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

Patricia Timper,Amanda Kyle Gibson,Chang Liu,Levi T Morran,R Scott Tubbs

doi:10.1111/eva.12750

Patricia Timper, Amanda Kyle Gibson + Show 3 more

Open Access

https://doi.org/10.1111/eva.12750

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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 biological control agent could increase or decrease its efficacy. Here, we tested for change in host specificity in a field population of the biological control organism Pasteuria penetrans. Pasteuria penetrans is an obligate parasite of the plant parasitic nematodes Meloidogyne spp., which are major agricultural pests. From 2013 through 2016, we collected yearly samples of P. penetrans from eight plots in a field infested with M. arenaria. Plots were planted either with peanut (Arachis hypogaea) or with a rotation of peanut and soybean (Glycine max). To detect temporal change in host specificity, we tested P. penetrans samples annually for their ability to attach to (and thereby infect) four clonal lines of M. arenaria. After controlling for temporal variation in parasite abundance, we found that P. penetrans from each of the eight plots showed temporal variation in their attachment specificity to the clonal host lines. The trajectories of change in host specificity were largely unique to each plot. This result suggests that local forces, at the level of individual plots, drive change in specificity. We hypothesize that coevolution with local M. arenaria hosts may be one such force. Lastly, we observed an overall reduction in attachment rate with samples from rotation plots relative to samples from peanut plots. This result may reflect lower abundance of P. penetrans under crop rotation, potentially due to suppressed density of host nematodes. As a whole, the results show local change in specificity on a yearly basis, consistent with evolution of a biological control organism in its ability to infect and suppress its target pest.

Highlights

Host specificity is the foremost challenge for the safe and effective use of biological control agents
It simultaneously lost its ability to attach to its. We addressed this question by testing for spatial and temporal variation in the host specificity of P. penetrans sampled from plots in an experimental agricultural field
Long‐term sampling of this study site provided preliminary evidence for change in host specificity: Starting in 1998, we used a single laboratory population of M. arenaria to assay the soil for abundance of P. penetrans endospores

Summary

| INTRODUCTION

Host specificity is the foremost challenge for the safe and effective use of biological control agents (reviewed in Brodeur, 2012; Fagan, Lewis, Neubert, & Driessche, 2002; McEvoy, 1996). Upon release into a novel range, generalist predators or parasites may attack unintended prey or host species, leading to a decline in their population size and an increase in extinction risk (e.g., Boettner, Elkinton, & Boettner, 2000; Louda, Kendall, Connor, & Simberloff, 1997; reviewed in Louda, Pemberton, Johnson, & Follett, 2003; Simberloff & Stiling, 1996) Such nontarget effects motivated a shift toward biological control agents with narrow host ranges. Long‐term sampling of this study site provided preliminary evidence for change in host specificity: Starting in 1998, we used a single laboratory population of M. arenaria to assay the soil for abundance of P. penetrans endospores. After controlling for variation in endospore abundance, we observed substantial yearly change in attachment rates of field‐sampled P. penetrans to the tested host lines, consistent with the hypothesis of rapid evolution of host specificity

| MATERIALS AND METHODS

Findings

| Conclusion