Non-target pathogen affects the costs of resistance to viral pathogens in the wild gourd, Cucurbita pepo ssp texana

Background/Question/Methods There is increasing concern about the escape of transgenes that convey resistance to natural enemies from cultivated crops to wild species. Establishment and spread of a resistance gene in wild populations depends both on the fitness costs associated with resistance and the ecological context that mediates those costs. Following escape into native populations, a resistance gene is likely to face a more complex selective landscape that may modulate the relative benefits of resistance. We study the introgression of a viral resistance transgene from cultivated squash to their wild con-specific, Cucurbita pepo ssp texana in the presence of a non-target pathogen. C. pepo is affected by two major classes of vector-transmitted pathogens: viruses transmitted predominantly by generalist aphids and the bacterium, Erwinia tracheiphila, transmitted by specialist cucumber beetles. The beetle vectors of Erwinia selectively forage on large plants with many flowers, resulting in a cost to these individuals in terms of increased mortality risk due to bacterial infection. Viral infection results in reduced growth rates and fecundity, while bacterial infection is almost always fatal. Thus, in the presence of viruses, transgenic resistant plants may have an increased risk of a fatal bacterial infection.

Results/Conclusions We studied rates of bacterial and viral infections in mixed fields of wild-type C. pepo as well as F1, BC1, BC2, and BC3 hybrids that either did or did not have the viral resistance transgene. F1 hybrids had increased rates of bacterial infection, regardless of the presence of the transgene, due to increased beetle visitation. However, rates of bacterial infection drop with repeated back-crosses to the wild-type. This suggests that the viral resistance transgene may face an initial barrier to escape into wild populations in the presence of Erwinia, though this effect may decrease over subsequent generations. We developed a simulation model, parameterized to field measurements, to explore the likelihood of invasion and rate of spread of the transgene over multiple generations in the presence and absence of Erwinia. The model highlights that the costs of viral resistance in C. pepo are highly dependent on the presence of Erwinia and its rate of spread relative to viruses.