The genetic basis of adaptive behavioural traits in a global crop pest Myzus persicae (Sulzer)

Myzus persicae is the most economically important aphid pest in temperate regions of the world causing damage to a range of food and commodity crops. This species is highly adaptable and attempts to control M. persicae using chemical insecticides have led to the evolution of resistance – with at least eight genetically distinct mechanisms described to date. In addition to variation in sensitivity to insecticides different genotypes of M. persicae exhibit variation in a range of other traits. These include behavioural traits, such as response to alarm pheromone, predator threat or insecticide presence. Additionally, in certain cases variation in these traits has been associated with genetic alterations that confer insecticide resistance, revealing potential fitness costs associated with resistance. Despite previous studies the extent of variation in behavioural traits within and between different genotypes of M. persicae, the link with insecticide resistance, and their genetic control is poorly understood. To address this knowledge gap, 110 genetically distinct clonal lines of M. persicae were examined for variation in behavioural responses to three external stimuli with behavioural variation analysed against genomic and transcriptomic variation between clones. Pheromone behavioural assays provided clear evidence that genetically distinct clones of M. persicae vary in their response to (E)-β-Farnesene. Marked variation was observed between high responding clones (>60% total response) and low responding clones (<3% total response). High responders remained consistently responsive in pheromone assays, regardless of alarm pheromone concentration. Moreover, with increasing concentrations lower responding clones remained significantly less responsive. Non-consumptive predation behavioural assays also demonstrated marked variation between clones of M. persicae in both behavioural categories assessed (walking and dropping). Interestingly, intra-clonal variation was observed in both EβF and predator assays however, repeatability of behaviour was only significant for dropping behaviour in predator assays. To understand the genetic control of the measurable behavioural variation between clones of M. persicae, insecticide resistance mechanisms were initially analysed. Links with insecticide resistance alleles identified clear positive associations with walking response and dropping response in both EβF and predation behavioural assays. L1014F (kdr) resistance in both heterozygous and homozygous states was significantly associated with increased responsiveness (P < 0.001). MACE resistance showed significant association with an increase in both walking and dropping behaviours in non-consumptive predator assays, although was only measured for heterozygous resistant clones. Indeed, L1014F resistance was also associated with an increase in walking and dropping behaviour. Conversely, only one resistance mechanism was associated with a decreased behavioural response. M. persicae clones with the skdr mutation M918L, showed a small but significant reduction in walking behaviour in EβF assays. Genome-wide association studies and transcriptomic analysis pooled behaviours into trait categories with each behavioural assay providing separate traits (three behavioural traits included overall). Although a clear association with L1014F resistance was not achieved in this study, several candidate genes linked to behavioural variation were discovered. GWAS identified a clear association with octopamine reception and transcriptomic analysis with odorant binding proteins with both types of genes linked to increased dropping behaviour in M. persicae. Indeed, high responding clones overexpressed 3 out of 7 odorant binding proteins compared to low responding clones. Additionally, a significant association with a gene regulating locomotor rhythm aligned with an increase in walking response from M. persicae clones in EβF behavioural assays. From the data generated in this thesis, marked variation between clonal populations of M. persicae when presented with stimuli that elicits adaptive behavioural responses is clear both between and within clones. The identification of proximate candidate mechanisms underlying behavioural variation in M. persicae shed light on the adaptive potential of the species. Moreover, the data obtained contribute to the understanding of behavioural adaptation in invertebrates providing a foundation for future research