Population genetic analysis reveals the role of natural selection and phylogeography on genome-wide diversity in an extremely compact and reduced microsporidian genome
Authors: Angst Pascal , Ebert Dieter , Fields Peter D. 
Published: March 2022

The determinants of variation in a species’ genome-wide nucleotide diversity include historical, environmental, and stochastic aspects. This diversity can inform us about the species’ past and present evolutionary dynamics. In parasites, the mode of transmission and the interactions with the host might supersede the effects of these aspects in shaping parasite genomic diversity. We used genomic samples from ten populations of the microsporidian parasiteOrdospora colligatato investigate present genomic diversity and how it was shaped by evolutionary processes, specifically, the role of phylogeography, co-phylogeography (with the host), natural selection, and transmission mode. Although very closely related microsporidia cause diseases in humans,O. colligatais specific to the freshwater crustaceanDaphnia magnaand has one of the smallest known eukaryotic genomes. We found an overlapping phylogeography betweenO. colligataand its host highlighting the long-term, intimate relationship between them. The observed geographic distribution reflects previous findings thatO. colligataexhibits adaptations to colder habitats, which differentiates it from other microsporidian gut parasites ofD. magnapredominantly found in warmer areas. The co-phylogeography allowed us to calibrate theO. colligataphylogeny and thus estimate its mutation rate. We found patterns of more efficient purifying selection inO. colligatarelative to other microsporidia sharing the same host, which likely allowed this parasite to maintain its very compact genome. We also identified regions under potential selection related to coevolution including the ribosomal protein L24, a leucyl-tRNA synthetase, and a putative ABC-like lipid transport protein. Our whole-genome study provides insights into the evolution of one of the most reduced eukaryotic genomes and shows how different processes shape genomic diversity of an obligate parasite.

Author summary

Microsporidia are intracellular parasites that infect vertebrates, invertebrates, and even unicellular organisms. Due to their high variation in many aspects of life history and genomics, microsporidia have become a model clade for understanding evolutionary processes related to intracellular parasitism. However, the evolution of extreme genomic architectures in microsporidia and the coevolution with their hosts is still under-surveyed, especially given their role in human disease. Here, we study past and present evolutionary dynamics in a microsporidian species with one of the smallest known eukaryotic genomes,O. colligata. Close relatives ofO. colligatacause death and disease in humans and agriculturally important animals. We show that purifying selection helped maintaining its reduced, compact genome and corroborate hypotheses about the evolution of different genome sizes in microsporidia. Importantly, we utilize the highly resolved phylogeny of its host to estimate the parasite’s mutation rate. This methodology allowed us to establish the first mutation rate estimate for a microsporidium, an estimate which is within the range of mutation rates estimated for phylogenetically related, non-parasitic fungi. Our study exemplifies how the combined knowledge about a species’ biology, ecology, and genomic diversity helps to resolve its evolutionary dynamics, in particular when phylogenomic information can be brought to bear for both host and parasite.