Résumé
Expanding global trade and the domestication of ecosystems have greatly
accelerated the rate of emerging infectious fungal diseases, and
host-shift speciation appears to be a major route for disease emergence.
There is therefore an increased interest in identifying the factors that
drive the evolution of reproductive isolation between populations adapting
to different hosts. Here, we used genetic markers and cross-inoculations
to assess the level of gene flow and investigate barriers responsible for
reproductive isolation between two sympatric populations of Venturia
inaequalis, the fungal pathogen causing apple scab disease, one of the
fungal populations causing a recent emerging disease on resistant
varieties. Our results showed the maintenance over several years of strong
and stable differentiation between the two populations in the same
orchards, suggesting ongoing ecological divergence following a host-shift.
We identified strong selection against immigrants (i.e. host-specificity)
from different host varieties as the strongest and likely most efficient
barrier to gene flow between local and emerging populations. Cross-variety
disease transmission events were indeed rare in the field and
cross-inoculation tests confirmed high host specificity. Because the
fungus mates within its host after successful infection and because
pathogenicity-related loci prevent infection of non-host trees, adaptation
to specific hosts may alone maintain both genetic differentiation between
and adaptive allelic combinations within sympatric populations
parasitizing different apple varieties, thus acting as a “magic trait”.
Additional intrinsic and extrinsic post-zygotic barriers might complete
reproductive isolation and explain why the rare migrants and F1 hybrids
detected do not lead to pervasive gene flow across years.