Parasite induced changes in neuronal activity : is the parasitic eye-fluke (Diplostomum spp.) manipulating its Arctic charr (Salvelinus alpinus) host?

Abstract

Many parasites possess complex lifecycles and depend on several host species to complete their lifecycle. Some parasites even manipulate their hosts phenotype in a way that facilitates trophic transmission to their final host (i.e., parasite-induced trophic transmission; PITT) in order to complete their life cycle. The parasitic eye-fluke (Diplostomum spp.) has the Arctic charr (Salvelinus alpinus) as its second intermediate host where it establishes within the eyes and develops into metacercaria. For the eye-fluke to complete its life cycle and successfully reproduce, it depends on trophic transmission to a bird final host. Which means, the fish must be eaten by a bird. The physiological effects Diplostomum spp. infection might have on the Arctic charr and the possible effects on the fish’s phenotype (e.g., coloration and behavior) is largely unknown. The aim of this study was to investigate the effects of Diplostomum spp. infection on neuronal activity and gene expression in the arctic charr. By quantification of immunohistochemistry for the neuronal activity marker phosphorylated Extracellular signal Regulated Kinase (pERK) a significantly lower neuronal activity was observed in the tuberal nucleus of the hypothalamus in arctic charr with high eye-fluke infection. Further RNA sequencing revealed an upregulation of gonadotropin-releasing hormone-3 (GnRH-3) and luteinizing hormone sub-unit  (LH) in heavily infected fish. These genes are involved in the hypothalamic-pituitary-gonadal (HPG) axis and serves as major regulatory genes in reproduction and steroid hormone production. Increased investment in reproduction is associated with a more conspicuous phenotype (i.e., bright coloration, courting behavior and risk-taking behavior) which is linked to increased mortality by predation. For the parasite awaiting trophic transmission to its final host, interfering with the HPG-axis might be an effective way for the eye-fluke to indirectly influence the phenotype of the fish in a way that facilitates PITT. Further investigations are required to get a better understanding of the underlying physiological mechanisms involved in the potential phenotypic changes caused by Diplostomum spp. infection in the Arctic charr.