Cooperation or conflict in coexisting aphid symbionts?

Lead Research Organisation: University of York
Department Name: Biology

Abstract

Many insects carry bacterial symbionts that are transmitted from mother to offspring. These symbionts have diverse roles in their hosts' life-histories. The best-known group of symbionts are bacteria that provide nutrients to their hosts, which the host cannot obtain from its diet. These types of bacteria typically occur in insects that feed on very imbalanced types of food such as plant saps, cellulose or blood and are usually found in every individual of the insect species. A second group of symbionts has a much more variable distribution; within a population of insects they are usually found in some individuals but not others. However, these types of bacteria, called secondary symbionts, can provide important benefits to their hosts and often help the insect to cope with environmental challenges. They can, for example, protect the insect from attack by natural enemies such as viruses and other pathogens or reduce the detrimental effects of high temperatures.

Many of the insects that carry such symbionts are agricultural pests or vectors of human diseases. Understanding the biology of these interactions is therefore important and might lead to novel control strategies. For example, there are attempts of using symbiotic bacteria to inhibit the transmission of insect-borne pathogens that cause diseases such as malaria, dengue virus or Chagas disease.
Aphids are one of the most important agricultural pests in temperate regions. They damage plants by feeding on plant sap and simultaneously often transmit plant viruses. All aphids host a nutritional symbiont and many also carry one or more secondary symbionts.

The proposed project seeks to understand the interactions in this menagerie of symbionts. Often several secondary symbiont species are found in one host individual. We have a good understanding of many of the effects of these symbionts on their own, but know very little of how they act in concert. For example, one of the symbiont species increases the aphid's resistance to parasitic wasps, while another increases resistance to pathogenic fungi. When they co-occur, it is likely that the two species compete with each other inside the insect and we seek to investigate whether this competition limits their ability to benefit the host. At the same time, the two symbionts are likely to coexist over many generations since they are transmitted from mother to offspring. They therefore share interests with their host and should be selected so that the insect fitness is maximised. The proposed work aims at understanding these interacting processes. One prediction is that the negative effects of competition are minimised when symbionts that have coexisted for a long time interact, but that competition is more severe and might carry higher costs for the host when symbionts form novel associations. This work will advance our understanding how ecological communities evolve and might through a better understanding of aphid biology provide avenues towards new pest control strategies.

Technical Summary

The ecology of many insects is strongly affected by their vertically-transmitted bacterial symbionts: symbionts enable their hosts to feed on nutritionally imbalanced diets and many protect the host from unfavourable environmental conditions and natural enemies. A surprising range of ecologically-important effects have been described. Many insect species that harbour symbiotic bacteria are agricultural pests or vectors of diseases. The symbionts might therefore prove useful for the control of the insects or for limiting the spread of diseases.

Due to the recent discovery of many of the bacterial species, most of their effects have been studied using infections with single symbiont species. However, many symbionts coexist with other species within a host individual. Coexisting symbionts are likely to compete for resources and space. At the same time, their interactions will be expressed at the level of the host's phenotype and because the symbionts are vertically transmitted, mutualistic interactions should evolve. These systems are therefore ideal for studying how selection acts on multiple levels in a community.

The overarching aim of the proposed project is to elucidate the ecological effects of multiple symbionts in an aphid model system by studying within-host competition, co-transmission and the effects of multiple symbionts on the host's fitness and interactions with other species.
This aims will be achieved by manipulating the symbiont species complement in a series of aphid genotypes. These aphid lines will then be compared for a series of traits, including fecundity, resistance to parasitoids and pathogenic fungi and tolerance to heat shock. This will be complemented by studying the interactions of multiple symbionts inside the insect using quantitative PCR.

The results will be important for evolutionary ecology, but through an increased understanding of aphid biology might also have implications for pest control.

Planned Impact

Who will benefit from this research and how?

The primary beneficiary of this research is the academic community as described elsewhere. Briefly, this work will be of interest to evolutionary biologists and ecologists, especially those with interests in symbiosis, as well as applied entomologists working on the control of agricultural pests and vector-borne diseases.

The agricultural industry is likely to benefit from this research in the long term. The proposed project will contribute to a better understanding of aphid biology and insect-symbiont interactions in general. Aphids are major agricultural pests and a thorough understanding of their biology will diversify the range of possible control methods and therefore contribute to improved food security. The use of insecticides is a major concern for human and ecosystem health and developing pest management strategies that decrease pesticide use is desirable. Insect symbionts might provide more specific targets for pest control or routes of limiting the spread of plant viruses. This project will provide some of the scientific underpinning to such approaches, but is likely to have an applied impact only in the long term and in combination with other studies.

The PDRA and the technician (as well as their future employers) will benefit since both will be trained in a variety of molecular and entomological techniques. These techniques can be applied in a wide variety of other academic fields and in industry. They will also acquire many transferable skills such presentation skills, analytical skills and be trained in experimental design. These well-qualified individuals will be in a strong position to contribute to the economic and social wealth of the country.

The diversity of symbionts and their effects on natural communities can be used as examples of extraordinary natural adaptations and for illustrating principles of evolution. The general public will benefit from the research by having access to these examples and by hopefully gaining a deeper understanding of the intricacies of natural processes. This will be achieved by participation in the Department of Biology's outreach activities, which are predominantly aimed at school children, but also through the production of materials suitable for all ages.

Because the work concentrates on the fundamental biology of aphid/symbiont/natural enemy interactions, the impact activities will concentrate on public engagement, communication with the agricultural sector and training.

