Shifts in diversification rates and host jump frequencies shaped the diversity of host range among Sclerotiniaceae fungal plant pathogens

Abstract

The range of hosts that a parasite can infect in nature is a trait determined by its own evolutionary history and that of its potential hosts. However, knowledge on host range diversity and evolution at the family level is often lacking. Here, we investigate host range variation and diversification trends within the Sclerotiniaceae, a family of Ascomycete fungi. Using a phylogenetic framework, we associate diversification rates, the frequency of host jump events and host range variation during the evolution of this family. Variations in diversification rate during the evolution of the Sclerotiniaceae define three major macro-evolutionary regimes with contrasted proportions of species infecting a broad range of hosts. Host-parasite cophylogenetic analyses pointed towards parasite radiation on distant hosts long after host speciation (host jump or duplication events) as the dominant mode of association with plants in the Sclerotiniaceae. The intermediate macro-evolutionary regime showed a low diversification rate, high frequency of duplication events and the highest proportion of broad host range species. Our findings suggest that the emergence of broad host range fungal pathogens results largely from host jumps, as previously reported for oomycete parasites, probably combined with low speciation rates. These results have important implications for our understanding of fungal parasites evolution and are of particular relevance for the durable management of disease epidemics.

Keywords: angiosperms; coevolution; fungi; host parasite interactions.

Figure 1

Multiple independent shifts and expansions of host range in the evolution of the Sclerotiniaceae. (a) Distribution of plant hosts of parasites from the Sclerotiniaceae and Rutstroemiaceae fungi. (b) Maximum‐likelihood ITS phylogeny of 105 Sclerotiniaceae and 56 Rutstroemiaceae species showing host range information and ancestral host reconstruction. Host range is shown as circles at the tips of branches, sized according to the number of host families and coloured as in (a) according to the earliest diverging plant group in host range. Numbers at the tips of branches refer to species listed in Table S1. Branch support indicated in light red for major clades corresponds to SH‐aLRT (regular), bootstrap (bold) and Bayesian posterior probabilities (italics). Reconstructed ancestral host is shown as triangles at intermediate nodes when a change compared to the previous node is predicted. Endophytes and biotrophic parasites are shown with empty circles. (c) Distribution of Sclerotiniaceae and Rutstroemiaceae species according to their number of host families [Colour figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Two major diversification rate shifts in the evolution of the Sclerotiniaceae. (a) Dated ITS‐based species tree for the Sclerotiniaceae with diversification rate estimates. The divergence times correspond to the mean posterior estimate of their age in millions of years calculated with beast. Mean age is shown for selected nodes with bars showing 95% confidence interval of the highest posterior density (HPD). Branches of the tree are colour‐coded according to diversification rates determined with BAMM. Major rate shifts identified in BAMM are shown as red circles, noted s ₁, $s_1^{\prime }$, s ₂ and $s_2^{\prime }$ and labelled with the posterior distribution in the 95% credible set of macro‐evolutionary shift configurations. Species names are shown in black if host range includes less than five plant families, in yellow for five to nine plant families and in red for 10 or more plant families. Diversification rate shifts define three macro‐evolutionary regimes noted G1, G2 and G3 and boxed in blue, grey and brown, respectively. (b) Distribution of broad host range (five or more host families) parasites in Rutstroemiaceae, Sclerotiniaceae and under each macro‐evolutionary regime of the Sclerotiniaceae. p‐Values calculated by random permutations of host ranges along the tree are indicated above bars. Holo., Holocene; Mya, Million years ago; Plei., Pleistocene; Plio., Pliocene; Quat. Quaternary; Rut., Rutstroemiaceae [Colour figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Robustness of diversification rate shifts identification in the Sclerotiniaceae phylogeny. (a) Lineage‐through‐time plots for the Sclerotiniaceae tree and 1,000 trees in which branching times were altered randomly by −15% to +15% to control for the sensitivity to divergence time estimates. Pybus γ for the Sclerotiniaceae tree is provided. (b) Frequency (n) of diversification rate shift detection and diversification rate estimates (r) in a 100 MEDUSA bootstrap replicates in which sampling richness, tree completeness and divergence times were randomly altered. Labels indicate average diversification rate estimates (r) for each macro‐evolutionary regime (blue for G1, grey for G2, brown for G3), with standard deviation of the mean for a 100 replicates. (c) Net diversification rates over time estimated by BAMM for each macro‐evolutionary regime (blue for G1, grey for G2, brown for G3) [Colour figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Diversification rate shifts associate with variations in rates of cospeciation, duplication and host switch in Sclerotiniaceae fungi. (a) Tanglegram depicting the associations between 102 Sclerotiniaceae species and 59 plant families. The three macro‐evolutionary regimes are indicated by coloured boxes on the Sclerotiniaceae tree. Fungal species labels are colour‐coded as in Figure 2. (b) Proportion of cospeciation, sorting/loss, duplication and host switches in host–Sclerotiniaceae associations as predicted by CoRe‐PA in 1,000 cophylogeny reconstructions. ** indicate large effect size in a macro‐evolutionary compared to the complete set of associations as assessed by Cohen's d test. (c) Proportion of host–Sclerotiniaceae associations contributing significantly and positively (likely cospeciation), non significantly and significantly and negatively (likely host switch) to cophylogeny in PACo analysis. The black dotted line indicates the percentage of broad host range species (five or more host families) in each group [Colour figure can be viewed at http://wileyonlinelibrary.com]