Rapid change in host specificity in a field population of the biological control organism Pasteuria penetrans

Authors: LIU, CHANG - University Of Georgia; GIBSON, AMANDA - Emory University; Timper, Patricia - Patty; MORRAN, LEVI - Emory University; TUBBS, SCOTT - University Of Georgia

Submitted to: Evolutionary Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/28/2018
Publication Date: 12/9/2018
Citation: Liu, C., Gibson, A., Timper, P., Morran, L.T., Tubbs, S. 2018. Rapid change in host specificity in a field population of the biological control organism Pasteuria penetrans. Evolutionary Applications. 12:744-756. https://doi.org/10.1111/eva.12750.
DOI: https://doi.org/10.1111/eva.12750

Interpretive Summary: In biological control, populations of both the biological control agent and the pest have the potential to evolve and even to coevolve. This feature marks the most powerful and unpredictable aspect of biological control strategies. In particular, evolutionary change in host specificity of the biocontrol agent could increase or decrease its efficacy. Here, we tested for evolutionary change in host specificity of populations of the biological control agent Pasteuria penetrans. Pasteuria is a bacterium that naturally parasitizes root-knot nematodes nematodes, which are major agricultural pests. From 2013 through 2016, we collected yearly samples of Pasteuria populations from eight plots in a field infested with the peanut root-knot nematode. Plots were planted either with peanut or with a rotation of peanut and soybean. To detect changes in host specificity over time, we tested Pasteuria samples annually for their ability to attach to four different clonal lines of root-knot nematodes. These clonal lines are susceptible to different subsets of Pasteuria spores. Each of the eight populations of Pasteuria showed changes in their attachment specificity among the clonal host lines over time. This result is consistent with rapid change in the host specificity of biocontrol populations. The Pasteuria population within each plot appeared to evolve independently, indicating that local forces, at the level of individual plots, drive evolutionary change. We hypothesize that evolution of the host nematodes is the driving force behind the changes in specificity of Pasteuria. In other words, as the nematode population becomes resistant to attachment by the local Pasteuria, the bacterium changes so that it can attach to the nematode population akin to an arms race. Lastly, we observed reduced attachment using samples from rotation relative to peanut plots. This result may reflect lower density, and thereby dose, of Pasteuria under crop rotation, potentially due to lower densities of host nematodes. As a whole, our study demonstrates rapid, local evolution of populations of a biological control agent which may allow them to overcome resistance in the host population.

Technical Abstract: In biological control, populations of both the biological control agent and the pest have the potential to evolve and even to coevolve. This feature marks the most powerful and unpredictable aspect of biological control strategies. In particular, evolutionary change in host specificity of the biocontrol agent could increase or decrease its efficacy. Here, we tested for evolutionary change in host specificity of populations of the biological control agent Pasteuria penetrans. P. penetrans naturally parasitizes the plant parasitic nematodes Meloidogyne spp., which are major agricultural pests. From 2013 through 2016, we collected yearly samples of P. penetrans populations from eight plots in a field infested with M. arenaria. Plots were planted either with peanut or with a rotation of peanut and soybean. To detect temporal change at loci linked to host specificity, we tested P. penetrans samples annually for their ability to attach to four clonal lines of M. arenaria. Each of the eight populations of P. penetrans showed temporal variation in their attachment specificity among the clonal host lines. This result is consistent with rapid change in the host specificity of biocontrol populations. The trajectories of change in host specificity were unique to each P. penetrans population. This result indicates that local forces, at the level of individual plots, drive evolutionary change. We hypothesize that coevolution with local M. arenaria hosts is one such force. Lastly, we observed reduced attachment using samples from rotation relative to peanut plots. This result may reflect lower density, and thereby dose, of P. penetrans under crop rotation, potentially due to suppressed density of host nematodes. As a whole, our study demonstrates rapid, local evolution of populations of a biological control agent at loci linked to their ability to infect and suppress the target pest.