The evolution of pathogen defence in insect hosts: whitefly resistance to biocontrol agents in horticulture


Explore the extraordinarily dynamic coevolution between hosts, pathogens and intracellular symbionts, and help apply this new knowledge to improve the sustainability of modern agriculture.

The control of insect pests in agriculture using conventional chemical insecticides has led to widespread insecticide resistance evolution and triggered extensive biodiversity loss. In response to these problems many agricultural sectors are increasingly switching to biological control agents (such as pathogens and parasitoids) as part of an integrated pest management approach. However, in contrast to the volume of research into chemical insecticide resistance, the possibility that target pests may evolve resistance to these biological control agents has received relatively little attention.

Insect populations harbour substantial genetic variation for infection susceptibility, providing strong potential for resistance evolution [1]. Evolutionary responses to parasites are often assumed to be due to changes in components of the immune system coded for by the nuclear genome. However, other factors often strongly influence the susceptibility of insect hosts to infection and may provide novel routes to resistance evolution. For example, behaviour can have major impacts on infection susceptibility [2]: insects that avoid contact with parasites may be at a significant evolutionary advantage. Also, insect resistance to parasitism is often strongly influenced by the presence of maternally inherited symbiotic microbes that live inside the insect’s tissues: these “influential passengers” can be the principal determinant of infection susceptibility in many systems, meaning that resistance can evolve through the spread of a novel symbiont rather than via genomic evolution [3].

The glasshouse whitefly Trialeurodes vaporariorum is a major pest of agriculture worldwide; in the UK it especially affects greenhouse horticulture. It damages plants by removing resources through sap-sucking, depositing honeydew on foliage thereby promoting fungal growth and by vectoring a range of viral infections. This insect is particularly problematic for commercial greenhouse tomato growers in the UK; growers deploy a range of control agents against whitefly, two of which are the parasitoid wasp Encarsia formosa and biopesticides formulated from the entomopathogenic fungus Beauveria bassiana. Whilst agricultural monocultures can rapidly select for resistance phenotypes in pests, we are especially interested in how ecological heterogeneity can be enhanced in horticulture by planting multiple plant species/varieties and whether this can impede resistance evolution.

This PhD aims to investigate the extent to which Trialeurodes vaporariorum may be able to evolve resistance to parasitoids and pathogens used as biocontrol agents. It will assess the contribution of symbiotic microbes and behavioural factors influencing infection risk to overall parasitism susceptibility. Furthermore, the project will investigate the potential efficacy of strategies to mitigate the risk of resistance evolution by elevating crop plant heterogeneity in commercial glasshouse horticulture systems.
The PhD will combine field work in the UK with laboratory work at Stirling University in collaboration with Newcastle University. Depending on the project direction and applicant interests we will also encourage overseas fieldwork with our research partners in Kenya or Brazil

The precise objectives of this PhD are flexible and could be tailored around the interests and expertise of the applicant. The following outline represents one potential integrated programme of research. The project could either focus on host responses to fungal biocontrol agents, or to parasitoid wasps, or a combination of both.

Research Questions:

(1) To what extent do host genotype and symbiont infection status influence whitefly natural enemy resistance?

(2) Is the spatial ecology of symbiotic microbes infecting whitefly influenced by the use of biocontrol agents in horticulture?

(3) Do whitefly behavioural changes in response to horticultural crop plant heterogeneity alter whitefly exposure
and susceptibility to biocontrol agents?

(4) Does crop plant heterogeneity influence the intensity of selection for whitefly resistance to natural enemies?

Click on an image to expand

Image Captions

Whitefly nymphs and adults on a leaf; Whitefly nymphs being attacked by a parasitoid wasp using in biocontrol.


Whitefly will be collected from horticultural glasshouse farms (principally tomato growers) in the UK and then maintained in culture at Stirling.

Multiple matrilines of whitefly will be established in the lab and their resistance to fungal biopesticides and/or parasitoid wasps assessed to quantify the extent of genetic variation for resistance. We can exploit quantitative genetic breeding designs to partition how resistance variation is influenced by nuclear genetic variation and symbiont infection status.

