Final Report Summary - PLANTINSECTSYMBIONT (The role of insect symbionts in host plant use through their effect on plant-induced defenses)
It has long been known that insects are colonised by a diverse community of mutualistic symbionts that provide their hosts with nutrients that are missing in the diet. In the last decade it has become apparent that facultative symbionts (i.e. not required for host survival) in herbivorous insects can engage in complex interactions with the insect host plant and its natural enemies. Insect symbionts can influence host plant range in herbivorous insects by providing nutrients, but also through manipulation of plant defensive state or physiology. These changes may have consequences at the community level by affecting other insects sharing the same host plant. Insect symbionts can also affect the host’s interactions with natural enemies. Defensive symbionts, for example, are a group of micro-organisms that protect their hosts from natural enemies. These symbionts can confer direct protection, but they can also protect the host through changes in plant physiology and the emission of herbivore-induced plant volatiles, which are used by natural enemies to locate their insect host. An interesting community of insect natural enemies are parasitoids, a very diverse group of insects whose larvae develop at expenses of the host eventually killing it. To get a deeper understanding and to raise awareness on the importance of these interactions, the PlantInsectSymbiont project has developed several scientific objectives, training activities, dissemination practices and activities aimed at engaging the general public. To do this, we have used as a model system the pea aphid (Acyrthosiphon pisum), which is the main model species for the study of insect symbiosis.
One of the main research objectives of this project was to explore whether bacterial symbionts in the pea aphid could benefit their insect hosts by manipulating the physiology of the host plant. By allowing aphids with or without symbionts to feed on their host plant such effects can be tested. One of the hypotheses that we tested was whether such manipulation could directly benefit the aphid host and whether this had consequences for other insect species feeding on the same host plant. We found limited evidence in support of this hypothesis. Another hypothesis tested was whether aphids can benefit from their bacterial associates by reducing the emission of herbivore-induced plant volatiles that attract their natural enemies. By performing behavioural experiments, and analysing plant volatiles we found that the symbiont Hamiltonella defensa, but not Serratia symbiontica, affects the composition of the volatile blend in a way that attraction of the parasitic wasp Aphidius ervi is reduced. Pea aphids can feed on different host plants, and we have also demonstrated that this effect is consistent across host plant species, and at different aphid densities. For more than one decade, we know that H. defensa protects aphids from parasitoids by producing a toxin that is released in the insect body. Selection to acquire such an associated micro-organism is likely to be very high, but surprisingly these symbionts are only found in a proportion of aphid populations. Laboratory experiments suggest that symbiont prevalence varies in natural populations because in the absence of natural enemies, symbionts are costly. Despite great knowledge about the mechanisms of this interaction, we still know rather little about how this symbiont affects its host under field conditions. We therefore developed a field experiment that aimed at covering this gap. We found that defensive symbionts are costly in terms of aphid population densities. We also found that, although the symbiont is defensive in the laboratory against specific parasitoid species, in the field aphids were attacked by a diverse community of parasitoids and only the specialist Aphidius eadyi was negatively affected by the presence of the symbiont in the insect. In parallel to the main objectives proposed in the PlantInsectSymbiont project, we developed a project where we explored how H. defensa in the pea aphid affects the stability and dynamics of a community composed of three aphid species and their specialistic parasitoids. This project was partially funded by the British Ecological Society and revealed that in this aphid-parasitoid community the symbiont allowed its aphid host to dominate the community and to trigger cascades of extinctions that affected other aphid and parasitoid species.
An important part of the project has been devoted to result dissemination and networking. The fellow has attended to seven international conferences (one of them overseas), one Dutch national conference and has visited a total of seven international research institutes where talks about the project were given. This project is of multidisciplinary and collaborative nature, and the laboratory led by Prof. Godfray at the University of Oxford (England) has been the main collaborator. The fellow has visited the group several times, and three publications that involve both Wageningen and Oxford are now on their way of submission. Collaboration with the group in Oxford was important to improve the quality of the research, but also to forge the links between chemical and community ecology, and insect symbiosis. Together with Dr. Arjen Biere (Nederlands Instuitute of Ecology, Wageningen, the Netherlands), the fellow organised a Symposium at the Joint Annual Meeting of the British Ecological Society and Société Française d'Écologie entitled "Ménage à trois: ecological consequences of intricate interactions between plants, microbes and insects". In this Symposium Prof. Dicke gave the plenary talk and several contributions dealt with insect symbiosis. The main partners of this proposal have become recently involved in the COST Action (funded by the European Science Foundation) FA1405 “Using three-way interactions between plants, microbes and arthropods to enhance crop protection and production”. Prof. Dicke and the fellow are members of the Management Committee, and the fellow coordinates the Short Term Scientific Missions. This Action will build a European network of scientists in academia and in the Agri-business sector that working on the topic, and specific sections are devoted to explore the role on insect symbionts in insect-plant interactions. At the societal level, this network will be used to disseminate results to the general public, and to interact with farmers. The Action has already prioritized the inclusion of female researchers and researchers in early stages of their career.
