Adaptive evolution of stress response genes in two monogenean parasite lineages aligns with their respective host niche diversity

Abstract

Stress responses are crucial for parasite survival and, consequently, contribute to the evolutionary success of these organisms. However, the evolution of the molecular pathways dealing with environmental stressors is poorly understood in parasites. A notable bias in parasite genomic research towards few health-relevant human pathogens results in a lack of DNA and RNA sequence data and limiting knowledge of diversification mechanisms among wildlife parasites. Comparative studies of closely related and functionally similar lineages of species-rich wildlife parasite taxa might provide insight into the factors driving adaptive evolution of stress responses. To address this knowledge gap, we comparatively investigated antioxidant, heat shock, osmoregulatory, and behaviour-related genes (foraging) in the two parasitic flatworm lineages with varying species and ecological diversity, Cichlidogyrus and Kapentagyrus (Platyhelminthes: Monogenea), through whole-genome sequencing of 11 species. We assembled the sequences of 48 stress-related genes using an exon bait capture approach. The study reports the first foraging (for) gene orthologs in flatworms. We also discovered that species of Cichlidogyrus present gene duplications of heat shock (hsp) and oxidative stress genes compared to Kapentagyrus. This difference might be linked to the high ecological diversity of the host lineage of Cichlidogyrus (African cichlid fishes), unlike the ecologically conserved niches of the hosts of species of Kapentagyrus (African freshwater sardines). Positively selected sites were detected in genes related to mitochondrial protein import (hsp) and behaviour (for) in species of Cichlidogyrus infecting a host lineage undergoing 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 functions linked to a flatworm radiation. Additionally, the absence of cytochrome P450 and kappa and sigma-class glutathione S-transferases in monogenean flatworms is reported, genes typically considered essential for metazoan life.