Hidden invasion and niche contraction revealed by herbaria specimens in the fungal complex causing oak powdery mildew in Europe

Abstract

Deciphering the dynamics involved in past microbial invasions has proven difficult due to the inconspicuous nature of microbes and their still poorly known diversity and biogeography. Here we focus on powdery mildew, a common disease of oaks which emerged in Europe at the beginning of the twentieth century and for which three closely related Erysiphe species are mainly involved. The study of herbaria samples combined with an experimental approach of interactions between Erysiphe species led us to revisit the history of this multiple invasion. Contrary to what was previously thought, herbaria sample analyses very strongly suggested that the currently dominant species, E. alphitoides , was not the species which caused the first outbreaks and was described as a new species at that time. Instead, E. quercicola was shown to be present since the early dates of disease reports and to be widespread all over Europe in the beginning of the twentieth century. E. alphitoides spread and became progressively dominant during the second half of the twentieth century while E. quercicola was constrained to the southern part of its initial range, corresponding to its current distribution. A competition experiment provided a potential explanation of this over-invasion by demonstrating that E. alphitoides had a slight advantage over E. quercicola by its ability to infect leaves during a longer period during shoot development. Our study is exemplary of invasions with complexes of functionally similar species, emphasizing that subtle differences in the biology of the species, rather than strong competitive effects may explain patterns of over-invasion and niche contraction.

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