Geography, phylogeny and host switch drive the co-evolution of parasitic Gyrodactylus flatworms and their hosts

Abstract

Abstract Background: Gyrodactylus is a lineage of monogenean flatworm ectoparasites exhibiting many features that make them a suitable model to study the host-parasite co-evolutionary dynamics. Previous co-evolutionary studies of this lineage mainly relied on low-power datasets (a small number of samples and a single molecular marker), and (now) outdated algorithms. Methods: To investigate the coevolutionary relationship of gyrodactylids and their fish hosts in high resolution, we used complete mitogenomes (including two newly sequenced Gyrodactylus species), a large number of species in the single-gene dataset, and four different coevolutionary algorithms. Results: The overall co-evolutionary fit between the parasites and hosts was consistently significant. Multiple indicators support gyrodactylids as highly host-specific parasites, but few gyrodactylids can parasitize either multiple (more than 5) or phylogenetically-distant fish hosts. The molecular dating results indicate they tend to evolve towards high host specificity. Speciation by host-switching is a more important speciation mode than co-speciation for them. Assuming the origin on Cypriniformes, we inferred four major host switch events to non-Cypriniformes hosts (mostly Salmoniformes) occurred deep in the evolutionary history. Despite their relative rarity, these events had strong macroevolutionary consequences for gyrodactylid diversity. For example, in our dataset, 57.28% of all studied gyrodactylids parasitised only non-Cypriniformes hosts, which implies that the evolutionary history of more than half of all included lineages could be traced back to these major host switch events. The geographical co-occurrence of fishes and gyrodactylids determined the host use by these gyrodactylids, and geography accounted for most of the phylogenetic signal in host use. Conclusions: In a sentence, our findings suggest that the co-evolution of Gyrodactylus flatworms and their hosts is largely driven by geography, phylogeny, and host switches.