Potato late blight populations: migration, selection and chance?

Abstract

Since the 1970s, new genotypes of Phytophthora infestans introduced into many parts of the world have almost completely displaced the old, A1 clonal lineage. Despite introductions of both mating types, in many regions this has not resulted in sexually-recombinant populations becoming established, but in the evolution of new, but largely clonal populations. These may comprise several major clonal genotypes and sometimes undergo periodic upheavals when new fit genotypes appear by migration, infrequent recombination or other mechanisms. For example, the P. infestans population in Ireland consists of a number of clones all of the A1 mating type: A2 mating type strains, although introduced in the 1980s, do not appear, so far, to have become widely established in the population and are rarely detected. The population in Great Britain also appears clonal, but is currently undergoing major changes. In Taiwan, displacement of the old US-1 population took place within 2 years, but the new population is also A1 and clonal. In the USA, although numerous A1 and A2 genotypes have appeared since the early 1990s, only a limited number have been perpetuated. At present, in the eastern and mid-western states, the US-8 genotype, which first appeared in the mid 1990s, is dominant, but US-11 is the main genotype isolated from potato and tomato from Washington, Oregon, and Alaska, while US-14 and variants occur on both potato and tomato in Florida. There is currently evidence of the appearance of new genotypes in parts of the US, but it remains to be seen if these will displace existing ones. Thus, in some regions (e.g. Taiwan), the new genotypes belonged to only a single mating type, but in others, even where multiple genotypes of both mating types were introduced, only a few have been perpetuated. What mechanisms are involved? Field trials in Northern Ireland and Michigan using multiple potato cultivars and P. infestans genotypes showed that extreme selection occurred within the P. infestans populations at both locations. In Northern Ireland, there was a strong influence of cultivar; different genotypes dominated infection of different cultivars. Selection was partly due to aggressiveness to specific cultivars, but this did not fully explain the extreme selection in the field, other factors such as direct competition during the infection process may also play a role. In the US, the US-8 genotype proved the most aggressive and also dominated infection of all cultivars in the field: other genotypes were rarely detected. Additional selection occurs during the tuber phase. Studies in Belfast demonstrated that the cultivar influences which genotypes infect tubers; even where multiple genotypes have colonised foliage, few infect tubers. Over the winter, some genotypes may be lost by tuber rotting. A further bottle-neck occurs when epidemics are initiated by surviving infected tubers: field trials showed that when tubers inoculated with different genotypes were planted, generally only one successfully initiated foliar infection. Finally, the extreme efficiency of asexual reproduction in P. infestans, compared with the sexual cycle, must be important in perpetuating clonal genotypes in regions where tuber infection is frequent and infected tubers can survive the winter. However, none of these factors seems sufficient to explain why sexually-recombinant populations have apparently become established in some parts of Europe, including the Netherlands, Poland and the Nordic countries, yet, in many other regions, sexual recombination seems to be very infrequent or even absent. Barriers to successful recombination and perpetuation of sexual progeny may well be important: these merit further investigation. Above all, chance may play a crucial role, particularly in terms of the introduction and survival of new, fit genotypes of P. infestans by man, its principal vector.