Aphids, Bacteria and Fungal Pathogens; the Ecology of a Complex Symbiosis

Lead Research Organisation: University of Oxford
Department Name: Zoology

Abstract

The easy availability of molecular techniques over the last two decades has revolutionised our understanding of how animals and plants interact with micro-organisms. Many previously unsuspected symbioses have been discovered and many new issues for our understanding of biodiversity and community ecology have arisen. This proposal is part of a long-term project to understand the dynamics and persistence of a complex mutualistic symbiosis involving an aphid and no less than eight bacterial partners. This has become a model system used by laboratories around the world exploring the ecology and evolution of symbiosis.

Aphids are familiar insects in temperate regions and in these areas are the most important pests of arable crops. Despite being closely studied since the dawn of the scientific age the last 15 years have seen a complete reappraisal of many aspects of their biology as the importance of their bacterial symbionts has become apparent. Aphids feed on plant sap which is nutritionally imbalanced and it has been known for 50 years that they carry an obligate (or primary) bacterial symbiont called Buchnera which synthesises essential nutrients missing in their diet. But we now know that in addition to Buchnera there are at least seven other facultative or secondary symbionts, present in some aphids but not others. Moreover, these facultative symbionts have many effects on their host's biology including conferring resistance to parasites and pathogens, enabling their hosts to withstand heat shock or use different host plants, and influencing life history strategy.

Our laboratory has particularly worked on how symbionts influence the aphid's ability to withstand attack by fungal pathogens. We discovered that one bacteria called Regiella insecticola markedly increased resistance to the most common fungal disease. Curiously this symbiont species is particularly associated with aphids feeding on clover (pea aphid has a complex population structure comprised of genetically differentiated "biotypes" associated with different host plants within the pea family). Very recently our laboratory has mapped the genetic structure of Regiella showing that isolates from pea aphid are organised into two major genetic groups (or clades). We have also found that other recently discovered secondary symbionts can impart fungal resistance which suggests that this might be a general strategy that symbionts use to spread through host populations.

The proposal is to support continuing work on pea aphid symbionts in our laboratory focussing on the ecology of the interaction between pea aphid, their host plants and fungal pathogens, and the facultative symbionts that confer resistance. We shall test the hypothesis that the aphid biotype on clover suffers particularly from fungal pathogens and hence needs to carry Regiella. Using reciprocal introductions of bacteria we shall ask why Regiella from the two major clades infect different biotypes and explore whether all clades provide resistance. Fungus can still kill aphids carrying Regiella (though with lower probability) but they are then less likely to produce infectious spores and we shall test the hypothesis that this has evolved through kin selection. All work to date has involved a single fungal pathogen though we know from our community studies that other pathogens are present in the field. We shall investigate the specificity of fungal resistance. We shall build on our recent pilot study demonstrating that some isolates of other symbionts confer resistance to establish the extent to which this occurs in natural populations. Finally, we shall use modern DNA sequencing techniques to test the hypothesis that fungal resistance is caused by a common mechanism that has been transferred horizontally amongst these unrelated bacteria.

Planned Impact

The major aims of the project are to contribute to the fundamental science base and we are not able to identify precise beneficiaries outside the academic community who we can definitely say will be influenced by our work within the course of the project. Nevertheless we appreciate the importance of exploring possible beneficiaries and in our Pathways to Impact plan seek to maximise the likelihood that all possible beneficial outcomes are realised.

The following potential beneficiaries have been identified.

Research scientists engaged in applied pest management.

We understand that academic beneficiaries should not be included in this section unless their role in pathways to impact can be justified. We include them here as if this fundamental research involving a major crop pest is to be translated into economic benefits through improved pest management then there needs to be improved communication between the more basic and applied wings of entomology. We include here not only "strictly" academic research scientists in universities but also those working in research stations, particularly Rothamsted Research International which in England contains the major group doing translational research on aphids as crop pests.

Industry and farmers

The chief strategy for aphid control at the moment is insecticide application and it unlikely that our work will assist in the discovery of new compounds or better strategies to apply insecticides. There are however two ways in which our work might help the farming industry. First there is strong pressure to reduce insecticide use on conventional farms while organic already restrict synthetic chemical use. Increasing the efficacy of biological control including through the natural enhancement of fungal pathogens, or by their direct application, is a strategy that has been considered in the past though as far as we are aware does not currently contribute to integrated pest management. We shall (i) describe our emerging results in non-specialist terms on the Oxford Martin School's Future of Food website and (ii) participate in our third year in a stakeholder event organised by the Programme.

The second possible application is more speculative. Aphids transmit some very important crop diseases(such as Barley Yellow Dwarf Virus which is not confined to wheat). It is likely that techniques will soon become available to genetically manipulate aphids such that transmission is no longer possible (in the same way that mosquitoes can now be manipulated so that they cannot transmit malaria). Such innovations are useless unless means exist of "driving" a beneficial trait through a wild population. There are two classes of drive mechanisms being actively considered in mosquitoes (work in this area is more advanced in human disease vectors than in crop disease vectors). The first is molecular drive mechanisms and the second is the use of endosymbionts which can naturally spread through a population (our group has published in both areas). Work in this area is most advanced using the endosymbiont Wolbachia where experimental releases in a mosquito have already occurred in Australia . Our experience in the application of drive mechanisms to important problems puts us in an excellent position to capitalise on any relevant findings that come out of our research on aphid endosymbionts. Were new finding relevant endosymbiont drive to occur we would work with a company called Oxitec which was spun out of the Zoology Department to commercialise a technology called RIDL (a genetic-form of sterile insect release) but which has broader interests in novel molecular means of pest and vector control.

The general public

Everyone knows what an aphid is and they are thus a great system to engage the public in modern ecology and evolution. The PI speaks regularly at Cheltenham Science Festival and in other forums for public engagement and will include the research in his talks.

Publications


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Hrcek J (2015) What do molecular methods bring to host-parasitoid food webs? in Trends in parasitology
Lukasik P (2015) Horizontal transfer of facultative endosymbionts is limited by host relatedness. in Evolution; international journal of organic evolution
McLean AH (2016) Insect symbionts in food webs. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
McLean AH (2015) Evidence for specificity in symbiont-conferred protection against parasitoids. in Proceedings. Biological sciences
 
Description Eukaryotes commonly host communities of heritable symbiotic bacteria many of which are not essential for their hosts' survival and reproduction. There is laboratory evidence that such facultative symbionts can provide useful adaptations, such as increased resistance to natural enemies. However, we do not know how symbionts affect host fitness when the latter are subject to attack by a natural suite of parasites and pathogens. As part of this project we conducted a replicated, controlled field experiments to test whether two protective symbionts, Regiella insecticola and Hamiltonella defensa, increase the fitness of their host, the pea aphid (Acyrthosiphon pisum), under natural conditions. We found that both Regiella and Hamiltonella reduce the proportion of aphids killed by the specific natural enemies identified in laboratory and cage experiments. However, this advantage was nullified (Hamiltonella) or reversed (Regiella) by an increase in mortality from other natural enemies and by the cost of carrying the symbiont. Our work suggests that these protective symbionts may be behaving more like parasites than mutualists, challenging the model of symbionts as a "horizontal gene pool" from which hosts can draw useful adaptations. We also show that symbionts influence community structure by altering the relative success of different natural enemies. We conclude that bacterial symbionts may play an important role in determining food web structure and dynamics.
Exploitation Route We are currently exploring how the presence of the symbiont may affect aphid host plant utilisation or their capacity to transmit viral diseases
Sectors Agriculture, Food and Drink,Environment