Publications

10 25 50
 
Description Insects carry many bacterial symbionts which have been shown to affect many of their life-history traits and interactions with other species. The pea aphid is a model system to study these symbioses. Using the pea aphid, we aimed at testing the hypothesis that long-term co-transmission of secondary symbionts has led to mutualistic associations between multiple symbiont species and their host. We have assessed how selection on multiple levels in this community affects the ecology of their host by studying the levels of co-transmission of all three partners, within-host competition and the ecological effects of long-term associations of symbiont genotypes of different species compared to artificial associations of the same species.
Our objectives were the following:
1. To characterise the phenotypic effects of the recently discovered "X-type" symbiont.
2. To test the hypothesis that double-infections of two symbiont species reduce the benefits provided by a secondary symbiont compared to single infections.
3. To test the hypothesis that naturally co-occurring symbiont genotypes have coevolved to provide greater benefits to the host than artificial combinations of the same symbiont species in a variety of ecological scenarios.
4. To assess whether infections of multiple symbiont species are independently regulated by the host or whether competition results in reduced densities of one or both species.
5. To measure the frequency of co-transmission of multiple symbionts through the sexual part of the aphid life-cycle.

We have characterised the effects of the "X-type" symbiont, and found that it has multiple effects on the host, including increasing resistance to a fungal pathogen, a parasitoid wasp and to heat shock. This has been published in Heyworth and Ferrari (2015).
We are still in the process of analysing and publishing the remaining data, which are very promising. There are widespread genotype x genotype interactions between the different species of symbionts for most of the traits tested. There is little evidence that there are differences between older and more recent associations of symbiont strains.
We will report on this more fully once the papers are published.
Exploitation Route Bacterial symbionts in insects have the potential of being employed for pest and vector control. Through a deeper understanding of their ecology, it may be possible to develop more efficient control methods.
It will be important to investigate the mechanisms of the interactions highlighted above.
Sectors Agriculture, Food and Drink,Environment

 
Description Speciaphid 
Organisation French National Institute of Agricultural Research
Department INRA Rennes Centre
Country France 
Sector Public 
PI Contribution Our work on speciation in aphids and on the role of bacterial symbionts in aphids is done under the speciaphid agreement, an agreement between French and British researchers to coordinate their research efforts on this system, collaborate and share material. We have exchanged samples, data as well as meeting on a regular basis.
Collaborator Contribution Our work on speciation in aphids and on the role of bacterial symbionts in aphids is done under the speciaphid agreement, an agreement between French and British researchers to coordinate their research efforts on this system, collaborate and share material. We have exchanged samples, data as well as meeting on a regular basis.
Impact The collaboration involves researchers specialising in ecology, evolutionary biology, agricultural sciences, genomics and bioinformatics.
Start Year 2012
 
Description Speciaphid 
Organisation University of Montpellier
Department Institute of Evolutionary Sciences (ISEM)
Country France 
Sector Academic/University 
PI Contribution Our work on speciation in aphids and on the role of bacterial symbionts in aphids is done under the speciaphid agreement, an agreement between French and British researchers to coordinate their research efforts on this system, collaborate and share material. We have exchanged samples, data as well as meeting on a regular basis.
Collaborator Contribution Our work on speciation in aphids and on the role of bacterial symbionts in aphids is done under the speciaphid agreement, an agreement between French and British researchers to coordinate their research efforts on this system, collaborate and share material. We have exchanged samples, data as well as meeting on a regular basis.
Impact The collaboration involves researchers specialising in ecology, evolutionary biology, agricultural sciences, genomics and bioinformatics.
Start Year 2012
 
Description Speciaphid 
Organisation University of Oxford
Department Department of Zoology
Country United Kingdom 
Sector Academic/University 
PI Contribution Our work on speciation in aphids and on the role of bacterial symbionts in aphids is done under the speciaphid agreement, an agreement between French and British researchers to coordinate their research efforts on this system, collaborate and share material. We have exchanged samples, data as well as meeting on a regular basis.
Collaborator Contribution Our work on speciation in aphids and on the role of bacterial symbionts in aphids is done under the speciaphid agreement, an agreement between French and British researchers to coordinate their research efforts on this system, collaborate and share material. We have exchanged samples, data as well as meeting on a regular basis.
Impact The collaboration involves researchers specialising in ecology, evolutionary biology, agricultural sciences, genomics and bioinformatics.
Start Year 2012
 
Description Speciaphid 
Organisation University of Sheffield
Country United Kingdom 
Sector Academic/University 
PI Contribution Our work on speciation in aphids and on the role of bacterial symbionts in aphids is done under the speciaphid agreement, an agreement between French and British researchers to coordinate their research efforts on this system, collaborate and share material. We have exchanged samples, data as well as meeting on a regular basis.
Collaborator Contribution Our work on speciation in aphids and on the role of bacterial symbionts in aphids is done under the speciaphid agreement, an agreement between French and British researchers to coordinate their research efforts on this system, collaborate and share material. We have exchanged samples, data as well as meeting on a regular basis.
Impact The collaboration involves researchers specialising in ecology, evolutionary biology, agricultural sciences, genomics and bioinformatics.
Start Year 2012
 
Description Hosting school pupils 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Two students visited the lab for a day to learn more about our research.
Year(s) Of Engagement Activity 2016
 
Description Microbiologist article 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Article for publication of the Society for Applied Microbiology "Microbiologist"
Year(s) Of Engagement Activity 2017
URL https://issuu.com/paulsainsbury1/docs/microbiologist_march_web
 
Description School Visit (York) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact 60 primary school children attended this session, which sparked interest in entomology, aphids and ecology more generally
Year(s) Of Engagement Activity 2017
 
Description ZSL event 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Evening event at the Zoological Society London "Ecosystems under the microscope: why microbes matter for conservation"
Approximately 120 people attended this event with three talks and a panel debate
Year(s) Of Engagement Activity 2018