spatially heterogeneous habitat for specialised herbivores potentially leading to non-random distribution of individuals across host plants. Plant variation can affect herbivores directly and indirectly via a third species, resulting in variable herbivore growth rates across different host plants. Herbivores also exhibit within-species variation, with some genotypes better adapted to some plant variants than others. We genotyped aphids collected across 2 years from a field site containing ~200 patchily distributed host plants that exhibit high chemical diversity. The distribution of aphid genotypes, their ant mutualists, and other predators was assessed across the plants. We present evidence that the local distribution of aphid (Metopeurum fuscoviride) genotypes across host-plant individuals is associated with variation in the plant volatiles (chemotypes) and non-volatile metabolites (metabotypes) of their host plant tansy (Tanacetum vulgare). Furthermore, these interactions in the field were influenced by plant-host preferences of aphid-mutualist ants. Our results emphasise that plant intraspecific variation can structure ecological communities not only at the species level but also at the genetic level within species and that this effect can be enhanced through indirect interactions with a third species

Under fire-simultaneous volatilome and transcriptome analysis unravels fine-scale responses of tansy chemotypes to dual herbivore attack

BACKGROUND: Tansy plants (Tanacetum vulgare L.) are known for their high intraspecific chemical variation, especially of volatile organic compounds (VOC) from the terpenoid compound group. These VOCs are closely involved in plant-insect interactions and, when profiled, can be used to classify plants into groups known as chemotypes. Tansy chemotypes have been shown to influence plant-aphid interactions, however, to date no information is available on the response of different tansy chemotypes to simultaneous herbivory by more than one insect species. RESULTS: Using a multi-cuvette system, we investigated the responses of five tansy chemotypes to feeding by sucking and/or chewing herbivores (aphids and caterpillars; Metopeurum fuscoviride Stroyan and Spodoptera littoralis Boisduval). Herbivory by caterpillars following aphid infestation led to a plant chemotype-specific change in the patterns of terpenoids stored in trichome hairs and in VOC emissions. The transcriptomic analysis of a plant chemotype represents the first de novo assembly of a transcriptome in tansy and demonstrates priming effects of aphids on a subsequent herbivory. Overall, we show that the five chemotypes do not react in the same way to the two herbivores. As expected, we found that caterpillar feeding increased VOC emissions, however, a priori aphid infestation only led to a further increase in VOC emissions for some chemotypes. CONCLUSIONS: We were able to show that different chemotypes respond to the double herbivore attack in different ways, and that pre-treatment with aphids had a priming effect on plants when they were subsequently exposed to a chewing herbivore. If neighbouring chemotypes in a field population react differently to herbivory/dual herbivory, this could possibly have effects from the individual level to the group level. Individuals of some chemotypes may respond more efficiently to herbivory stress than others, and in a group environment these "louder" chemotypes may affect the local insect community, including the natural enemies of herbivores, and other neighbouring plants

Global urban environmental change drives adaptation in white clover

Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale