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Title: Limiting opportunities for cheating stabilizes virulence in insect parasitic nematodes

item Shapiro Ilan, David
item RAYMOND, BEN - Imperial College

Submitted to: Evolutionary Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/16/2015
Publication Date: 3/1/2016
Citation: Shapiro-Ilan, D.I., Raymond, B. 2016. Limiting opportunities for cheating stabilizes virulence in insect parasitic nematodes. Evolutionary Applications. 9(3):462-470.

Interpretive Summary: Entomopathogenic nematodes, also known as beneficial nematodes, are environmentally friendly bio-insecticides that are used to control a wide variety of economically important insect pests. These nematodes are routinely cultured in scientific laboratories for experimentation and mass-produced by companies for commercial applications. One problem with growing the nematodes is that some of their important properties, such as virulence (killing ability) and reproductive capacity, begin to decline after multiple generations. In this study we explored one of the possible causes for loss of virulence. We hypothesized that groups of nematodes that are not closely related will lose virulence faster than related groups. In a population of less related individuals, the pressure for an individual to be virulent and take part in “carrying the load” is reduced. We tested our hypothesis using a beneficial nematode called, Heterorhabditis floridensis. The hypothesis was supported because groups with lower relatedness quickly lost virulence and became extinct. One way to increase relatedness among nematodes when culturing them is to avoid using too many nematodes upon infection. Thus, our research indicates that companies and laboratories producing beneficial nematodes should avoid overly high rates of infection and thereby maintain virulence in the nematode populations.

Technical Abstract: Cooperative secretion of virulence factors by pathogens can often lead to social conflict as cheating mutants that benefit from collective action, but do not contribute to it, can arise and locally outcompete cooperators within hosts, leading to loss of virulence. There is a wide range of in vivo studies supporting this theory, including studies of microbial biocontrol agents. Insect parasitic nematodes are an important tool in biological control: both the nematode and symbiotic bacteria secrete diverse virulence factors. Critically, effective nematodes are hard to maintain without serial propagation in vivo (passage), and this can lead to attenuation. We tested whether cooperation is important for the maintenance of virulence in the nematode Heterorhabditis floridensis via experimental evolution. Low relatedness treatments (high multiplicity of infection) led to reduced virulence, lower reproductive rates and premature extinction of all replicates. In contrast, high relatedness led to stable infection rates and increased nematode reproduction at the end of the experiment. Cooperation also requires strong global (between-host) competition. Contrary to expectation, manipulations aimed at increasing between-host competition led to reduced virulence. We conclude that because between-host competition is a fundamental part of parasite invasion, it is difficult to manipulate the scale of competition without affecting relatedness.