Stress responses are key for parasite survival and, consequently, also the evolutionary success of these organisms. Despite this importance, our understanding of the molecular pathways dealing with environmental stressors remains limited for parasitic animals. Here, we targeted the molecular pathways dealing with environmental stressors and comparatively investigated antioxidant, heat shock, osmoregulatory, and behaviour-related genes (foraging) in two parasitic flatworm lineages with contrasting species and ecological diversity, Cichlidogyrus and Kapentagyrus (Platyhelminthes: Monogenea), through whole-genome sequencing of 11 species. Using an in silico exon bait capture approach, we assembled the sequences of 48 stress-related genes and report the first foraging (for) gene orthologs in flatworms. We found duplications of heat shock- (hsp) and oxidative stress genes in Cichlidogyrus compared to Kapentagyrus. We also observed positive selection patterns in genes related to mitochondrial protein import (hsp) and behaviour (for) in species of Cichlidogyrus infecting East African cichlids—a host lineage under adaptive radiation—consistent with a potential adaptation linked to a co-radiation of parasites and hosts. Accordingly, this study potentially identifies the first molecular function 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 considered essential for metazoan life.

Many species-rich ecological communities result from adaptive radiation events. The effects of these explosive speciation events on community assembly remain poorly understood. Here, we explore the well-documented radiations of African cichlid fishes and interactions with their flatworm gill parasites (Cichlidogyrus spp.) including 10529 reported infections and 477 different host-parasite combinations collected through a survey of peer-reviewed literature. We assess the evolutionary, ecological, and morphological parameters on meta-communities partially affected by adaptive radiation evens using network metrics, host repertoire measures, and network link prediction (NLP). The hosts’ evolutionary history mostly determined host repertoires. Ecological and evolutionary parameters predicted host-parasite associations, but many interactions remain undetected according to NLP. Parasite meta-communities under host adaptive radiation are more specialised and stable while ecological opportunity and ecological fitting have shaped interactions elsewhere. The cichlid-Cichlidogyrus network is a suitable eco-evolutionary study system but future studies should validate our findings in other radiating host-parasite systems.

Hosts and parasites have often intimate associations. Therefore, the evolution of their interactions is crucial for understanding species-rich host-parasite communities. Yet relatively few studies investigate eco-evolutionary feedbacks in these systems as large datasets remain scarce. Here, we explore African cichlid fishes and their flatworm gill parasites (Cichlidogyrus spp.) including 9901 reported infections and 473 different host-parasite combinations collected through a survey of peer-reviewed literature. We apply network metrics, estimate host repertoires, and use network link prediction (NLP) algorithms to investigate meta-community structures and their predictors including evolutionary, ecological, and morphological parameters. Host repertoire was mostly determined by the hosts’ evolutionary history. Both ecological and evolutionary parameters predicted host parasite associations but many interactions remain undetected according to NLP. We conclude that ecological opportunity paired with ecological fitting has shaped interactions. The cichlid-Cichlidogyrus network is a suitable study system for eco-evolutionary feedbacks but taxonomic research remains key to finding undetected interactions.