[Free Download Hidden Invasion
Melvin Amey
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.
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). However, 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). For example, the spread of the fungus Batrachochytrium dendrobatidis, which causes chytrid disease, has been shown to be a key factor in the worldwide decline of amphibian populations (Fisher et al. 2009). The global emergence of invasive microbial pathogens is now considered a major challenge in invasion science (Ricciardi et al. 2017). Microbes are characterized by a tremendous diversity, harboring still numerous undescribed species. In particular, the fungal kingdom has been estimated to include several millions of species, of which only a few percent have been formally described (Blackwell 2011; Hawksworth and Lcking 2017; Wu et al. 2019). The lack of diagnostic features for species identification before the advent of molecular and phylogenetic methods explains that many species, only defined on a morphological basis, were thought to be cosmopolitan (Taylor et al. 2000). The recognition of cryptic species within morphological species has now become extremely common (Fitt et al. 2006; Crous et al. 2016). Cryptic species often show a different geographic distribution, ecology and pathogenicity (Taylor et al. 2000). For example, 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. H. fraxineus has probably co-evolved with Asian ash, on which it causes little damage (Gross et al. 2014; Enderle et al. 2019). The introduced species H. fraxineus has now 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).
With increasing rates of introductions, invasions may involve not only interactions between native and introduced species but also between introduced species in the same area. Multiple or successive invasions by functionally equivalent or closely related species have started to be documented and investigated, especially in plants and animals (Rauschert and Shea 2012; Russell et al. 2014; Linzmaier et al. 2018). Many examples of multiple invasions have been reported for insects (Reitz and Trumble 2002). It may be hypothesized that such multiple invasions could also be very frequent for microbial pathogens which, similar to insects, show a great diversity, including complexes of cryptic species, and propensity to be disseminated with human activities. The two successive pandemics of Dutch Elm Disease, caused by the spread of two fungal species (Ophiostoma ulmi and Ophiostoma novo-ulmi) outside their native area, is one among very few documented examples for fungi (Brasier and Buck 2001) but the availability of molecular methods may increasingly reveal the high significance of multiple microbial invasions. Multiple invasion events are interesting to address important questions in ecology, e.g. species coexistence or displacement. Historically, species displacements, intimately linked to invasions, have been considered as an illustration of competitive exclusion, where the most competitive species eliminates the other species sharing the same ecological niche (DeBach 1966; Gao and Reitz 2017). However, the outcome of competitive interactions during invasions may not be as extreme, depending on the amount of niche overlap, the relative competitive ability of species for resource use, and spatial and temporal variations in the interaction (MacDougall et al. 2009; Gao and Reitz 2017). In the case of Dutch Elm Disease, the fitness advantage of O. novo-ulmi, which eventually displaced O. ulmi, was shown to include several components, such as direct competitive antagonism, exploitative competition through resource use and wider climatic niche (Brasier and Buck 2001). Considering cryptic species in invasions has also important practical implications. The fact that many microbial, including fungal, pathogens occur as species complexes may impede the detection of a new, potentially more damaging, introduced pathogen if a closely related species causing the same symptoms has already invaded. Ash dieback, but also grapevine powdery mildew in Europe are examples of diseases caused by an introduced pathogen species having close relatives in its native area, which constitute further risks for the target host species (Schrder et al. 2011; Gross and Han 2015).
The aim of the present study was to improve our understanding of the multiple invasion of oak powdery mildew fungi in Europe. By using more than 200 herbarium specimens of infected oak leaves, dating from 1875 to 2002 and distributed all over Europe, our first goal was to date the invasion history of the three species. Next, we tried to elucidate potential processes underlying the observed invasion dynamics by investigating two mechanisms possibly responsible for invasive success (i) the mating type ratio, conditioning sexual reproduction, characterized in the herbaria specimens for E. alphitoides and E. quercicola and (ii) competitive interactions between the two species, using an experimental approach with fresh isolates.
We tried to obtain as many specimens as possible from all over Europe collected between late nineteenth century and 1980 consisting of leaves infected by oak powdery mildew, recorded under different names, most often Microsphaera alphitoides, but also Erysiphe quercina or others (Online Resource 2).
Mean infection efficiency (estimated as the ratio of targeted DNA copies detected 10 days after inoculation to the estimated number of spores used for inoculation) for E. alphitoides and E. quercicola when inoculated alone or in mixture with the other species
Our study based on analyses of herbaria specimens provided several unexpected findings that challenge the currently admitted scenario of oak powdery mildew invasion in Europe based on historical reports (Mougou et al. 2008). The new scenario, strongly supported by evidence, resolve apparent contradictions (detailed below) in the history of this invasion by a complex of closely related species. Our results suggest that the first invasive species experienced niche contraction after over-invasion of the second species and point to several mechanisms potentially explaining this outcome. Our case study thus improves our understanding of multiple invasions by closely related, functionally equivalent species (Russell et al. 2014), which is of particular significance for fungi.
The first striking finding of our study is that, with the help of herbaria specimens, it was possible to date the presence of oak powdery mildew to as early as the year 1904 (excluding the two oldest specimens corresponding to another taxon), i.e. three years earlier than the first report of symptoms in the literature (Hariot 1907). It should be pointed out here that all the time estimates based on herbaria samples have to be taken with caution since they were gained by a limited sampling of herbaria specimens. An even earlier introduction is thus likely. Our finding helps to explain the fact that the species was detected in many European countries (England, Germany, Austria, Belgium, Portugal, Italy, Scandinavia, Switzerland) in 1908, only a single year after the first mentioning in the literature. Obviously, the epidemic had started before but was only noticed by few mycologists and was not reported in the literature. Lags in detection (i.e. time between entry and discovery of an invasive species) are very common in undeliberate introductions since populations often grow exponentially in the early phases of invasion and they become noticed only when they reach high density or cause significant damage (Crooks 2005). Such a lag was already reported for some fungal pathogens, e.g. H. fraxineus (Gross et al. 2014).
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