Informing disease management of cultivated figs by characterizing plant-wasp-nematode-fungal ecology in wild fig relatives

Maximizing crop production by minimizing disease is a central challenge in agriculture. The domestication process often displaces crops from co-adapted community associates, but the relevance of this effect for disease susceptibility is not fully understood. Cultivated figs (Ficus carica) and their wild relatives form an excellent system for investigating the implications. All figs have pollinating wasps which may unintentionally introduce pathogenic fungi (Fusarium) that reduce crop yield. Data from wild figs in Central America suggest that nematode associates of pollinating wasps (Parasitodiplogaster) suppress the growth of a similar fungal pathogen, but the mechanism of this interaction remains unclear. We identify the fungus associated with wild figs, ascertain if nematodes actively limit fungal growth, determine if US-based cultivated figs harbor associations with similar nematodes, and characterize the biotic dynamics of European wild relatives of US-cultivated figs. Phylogenomic analyses of fungi associated with wild and cultivated fig species suggest all sampled fungi are closely related Fusarium species. Experiments indicate dual antagonism between fungi and nematodes. No nematodes were observed in F. carica in the US. Finally, wild F. carica in southern Spain was found to have associations with both nematodes and fungus without significant negative correlations. These results suggest that Fusarium fungi are widespread antagonists of fig systems both in wild and cultivated contexts, and that nematodes can consume this fungus. This supports the notion of a secondary mutualism provided by fig nematodes and could inform the management of cultivated figs in the US and beyond.