COS 265-6 - Informing disease management of cultivated figs by characterizing plant-wasp-nematode-fungal ecology in wild fig relatives

Abstract: 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 such effects. All figs have a mutualistic pollinating wasp which may unintentionally introduce pathogenic fungi (genus Fusarium) that reduce crop yield. In cultivated figs this disease is called Fig Endosepsis and causes significant losses. Here we explore another ubiquitous component of the fig system: nematodes. Data from wild fig species in Central America suggest that Parasitodiplogaster nematode associates of pollinating wasps may suppress the growth of a similar fungal pathogen, but the mechanism and ecological relevance of this interaction remains unclear. It is hypothesized that through the mitigation of fungus, nematodes provide fig communities with a previously unappreciated mutualistic service. Using a combination of observations, field experiments, and phylogenomics we 1) identify the fungus associated with wild figs, 2) ascertain if Parasitodiplogaster nematodes actively limit fungal growth, 3) determine if cultivated figs in the US harbor associations with similar nematodes, and 4) characterize the plant-wasp-nematode-fungal dynamics of European wild relatives of US cultivated figs.

Surveys of the Ficus petiolaris community in Mexico showcase significant negative correlation between the presence of nematodes and fungus. Interaction experiments involving both organisms indicate dual antagonism: nematodes clear fungus but fungus can also kill nematodes. Microscopy indicates that nematodes are capable of consuming small amounts of fungus, likely through a previously unrecognized omnivorous mouthform. Sequencing of the fungal genome was conducted for isolates taken from Ficus petiolaris as well as from wild and cultivated Ficus carica figs in central California. Phylogenomic analyses indicate that all sampled fungi are closely related Fusarium species. No nematodes were observed in wild or cultivated Ficus carica figs in the US. Finally, wild Ficus carica figs in southern Spain were sampled and were found to have associations with both Schistonchus nematodes as well as Fusarium 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 Diplogastrid nematodes can consume this fungus, likely incidentally (consuming fungus and wasp material simultaneously). This supports the notion of a secondary mutualistic behavior provided by fig nematodes and could potentially inform the management of cultivated figs in the US and beyond.