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Host-plant genotypic diversity and community genetic interactions mediate aphid spatial distribution.

ABSTRACT: Genetic variation in plants can influence the community structure of associated species, through both direct and indirect interactions. Herbivorous insects are known to feed on a restricted range of plants, and herbivore preference and performance can vary among host plants within a species due to genetically based traits of the plant (e.g., defensive compounds). In a natural system, we expect to find genetic variation within both plant and herbivore communities and we expect this variation to influence species interactions. Using a three-species plant-aphid model system, we investigated the effect of genetic diversity on genetic interactions among the community members. Our system involved a host plant (Hordeum vulgare) that was shared by an aphid (Sitobion avenae) and a hemi-parasitic plant (Rhinanthus minor). We showed that aphids cluster more tightly in a genetically diverse host-plant community than in a genetic monoculture, with host-plant genetic diversity explaining up to 24% of the variation in aphid distribution. This is driven by differing preferences of the aphids to the different plant genotypes and their resulting performance on these plants. Within the two host-plant diversity levels, aphid spatial distribution was influenced by an interaction among the aphid's own genotype, the genotype of a competing aphid, the origin of the parasitic plant population, and the host-plant genotype. Thus, the overall outcome involves both direct (i.e., host plant to aphid) and indirect (i.e., parasitic plant to aphid) interactions across all these species. These results show that a complex genetic environment influences the distribution of herbivores among host plants. Thus, in genetically diverse systems, interspecific genetic interactions between the host plant and herbivore can influence the population dynamics of the system and could also structure local communities. We suggest that direct and indirect genotypic interactions among species can influence community structure and processes.

SUBMITTER: Zytynska SE

PROVIDER: S-EPMC3925376 | biostudies-literature | 2014 Jan

REPOSITORIES: biostudies-literature

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Host-plant genotypic diversity and community genetic interactions mediate aphid spatial distribution.

Zytynska Sharon E SE Frantz Laurent L Hurst Ben B Johnson Andrew A Preziosi Richard F RF Rowntree Jennifer K JK

Ecology and evolution 20131215 2

Genetic variation in plants can influence the community structure of associated species, through both direct and indirect interactions. Herbivorous insects are known to feed on a restricted range of plants, and herbivore preference and performance can vary among host plants within a species due to genetically based traits of the plant (e.g., defensive compounds). In a natural system, we expect to find genetic variation within both plant and herbivore communities and we expect this variation to i ...[more]

PMID: 24558568

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Project description:Background and aimsThe rising atmospheric CO2 concentration ([CO2]) is a ubiquitous selective force that may strongly impact species distribution and vegetation functioning. Plant-plant interactions could mediate the trajectory of vegetation responses to elevated [CO2], because some plants may benefit more from [CO2] elevation than others. The relative contribution of plastic (within the plant's lifetime) and genotypic (over several generations) responses to elevated [CO2] on plant performance was investigated and how these patterns are modified by plant-plant interactions was analysed.MethodsPlantago asiatica seeds originating from natural CO2 springs and from ambient [CO2] sites were grown in mono stands of each one of the two origins as well as mixtures of both origins. In total, 1944 plants were grown in [CO2]-controlled walk-in climate rooms, under a [CO2] of 270, 450 and 750 ppm. A model was used for upscaling from leaf to whole-plant photosynthesis and for quantifying the influence of plastic and genotypic responses.Key resultsIt was shown that changes in canopy photosynthesis, specific leaf area (SLA) and stomatal conductance in response to changes in growth [CO2] were mainly determined by plastic and not by genotypic responses. We further found that plants originating from high [CO2] habitats performed better in terms of whole-plant photosynthesis, biomass and leaf area, than those from ambient [CO2] habitats at elevated [CO2] only when both genotypes competed. Similarly, plants from ambient [CO2] habitats performed better at low [CO2], also only when both genotypes competed. No difference in performance was found in mono stands.ConclusionThe results indicate that natural selection under increasing [CO2] will be mainly driven by competitive interactions. This supports the notion that plant-plant interactions have an important influence on future vegetation functioning and species distribution. Furthermore, plant performance was mainly driven by plastic and not by genotypic responses to changes in atmospheric [CO2].

