Interactions between insect vectors and plant pathogens span the parasitism-mutualism continuum

Abstract

Agricultural crops infected with vector-borne pathogens can suffer severe negative consequences, but the extent to which phytopathogens affect the fitness of their vector hosts remains unclear. Evolutionary theory predicts that selection on vector-borne pathogens will favour low virulence or mutualistic phenotypes in the vector, traits facilitating effective transmission between plant hosts. Here, we use a multivariate meta-analytic approach on 115 effect sizes across 34 unique plant-vector-pathogen systems to quantify the overall effect of phytopathogens on vector host fitness. In support of theoretical models, we report that phytopathogens overall have a neutral fitness effect on vector hosts. However, the range of fitness outcomes is diverse and span the parasitism-mutualism continuum. We found no evidence that various transmission strategies, or direct effects and indirect (plant-mediated) effects, of phytopathogens have divergent fitness outcomes for the vector. Our finding emphasizes diversity in tripartite interactions and the necessity for pathosystem-specific approaches to vector control.

Keywords: multi-trophic interactions; parasitism–mutualism continuum; phytopathogen; symbiosis continuum; vector-borne; vector–pathogen interactions.

Figure 1.

Crops infected with vector-borne phytopathogens suffer negative consequences, but the extent to which phytopathogens affect the fitness of their vector hosts is unclear (a). Vector–phytopathogen interactions are diverse and range from parasitic to mutualistic (SMD = −0.1354, 95% CI: −0.8088–0.5381) (b). Mean effect and 95% confidence intervals are plotted in black. Effect sizes reported according to vector species (c), pathogen species (d) and plant host species (e). Individual effect sizes are jittered and coloured by family. Point size represents study sample size.

Figure 2.

Variation in the effect of infection on vector fitness was not significantly affected by pathogen type (a), transmission mode (circulative non-propagative; circulative-propagative; non-circulative, non-persistent; non-circulative, semi-persistent) (b), vertical transmission in vector (c), fitness measure (d), direct or indirect effects (e), vector sex (f), party infected (g) or acquisition time (h). Individual effect sizes are jittered and coloured by vector family. Point size represents study sample size. Mean effect sizes and 95% confidence intervals are plotted in black.