Limiting opportunities for cheating stabilizes virulence in insect parasitic nematodes.

David Shapiro-Ilan,Ben Raymond

doi:10.1111/eva.12348

Abstract

Cooperative secretion of virulence factors by pathogens can lead to social conflict when cheating mutants exploit collective secretion, but do not contribute to it. If cheats outcompete cooperators within hosts, this can cause loss of virulence. Insect parasitic nematodes are important biocontrol tools that secrete a range of significant virulence factors. Critically, effective nematodes are hard to maintain without live passage, which can lead to virulence attenuation. Using experimental evolution, we tested whether social cheating might explain unstable virulence in the nematode Heterorhabditis floridensis by manipulating relatedness via multiplicity of infection (MOI), and the scale of competition. Passage at high MOI, which should reduce relatedness, led to loss of fitness: virulence and reproductive rate declined together and all eight independent lines suffered premature extinction. As theory predicts, relatedness treatments had more impact under stronger global competition. In contrast, low MOI passage led to more stable virulence and increased reproduction. Moreover, low MOI lineages showed a trade-off between virulence and reproduction, particularly for lines under stronger between-host competition. Overall, this study indicates that evolution of virulence theory is valuable for the culture of biocontrol agents: effective nematodes can be improved and maintained if passage methods mitigate possible social conflicts.

Highlights

Kin selection theory resolves the conflict over the maintenance of behaviors that are beneficial for groups of organisms, but costly for individuals, by reasoning that costly cooperation is stable if it is primarily directed at individuals that share the same alleles for cooperation, that is under high relatedness (Hamilton 1964a,b)
Social conflicts have repeatedly been identified in microbial pathogens, which often secrete virulence factors that are analogous to ‘public goods’; these goods are costly to individuals, beneficial to groups and can be exploited by cheating mutants that benefit from collective action, but do not contribute to it (Ko€hler et al 2009; Raymond et al 2012; Diard et al 2014a)
Cooperation and evolution of virulence and parasite reproduction For pathogens, increased investment in secreted public goods may lead to improved infectivity, as toxins or quorum regulated enzymes may be required for effective host invasion (Raymond and Bonsall 2013; Zhou et al 2014)

Summary

Introduction

Kin selection theory resolves the conflict over the maintenance of behaviors that are beneficial for groups of organisms, but costly for individuals, by reasoning that costly cooperation is stable if it is primarily directed at individuals that share the same alleles for cooperation, that is under high relatedness (Hamilton 1964a,b). In contrast if competition is primarily global, for example between patches or groups of unrelated organisms, altruism can be favored (Frank 1998). While this theory is not experimentally tractable in vertebrates and higher organisms, experimental evolution of the cooperative secretion of iron-scavenging siderophores suggests that both relatedness and the scale of competition are important for microbial cooperation in simple systems (Griffin et al 2004; Ku€mmerli et al 2009)

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Conclusion