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Watermelon mosaic virus (WMV) and Zucchini yellow mosaic virus (ZYMV) are among the major cucurbit-infecting viruses worldwide. In France, WMV has a high prevalence every year throughout the growing season; ZYMV, although it can present locally a very high agronomic impact, induces epidemics that are very irregular both in spatial distribution and timing of infection. Large-scale epidemiological surveys followed by molecular analysis of all collected samples were performed during 5 years in France, and revealed the recent appearance of new, “emerging” (EM) isolates of both viruses in south-eastern France. In the case of WMV, four subgroups of EM isolates were defined, probably resulting from several recent introductions. They presented a strong geographic structure that remained stable over 5 years, and tended to replace rapidly the original “classic” isolates in areas where both types of strains were present. For ZYMV, at least two subgroups of new isolates were also detected in the last years, although the geographic structure of infections and evolution of populations was less obvious than for WMV. In order to characterize the evolution of viral populations and study the mechanisms favouring or limiting viral emergence and spread, several complementary approaches were developed: multilocal and multiscale epidemiological studies, molecular analyses and population genetics, as well as estimation of viral fitness in experimental condition and modeling. The risks of emergence of recombinants between “classic” and EM populations in the few years following their contact were also assessed.

Watermelon mosaic virus (WMV, Potyvirus) is very common in France where it has been present for at least 40 years. Since the early 2000s, new “emerging” (EM) strains of WMV, highly divergent molecularly from the “classic” (CL) strains present before and probably originating from recent introductions, were detected in southeastern France. Since both types of strains did not appear to be present in the same geographic locations before, this situation constituted a unique opportunity to study the frequency of appearance and the potential spread of recombinants in the few years following the introduction of the new strains. Analyzing isolates from experimental plots in Montfavet (Southeastern France) as well as from epidemiological surveys performed from 2004 to 2008 all around France (about 2000 WMV isolates) revealed at least 7 independent recombination events, either between CL and EM strains or between different EM subgroups. Most recombinants were found in a few plants from the same field, but, with one notable exception, did not seem to spread or be maintained locally for several years. Mixed infections of CL and EM isolates were also performed in experimental conditions in order to compare the frequency and nature of recombination events to those of natural situation. The fitness of natural recombinants relative to potential “parental” strains was also tested in controlled conditions. The epidemiological and evolutionary consequences of recombination in WMV populations will be discussed. This work represents one of the first estimation for the frequency of appearance of recombinants in natural populations of a plant RNA virus.