Rapid speciation in host lineage may lead to adaptive evolution of parasites’ stress response genes in monopisthocotylan flatworms

Stress responses are key for parasite survival and, thus, also the evolutionary success of these organisms. However, a strong bias in parasite genomic research towards few human pathogens results in a lack of knowledge on evolutionary diversification mechanisms. Comparative studies of closely related and functionally similar lineages are the key for understanding factors driving adaptive evolution of stress responses. To address this knowledge gap, we contrasted evolutionary patterns of several antioxidant, heat shock, osmoregulatory, and behaviour-related genes in two fish parasitic flatworm lineages with varying species and ecological diversity, Cichlidogyrus and Kapentagyrus (Monopisthocotyla). We assembled the sequences of 48 genes related to stress responses in 11 species through an in-silico exon bait capture approach, applied phylogenetic reconstruction and tested for signatures of selection. The study also reports the first foraging (For) gene orthologs in flatworms. Additionally, the absence of cytochrome P450 (Cyp) and kappa (Gstk) and sigma-class glutathione S-transferases (Gsts) in monopisthocotylan flatworms is reported, genes typically considered essential for metazoan life. The results reveal copy number differences in heat shock (Hsp) and oxidative stress genes between the two parasite lineages potentially linked to the diversity of ecological niches occupied by their respective host taxa. Positive selection is detected in genes related to mitochondrial protein import (Hsp) and behaviour (For) in species of Cichlidogyrus infecting a host lineage under adaptive radiation (East African cichlids), suggesting an adaptive link to a putative co-radiation of parasites and hosts. Therefore, the study identifies the first potential molecular function linked to a flatworm radiation.