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.
Highlights
The host range of a parasite has a central influence on the emergence and spread of disease (Woolhouse & Gowtage-Sequeria, 2005)
Our analyses lead to a model in which the extant diversity of Sclerotiniaceae fungi is the result of three macro-evolutionary regimes characterized by distinct diversification rates and host association patterns
Patterns of cophylogeny decreased from regime G1 to G3, while the frequency of inferred host jump events increased from G1 to G3
Summary
The host range of a parasite has a central influence on the emergence and spread of disease (Woolhouse & Gowtage-Sequeria, 2005). The poplar pathogen Ciborinia whetzelii and several Myriosclerotinia species are biotrophs that can live as endophytes (Andrew, Barua, Short, & Kohn, 2012; Schumacher & Kohn, 1985), while Coprotinia minutula is coprophilous (Elliott, 1967) How this remarkable diversity evolved remains elusive. We show that three macro-evolutionary regimes with distinct diversification rates and dominant host association patterns have shaped the diversity of the Sclerotiniaceae and lead to contrasted proportions of broad host range species. We highlight an increased emergence of broad host range parasites during the transition between macro-evolutionary regimes dominated by distinct patterns of host–pathogen association. These results suggest that reduced diversification rates and high host jump frequency could associate with the emergence of generalist pathogens
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