In the short term the main impacts of this project are to contribute to fundamental research, although we appreciate important environmental, agricultural, technological, economic and societal impacts in the medium and the long term. The model system we worked with was the pea aphid. This species, and aphids in general, can be important pests, and biocontrol strategies using parasitoids are increasingly common to fight them. Insect symbiosis is increasingly recognised as important to control insect pests. Insect symbionts, for example, can be used to manipulate pests and biocontrol agents via transgenesis (i.e. the use if symbionts to deliver gene products to their hosts). Symbionts like H. defensa, by protecting their hosts from natural enemies, can also challenge pest control. We visited the company Biobest Sustainable Crop Management (Belgium) and gave a presentation about symbiosis and its application in pest control. This visit strengthened the link between Wageningen University and this company and a small project is now being developed to test whether symbionts can affect parasitoid performance via parasitoid feeding on aphid body fluids.
One of the main research objectives of this project was to explore whether bacterial symbionts in the pea aphid could benefit their insect hosts by manipulating the physiology of the host plant. By allowing aphids with or without symbionts to feed on their host plant such effects can be tested. One of the hypotheses that we tested was whether such manipulation could directly benefit the aphid host and whether this had consequences for other insect species feeding on the same host plant. We found limited evidence in support of this hypothesis. Another hypothesis tested was whether aphids can benefit from their bacterial associates by reducing the emission of herbivore-induced plant volatiles that attract their natural enemies. By performing behavioural experiments, and analysing plant volatiles we found that the symbiont Hamiltonella defensa, but not Serratia symbiontica, affects the composition of the volatile blend in a way that attraction of the parasitic wasp Aphidius ervi is reduced. Pea aphids can feed on different host plants, and we have also demonstrated that this effect is consistent across host plant species, and at different aphid densities. For more than one decade, we know that H. defensa protects aphids from parasitoids by producing a toxin that is released in the insect body. Selection to acquire such an associated micro-organism is likely to be very high, but surprisingly these symbionts are only found in a proportion of aphid populations. Laboratory experiments suggest that symbiont prevalence varies in natural populations because in the absence of natural enemies, symbionts are costly. Despite great knowledge about the mechanisms of this interaction, we still know rather little about how this symbiont affects its host under field conditions. We therefore developed a field experiment that aimed at covering this gap. We found that defensive symbionts are costly in terms of aphid population densities. We also found that, although the symbiont is defensive in the laboratory against specific parasitoid species, in the field aphids were attacked by a diverse community of parasitoids and only the specialist Aphidius eadyi was negatively affected by the presence of the symbiont in the insect. In parallel to the main objectives proposed in the PlantInsectSymbiont project, we developed a project where we explored how H. defensa in the pea aphid affects the stability and dynamics of a community composed of three aphid species and their specialistic parasitoids. This project was partially funded by the British Ecological Society and revealed that in this aphid-parasitoid community the symbiont allowed its aphid host to dominate the community and to trigger cascades of extinctions that affected other aphid and parasitoid species.
An important part of the project has been devoted to result dissemination and networking. The fellow has attended to seven international conferences (one of them overseas), one Dutch national conference and has visited a total of seven international research institutes where talks about the project were given. This project is of multidisciplinary and collaborative nature, and the laboratory led by Prof. Godfray at the University of Oxford (England) has been the main collaborator. The fellow has visited the group several times, and three publications that involve both Wageningen and Oxford are now on their way of submission. Collaboration with the group in Oxford was important to improve the quality of the research, but also to forge the links between chemical and community ecology, and insect symbiosis. Together with Dr. Arjen Biere (Nederlands Instuitute of Ecology, Wageningen, the Netherlands), the fellow organised a Symposium at the Joint Annual Meeting of the British Ecological Society and Société Française d'Écologie entitled "Ménage à trois: ecological consequences of intricate interactions between plants, microbes and insects". In this Symposium Prof. Dicke gave the plenary talk and several contributions dealt with insect symbiosis. The main partners of this proposal have become recently involved in the COST Action (funded by the European Science Foundation) FA1405 “Using three-way interactions between plants, microbes and arthropods to enhance crop protection and production”. Prof. Dicke and the fellow are members of the Management Committee, and the fellow coordinates the Short Term Scientific Missions. This Action will build a European network of scientists in academia and in the Agri-business sector that working on the topic, and specific sections are devoted to explore the role on insect symbionts in insect-plant interactions. At the societal level, this network will be used to disseminate results to the general public, and to interact with farmers. The Action has already prioritized the inclusion of female researchers and researchers in early stages of their career.
In the short term the main impacts of this project are to contribute to fundamental research, although we appreciate important environmental, agricultural, technological, economic and societal impacts in the medium and the long term. The model system we worked with was the pea aphid. This species, and aphids in general, can be important pests, and biocontrol strategies using parasitoids are increasingly common to fight them. Insect symbiosis is increasingly recognised as important to control insect pests. Insect symbionts, for example, can be used to manipulate pests and biocontrol agents via transgenesis (i.e. the use if symbionts to deliver gene products to their hosts). Symbionts like H. defensa, by protecting their hosts from natural enemies, can also challenge pest control. We visited the company Biobest Sustainable Crop Management (Belgium) and gave a presentation about symbiosis and its application in pest control. This visit strengthened the link between Wageningen University and this company and a small project is now being developed to test whether symbionts can affect parasitoid performance via parasitoid feeding on aphid body fluids.