Field collected and lab whitefly will be tested to determine their infection status by common symbiotic microbes (eg Hamiltonella, Arsenophonous, Rickettsia, Wolbachia, Cardinium) using DNA extraction, PCR amplification and sequencing; this will enable tests to assess whether the intensity of biocontrol use at a given horticultural farm influences symbiont prevalence.

Agricultural crop plant heterogeneity can increase adult whitefly ‘restlessness’, increasing movement [4]. This phenomenon may be driven by the ‘confusion effect’ created by the mix of plant volatiles from multiple crops [5]. This project will undertake behavioural tests to investigate whether increased adult movement and potentially altered oviposition behaviour increases the exposure of adults or nymphs to biocontrol agents thereby enhancing the efficacy of pest control. These tests will begin in the laboratory but could be scaled up to ‘greenhouse’ scale through trials based with our commercial contacts.

Finally, the project will test for the evolutionary consequences of crop plant heterogeneity in horticultural environments, by investigating whether heterogeneity alters selection pressures for resistance evolution. This could take a number of approaches: eg. (a) investigate whether the host genotype/symbiont that confers highest resistance varies according to the host plant on which the insect feeds; (2) study whether whiteflies collected from farms with different histories of crop cultivation practice / biocontrol use differ in their behavioural responses and/or resistance to biocontrol agents (fieldwork could involve comparisons between populations from different horticultural farms in the UK, or comparisons between whitefly from different countries).

Project Timeline

Year 1

This 3.5 year studentship will begin with 6 months for project planning, literature review and training in key lab skills for working with whitefly and biocontrol agents. During the early summer, fieldwork will begin to address research questions 1 & 2 by collecting whitefly across the UK at horticultural farms whilst making records of the biocontrol agents used at each location. Lab tests of biocontrol agent susceptibility will follow.

Year 2

The project will move on to test the symbiont infection status of whitefly using PCR. The student will undertake statistical training and perform data analysis, followed by manuscript write up and paper submission for research questions (1) and (2).

Year 3

The project will address research questions (3) and (4) investigating the impact of ecological heterogeneity and whitefly behaviour on infection resistance under lab mesocosm conditions with potential opportunities to scale up experiments.

Year 3.5

Final thesis write up and submission.

& Skills

This PhD will principally be based in a vibrant multidisciplinary research environment at the University of Stirling. The PhD student will become a member of the ‘Evolving Organisms’ research group and will be able to attend regular lab group meetings, along with weekly seminar series giving informal and formal opportunities for research presentation. A core part of the PhD will be visits to Newcastle University to engage in collaborative research, with particular focus on the behavioural aspects of the project proposal.

The candidate will receive training in subject specific and generic skills. These will include: insect culture, experimentation and infection assays; behavioural tests on responses to plant stimuli; field sampling; advanced statistics (Stirling R course and other IAPETUS2 training); molecular biology protocols of DNA extraction, PCR, sequencing etc for symbiont identification.

The candidate will be expected to participate in training opportunities in a range of research and transferable skills offered at Stirling University and through the IAPETUS2 DTP.

Training will be given in scientific communication skills (both writing and conference presentation) so that the candidate can successfully publish research papers and attend conferences during the PhD.

References & further reading

You can find out more about our research work investigating how ecological heterogeneity in agroecosystems can limit the evolution of resistance to pest control interventions here:

[1] Tinsley MC, Blanford S, Jiggins FM. (2006). Genetic variation in Drosophila melanogaster pathogen susceptibility. Parasitology 132: 767–773.

[2] Sarabian C, Curtis V, McMullan R. (2018). Evolution of pathogen and parasite avoidance behaviour. Philos Trans R Soc Lond B Biol Sci. 19: 373(1751): 20170256.

[3] Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ. (2010). Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329: 212–215.

[4] Bernays EA. (1999). When host choice is a problem for a generalist herbivore: experiments with the whitefly, Bemisia tabaci. Ecological Entomology, 24: 260-267.

[5] Tosh CR, Brogan B. (2015). Control of tomato whiteflies using the confusion effect of plant odours. Agron. Sustain. Dev.  35: 183-193.

Further Information

Please contact Matt Tinsley ( to ask questions, gain further information and to make an informal application.

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