Project description:Previous syntheses on the effects of environmental conditions on the outcome of plant-plant interactions summarize results from pairwise studies. However, the upscaling to the community-level of such studies is problematic because of the existence of multiple species assemblages and species-specific responses to both the environmental conditions and the presence of neighbors. We conducted the first global synthesis of community-level studies from harsh environments, which included data from 71 alpine and 137 dryland communities. Here we: i) test how important are facilitative interactions as a driver of community structure, ii) evaluate whether the frequency of positive plant-plant interactions across differing environmental conditions and habitats is predictable, and iii) assess whether thresholds in the response of plant-plant interactions to environmental gradients exists between "moderate" and "extreme" stress levels. We also used those community-level studies performed across gradients of at least three points to evaluate how the average environmental conditions, the length of the gradient studied, and the number of points sampled across such gradient affect the form and strength of the facilitation-environment relationship. Over 25% of the species present were more spatially associated to nurse plants than expected by chance in both alpine and dryland areas, illustrating the high importance of positive plant-plant interactions for the maintenance of plant diversity. Facilitative interactions were more frequent, and more related to environmental conditions, in alpine than in dryland areas, perhaps because drylands are generally characterized by a larger variety of environmental stress factors and plant functional traits. The frequency of facilitative interactions in alpine communities peaked at 1000 mm of annual rainfall, and globally decreased with elevation. The frequency of positive interactions in dryland communities decreased globally with water scarcity or temperature annual range. Positive facilitation-drought stress relationships are more likely in shorter regional gradients, but these relationships are obscured in regions with a greater species turnover or with complex environmental gradients. By showing the different climatic drivers and behaviors of plant-plant interactions in dryland and alpine areas, our results will improve predictions regarding the effect of facilitation on the assembly of plant communities and their response to changes in environmental conditions.

Project description:Polyphagous aphids often consist of host-specialized lineages, which have greater fitness on their native hosts than on others. The underlying causes are important for understanding of the evolution of diet breadth and host shift of aphids. The cotton-melon aphid Aphis gossypii Glover is extremely polyphagous with many strict host-specialized lineages. Whether and how the lineage specialized on the primary host hibiscus shifts to the secondary host cucumber remains elusive. We found that the hibiscus-specialized lineage suffered high mortality and gave birth to very few nymphs developing into yellow dwarfs on fresh cucumber leaves, and did not inflict any damage symptoms on cucumber plants. The poor performance did not improve with prolonged exposure to cucumber; however, it did significantly improve when the cucumber leaves were pre-infected with a biotrophic phytopathogen Pseudoperonospora cubensis. More importantly, the hibiscus-specialized lineage with two-generation feeding experience on pre-infected cucumber leaves performed as well as the cucumber-specialized lineage did on fresh cucumber leaves, and inflicted typical damage symptoms on intact cucumber plants. Electrical penetration graph (EPG) indicated that the hibiscus-specialized lineage did not ingest phloem sap from fresh cucumber leaves but succeeded in ingesting phloem sap from pre-infected cucumber leaves, which explained the performance improvement of the hibiscus-specialized lineage on pre-infected cucumber leaves. This study revealed a new pathway for the hibiscus-specialized lineage to quickly acclimate to cucumber under the assistance of the phytopathogen. We considered that the short feeding experience on pre-infected cucumber may activate expression of effector genes that are related to specific host utilization. We suggest to identify host-specific effectors by comparing proteomes or/and transcriptomes of the hibiscus-specialized lineage before and after acclimating to cucumber.

Dataset Information

Host-plant genotypic diversity and community genetic interactions mediate aphid spatial distribution.

Publications

Host-plant genotypic diversity and community genetic interactions mediate aphid spatial distribution.

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