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.

Powdery mildews on Quercus: A worldwide distribution and rediscovered holotype provide insights into the spread of these ecologically important pathogens

“…The discovery of the holotype of Microsphaera alphitoides and subsequent sequencing results presented in the current study show that the ex-holotype sequence of this species from 1911 falls within the E. quercicola clade (Figure 1). This confirms the recent research by Gross et al (2021) arise with morphologically and genetically similar strains (Bradshaw, Braun, Elliott, et al, 2021) Erysiphe alphitoides and E. quercicola are two plurivorous species with oak species as the main hosts. Sequences retrieved from E. quercicola form a well-supported monophyletic clade (Figure 1 and Takamatsu et al, 2007), which supports the status of E. quercicola as an independent species.…”

“…However, the results of the sequence analysis of the holotype material revealed that M. alphitoides is identical to the powdery mildew that is currently referred to as Erysiphe quercicola, i.e., E. quercicola is now a heterotypic synonym of E. alphitoides and the common oak powdery mildews, which has been assigned to E. alphitoides, would need a new name. The results from the sequence analysis of the E. alphitoides holotype from 1911 are in accordance with recently published findings that showed that E. alphitoides was not present in European Herbaria until 1921 (Gross et al, 2021). Unfortunately, the implications of the 'true' identity of M. alphitoides are severe and would cause confusion regarding these intensely studied taxa.…”

“…on Quercus robur; however, recent results by Gross et al (2021) showed that this pathogen was not present in European until…”

“…lat consisted of a species complex of morphologically similar powdery mildews. Erysiphe alphitoides was originally described in France in 1911 on Quercus robur ; however, recent results by Gross et al (2021) showed that this pathogen was not present in European until 1921 based on specimens located in herbaria and not widespread throughout Europe until after 1960. The discovery of the holotype of E .…”

Ash Trees (Fraxinus spp.) in Urban Greenery as Possible Invasion Gates of Non-Native Phyllactinia Species

“…W. Phillips [20]. Further, the implementation of molecular methods has caused the formal break-down of species complexes with overlapping or distinct distribution ranges into separate taxa [21]. Phyllactinia fraxini is an excellent example of such a case.…”