Adaptive evolution of stress response genes in parasites aligns with host niche diversity

By: Armando J. Cruz-Laufer, Maarten P. M. Vanhove, Lutz Bachmann, Maxwell Barson, Hassan Bassirou, Arnold R. Bitja Nyom, Mare Geraerts, Christoph Hahn, Tine Huyse, Gyrhaiss Kapepula Kasembele, Samuel Njom, Philipp Resl, Karen Smeets & Nikol Kmentová

Parasites are some of the most abundant organisms on the planet, some of them of high importance for human health. Knowing what makes parasites successful should, therefore, be a priority. But we know surprisingly little about them. How can parasites adapt to new environments and hosts? What are the molecular tools to deal with environmental stressors?

In our study, we investigated the evolution of genes involved in the stress response of two lineages of flatworm parasites that infect the gills of fishes in Africa. Stress response genes code for different proteins that allow the parasite to deal with environmental stressors such as heat, salinity, reactive oxygen species, and the immune responses of their hosts. We selected two lineages of gill parasites whose host lineages experience very different variation of environmental conditions and, therefore, also environmental stressors (Fig. 1). Species of Cichlidogyrus are parasites that infect cichlid fishes, a species-rich group of fishes with diverse lifestyles (river vs. lakes, shoreline vs. deep water, predators vs. herbivores, etc.). Cichlid fishes in East Africa are particularly diverse, forming hundreds of species that each occupy a specific ecological niche in the lakes of this region. Species of Kapentagyrus are the opposite. They infect African freshwater sardines, a species of poor group with a similar lifestyle. We expected parasites infecting the ecologically diverse hosts to be inherently more adaptable than those infecting the hosts with a more conservative lifestyle.

Figure 1. The two flatworm parasite lineages Cichlidogyrus and Kapentagyrus differ substantially in species richness and host diversity. Species of Cichlidogyrus infect the gills of the hyperdiverse African cichlid fishes that include the adaptive radiations of Lake Tanganyika in East Africa.  Species of Kapentagyrus infect the gills of African freshwater clupeid fishes, an ecologically conserved group of 22 species inhabiting only pelagic environments of lakes and rivers. Based on these differences, we hypothesise that stress responses of Cichlidogyrus have adapted to the enhanced ecological diversity of their hosts

What did we find?

We targeted overall 29 different stress genes in 11 species (9 species of Cichlidogyrus and 2 of Kapentagyrus). We found that particularly in genes involved in heat shock responses, species of Cichlidogyrus had more copies than species of Kapentagyrus. This means that, as we predicted, the parasites with ecologically diverse hosts might be more adapted to different environmental conditions. We also found signs that parts of some stress genes are shaped by natural selection in the parasites infecting fishes in East African lakes. This can be seen as a sign of adaptive evolution in these regions of the parasite’s DNA. The genes in question are involved in mitochondrial protein import, meaning they help move protein molecules in the part of cell that is responsible for energy production.

Bathybates minor, one of the many ecologically diverse species of cichlid fishes in East Africa that are hosts of parasites belonging to Cichlidogyrus." Image credit: Wolfgang Gessl (https://pisces.at)

We interpret this as an initial indication that the East African species of Cichlidogyrus have adapted this specific mechanism to adapt to deal with the enormous diversity of the fish in the lake. While more research is needed to understand how exactly these stress genes help the parasites deal with stress, this discovery is important as it gives us the first insight into how parasites can ultimately adapt to changing environments and possibly new host species.

This research would not have been possible without the infrastructure provided by the VSC. To obtain the sequences of the stress genes, we processed hundreds of GBs of genomic data using a range of bioinformatic tools. Parallelising these tools enabled us to efficiently assemble the sequences of not only the 29 stress genes but also hundreds of additional DNA sequences that were needed as background data.

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Read the full article in BMC Biology here