Solving the mystery of ergot evolution

Despite having over 100 million years of historical evidence as a parasitic eukaryote, studies for Claviceps have yet to provide answers for its evolution and ancestral origins. In 2017, a study by Pichova et. al. analysed the genome sequences of 43 Claviceps spp. along with 15 related taxa. From this, the authors constructed several phylogenies via a range of computational methods: Bayesian binary method (BBM), maximum likelihood (ML) and maximum parsimony (MP). These differ in their approach to the construction of an “optimal” phylogenetic tree, and whether or not they account for evolutionary events like reversals, convergence and homoplasy which can lead to false positives.

Using three of the five loci above, Pichova and the researchers generated another phylogeny using molecular dating. This gave a visualisation of the time points at which Claviceps diverged throughout history.

Frustratingly, they found that contrary to existing classification schemes some Claviceps species overlapped with ecologically non-related taxa. Furthermore, no method produced results that could be supported statistically.

They hence decided to compromise with the traditionally accepted classification of Claviceps as a genus distinct from Aciculosporium, Cepsiclava and Neoclaviceps and the other taxa analysed. However they did find deep divergences between four distinct lineages or “sections”, with economically significant species C. africana, C. paspali and C. purpurea classified separately into three of these four sections. C. citrina appeared to be an outlier, being the only analysed species in its own section, however omitting it from the results did not resolve the issues with statistical support.

The distinction of these sections indicate that Claviceps as a genus is not as homogenous as previously thought. More interestingly, this would mean that characteristics such as a parasitic lifestyle and host interactions may differ from species to species.

“[Ergot’s] evolutionary history was primarily driven by the evolution and diversification of its hosts and the encountering of potential new host plants after spreading to new geographic areas. This resulted in deep diversification into four lineages of ergot that are distant enough that they can be treated as distinct genera.”

By analysing each species’ geographic distribution and host range, they also found that Claviceps originated in South America, and its ancestral host was the sedge (a type of grass). It appears that ergot evolution is mainly driven by diversification of its hosts and encountering potential new host plants after geographic spread. This is supported by their analysis of ergot alkaloid production in species not well characterised yet; they found that the parasitic ancestors of Claviceps, Aciculosporium and Corallocytostroma showed no traces of alkaloid production. Why then, did alkaloid production emerge in Claviceps?

As host-microorganism interactions occur on a spectrum, it may be explained by a shift from host parasitism to the protection of mutualistic endophytes, particularly other endophytes that produced alkaloids. Such alkaloids can be considered agents for preventing predation by herbivores, and thus their production may be driven by selective pressures on the host.

Graphical abstract.

References:

Píchová, K., Pažoutová, S., Kostovčík, M., Chudíčková, M., Stodůlková, E., Novák, P., … Kolařík, M. (2018). Evolutionary history of ergot with a new infrageneric classification (Hypocreales: Clavicipitaceae: Claviceps). Molecular Phylogenetics and Evolution, 123, 73–87. https://doi.org/10.1016/j.ympev.2018.02.013