Dispersal of cereal mildews across Europe

Abstract

Following the evolution and spread of the barley and the wheat mildew pathogens, ( Blumeria (Erysiphe) graminis f.sp. hordei and tritici, respectively) over a long period and a large scale in Europe brought us new insight into their population biology which appears to be much more affected by aerial dispersal than generally believed. Results on the local evolution of the number of colony forming units m −3 of air (cfu) gave us an insight into the major features of population genetics and epidemiology of the barley mildew pathogen. Firstly, the evolution of cfu demonstrates and quantifies the epidemiological significance of volunteer plants. Moreover, three or four periods of primary infections become evident per year, forcing the wind-borne pathogen spores to move from one field (or region) to the next. This makes the pathogen to be highly nomadic, and points out to be of major interest for studies across Europe. Pathogen samples were analyzed from within the geographical triangle Spain–Scotland–Byelorussia for virulence to host resistance. Most unexpectedly, virulence complexity (i.e. number of virulence genes per spore) increased by approximately one virulence per 1000 km from west to east, from Scotland and France to central and eastern Europe. It is presumably caused by the interaction of prevailing winds, pathogen spores migrating on them, and host selection. Prevailing westerly winds carry pathogen spores to the east. Along the way, they encounter barley cultivars with different genes for race-specific resistance, and selection increases virulence complexity. The increase is elucidating for basic concepts of population genetics of wind-borne species, and important for gene deployment strategies. There was ample evidence for the dispersal of genes and genotypes from the regional to the continental level and beyond. Depending on year and location, detailed analyses showed that major parts of the population in one region can be assumed to originate from neighboring or distant regions. Dispersal is reduced by distance, barriers like mountain chains, and host-free spaces. Further, mildew ‘waves’ consisting of populations highly adapted through selection in one region appear to move across Europe on the prevailing westerly winds, covering approximately 100 km/year. Another important unexpected finding relates to fundamental features of the evolution of new and dangerous pathotypes. The established way of thinking starts with the effect of (regional) mutation as the basis of variability. In contrast, our evidence stresses the importance of the extraordinary variability already present in the pathogen population due to inoculum exchange over the vast continuous areas of Europe, northern Africa and Asia where the pathogen is endemic. Though mutation will remain of importance in the end, variability through spore dispersal among regions appears to be of more immediate relevance for the rapid adaptation of cereal mildew populations. Implications of our findings for fundamental aspects of population biology and integrated pest management strategies, from the regional to the continental and intercontinental level, are outlined and discussed.