Natural selection drives population divergence for local adaptation in a wheat pathogen

Abstract

Evolution favors the emergence of locally-adapted optimum phenotypes that are likely to differ across a wide array of environmental conditions. The emergence of favorable adaptive characteristics is accelerated in agricultural pathogens due to the unique properties of agro-ecosystems. We performed a QST - FST comparison using 164 strains of Parastagonospora nodorum sampled from eight global field populations to disentangle the predominant evolutionary forces driving population divergence in a wheat pathogen. We used digital image analysis to obtain quantitative measurements of growth rate and melanization at different temperatures and under different fungicide concentrations in a common garden experiment. FST measures were based on complete genome sequences obtained for all 164 isolates. Our analyses indicated that all measured traits were under selection. Growth rates at 18 °C and 24 °C were under stabilizing selection (QST < FST), while diversifying selection (QST > FST) was the predominant evolutionary force affecting growth under fungicide and high temperature stress. Stabilizing selection (QST < FST) was the predominant force affecting melanization across the different environments. Melanin production increased at 30 °C but was negatively correlated with higher growth rates, consistent with a trade-off under heat stress. Our results demonstrate that global populations of P. nodorum possess significant evolutionary potential to adapt to changing local conditions, including warmer temperatures and applications of fungicides.