Parasites often manipulate host phenotypes to facilitate their own transmission. Wood ants, Formica aserva, infected with larvae of the lancet liver fluke, Dicrocoelium dendriticum, leave their nests during the cool hours of the day to ascend and attached to a plant, where they remain overnight, and detach the next morning when temperatures rise returning to their nest. They repeat this bizarre attachment and detachment sequence for the rest of the summer. My thesis seeks to understand the molecular mechanisms that underlie this complex manipulation of host behaviour that is ‘on-then-off’ through metabolomics and transcriptomics approaches.
I first characterized changes in the metabolite concentrations in ant brains collected from a site of D. dendriticum emergence in southern Alberta, Canada. Within the laboratory, I recreated the manipulation cycle to mimic pre-attached, attached, and post-attached stages, and sampled infected and uninfected ant brains from each stage. Mean brain concentration of neurotransmitters tyramine and serotonin were reduced in infected ants compared to uninfected during detachment phases by 22% and 17%, respectively. These reductions paralleled a 40% reduction in overall host activity in infected versus uninfected ants during the detachment phase.
I then compared the gene expression pattern of brains from infected and uninfected ants at the same samples stages as above. I found that 13,556 genes were differentially expressed, including those involved in environmental sensing and the production of biogenic monoamines. I found genes involved in odorant and vision were downregulated in attached infected ants. Vision genes were upregulated in post-attached infected ants compared to uninfected controls. Genes involved in serotonin synthesis were also downregulated during the post-attached stages in infected ants. These results support that the regulation of biogenic monoamines in the brains of infected ants plays a role in this complex manipulation of host behaviour.
Overall, this study helps us better understand how D. dendriticum manipulates their ant host behaviour. My findings show that the mechanisms driving reversible manipulations is more complex than the parasite-induced control of ‘on-then-off’ triggers. In the D. dendriticum-ant system, different mechanisms are involved at different stages of the manipulation
