Predicting the evolutionary fate of the virus resistant transgene in wild populations of Cucurbita pepo

Background/Question/Methods

Gene exchange between crops and their wild relatives is common and difficult to contain.  Unlike most traits of cultivated species, there are concerns that transgenes conferring resistance to herbivores or pathogens could enhance the fitness and weediness of wild species and/or have indirect impacts on non-target species such as pollinators, herbivores, predators, soil fauna, and other plants in the community.  Gene flow between cultivated squash and its wild counterpart (Cucurbita pepo ssp. texana) may result in the introduction of the virus resistant transgene (VRT) into wild populations.  Fitness of the transgene in wild populations or during escape is influenced by the full ecological community as indirect costs associated with increased exposure to bacterial wilt can mitigate the fitness benefits of the VRT.  We have extensively studied the interactions among C. pepo, its primary herbivores (cucumber beetles and aphids) and the pathogens they transmit (Erwinia tracheiphila, the causative agent of bacterial wilt, and three mosaic viruses).  Using observations from field-scale experimental epidemics using the entire Cucurbita pathosystem we parameterized a predictive model of transgene escape in wild populations.  The deterministic ODE model was used to run simulations of scenarios not possible with our field experiments. 

Results/Conclusions

Based on our field observations, we saw behavioral avoidance of virus infected plants by cucumber beetles, which increased the risk of mortality due to bacteria in transgenic plants.  We quantified behavioral avoidance by comparing the number of beetles in flowers between healthy and virus infected plants.  Our observations indicate that viral infection is not lethal, but suppresses reproductive output by approximately one-third relative to healthy plants.  Incorporating this behavioral avoidance and the reproductive cost of viral infection in a simulation model we show that the fitness of the transgene is affected both by the magnitude of beetle avoidance and the timing of virus and bacteria epidemics relative to the timing of plant reproduction. The former effect is expected to depend on host availability, while the latter will depend on vector phenology and the community of reservoir plants. Our simulations indicate that combinations of these ecological settings can result in fixation of the transgene in a population, failure of the transgene to invade, or stable polymorphism.  With the simulations we can identify the range of conditions under which the transgene will increase in frequency, which is useful for both monitoring and management.