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.
Highlights
The microbial component of biological invasions has been recognized rather lately compared to plant and animal invasions (Desprez-Loustau et al 2007; Mallon et al 2015; Dunn and Hatcher 2015; Blackburn and Ewen 2017)
Our results provide new insights into the history of the oak powdery mildew invasion in Europe
They strongly suggest that E. quercicola was the first invading powdery mildew species on oaks in Europe in the early twentieth century, another Erysiphe species was detected on oaks in 1875 in Italy, and that E. alphitoides over-invaded in a second stage
Summary
The microbial component of biological invasions has been recognized rather lately compared to plant and animal invasions (Desprez-Loustau et al 2007; Mallon et al 2015; Dunn and Hatcher 2015; Blackburn and Ewen 2017). The dramatic impact of diseases caused by pathogens of exotic origin in natural communities is well documented (Hatcher et al 2012; Fisher et al 2012). The recent ash dieback observed in Europe, which was initially thought to be caused by the native species Hymenoscyphus albidus, was shown to be associated with a closely related and morphologically almost indistinguishable species of Asian origin. The introduced species H. fraxineus has spread in almost the whole range of ash in Europe and has progressively outcompeted the native species, H. albidus, which can hardly be found in areas where the new disease has been reported (McKinney et al 2012; but see Dvorak et al 2015; Koukol et al 2015)
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