Parasite spillover rather than niche expansion explains infection of host brain by diplostomid eye flukes.

Abstract

Parasites often occupy specific sites within their host, which has important implications for host performance and parasite transmission. Nonetheless, parasitic infections can occur beyond their typical location within a host, significantly altering host-parasite interactions. Yet, the causes behind the atypical tissue tropism are poorly understood. Here, we focus on a ubiquitous group of diplostomid parasites that form diverse communities in fish eyes. We used targeted DNA metabarcoding (cytochrome c oxydase subunit 1, COX1, 250 bp) to evaluate potential mechanisms underlying eye parasite atypical tissue tropism to the brain of two widespread fish species (Eurasian perch and common roach). We found that the most common eye-infecting species (Tylodelphys clavata, Diplostomum baeri) are present in the brains of perch but not in roach. The bipartite network comprising 5 species and 24 mitochondrial haplotypes revealed no brain-specific haplotypes, indicating an apparent lack of genetic divergence between brain- and eye-infecting parasites. Instead, the prevalence, intensity and diversity of eye infections were positively correlated with brain infections. Thus, our results suggest that the most parsimonious mechanism underlying brain infection is density-dependent spillover rather than parasite divergence-driven niche expansion. We anticipate that 'off-target' infections are likely to be severely underestimated in nature with important ecological, evolutionary and medical implications.