Vector-borne pathogens may alter traits of their primary hosts in ways that influence the frequency and nature of interactions between hosts and vectors. Previous work has reported enhanced mosquito attraction to host organisms infected with malaria parasites but did not address the mechanisms underlying such effects. Here we document malaria-induced changes in the odor profiles of infected mice (relative to healthy individuals) over the course of infection, as well as effects on the attractiveness of infected hosts to mosquito vectors. We observed enhanced mosquito attraction to infected mice during a key period after the subsidence of acute malaria symptoms, but during which mice remained highly infectious. This attraction corresponded to an overall elevation in the volatile emissions of infected mice observed during this period. Furthermore, data analyses-using discriminant analysis of principal components and random forest approachesrevealed clear differences in the composition of the volatile blends of infected and healthy individuals. Experimental manipulation of individual compounds that exhibited altered emission levels during the period when differential vector attraction was observed also elicited enhanced mosquito attraction, indicating that compounds being influenced by malaria infection status also mediate vector host-seeking behavior. These findings provide important insights into the cues that mediate vector attraction to hosts infected with transmissible stages of malaria parasites, as well as documenting characteristic changes in the odors of infected individuals that may have potential value as diagnostic biomarkers of infection.

SignificanceMalaria elimination efforts are hindered by the prevalence of asymptomatic infections, which frequently go undetected and untreated. Consequently, there is a pressing need for improved diagnostic screening methods. Based on extensive collections of skin odors from human populations in Kenya, we report broad and consistent effects of malaria infection on human volatile emissions. Furthermore, we found that predictive models based on machine learning algorithms reliably determined infection status based on volatile biomarkers and, critically, identified asymptomatic infections with 100% sensitivity, even in the case of low-level infections not detectable by microscopy. These findings suggest that volatile biomarkers have significant potential for the development of robust, noninvasive screening methods for detecting symptomatic and asymptomatic malaria infections under field conditions.

Both biotic and abiotic stressors can elicit broad-spectrum plant resistance against subsequent pathogen challenges. However, we currently have little understanding of how such effects influence broader aspects of disease ecology and epidemiology in natural environments where plants interact with multiple antagonists simultaneously. In previous work, we have shown that healthy wild gourd plants (Cucurbita pepo ssp. texana) contract a fatal bacterial wilt infection (caused by Erwinia tracheiphila) at significantly higher rates than plants infected with Zucchini yellow mosaic virus (ZYMV). We recently reported evidence that this pattern is explained, at least in part, by reduced visitation of ZYMV-infected plants by the cucumber beetle vectors of E. tracheiphila. Here we examine whether ZYMV-infection may also directly elicit plant resistance to subsequent E. tracheiphila infection. In laboratory studies, we assayed the induction of key phytohormones (SA and JA) in single and mixed infections of these pathogens, as well as in response to the feeding of A. vittatum cucumber beetles on healthy and infected plants. We also tracked the incidence and progression of wilt disease symptoms in plants with prior ZYMV infections. Our results indicate that ZYMV-infection slightly delays the progression of wilt symptoms, but does not significantly reduce E. tracheiphila infection success. This observation supports the hypothesis that reduced rates of wilt disease in ZYMV-infected plants reflect reduced visitation by beetle vectors. We also documented consistently strong SA responses to ZYMV infection, but limited responses to E. tracheiphila in the absence of ZYMV, suggesting that the latter pathogen may effectively evade or suppress plant defenses, although we observed no evidence of antagonistic cross-talk between SA and JA signaling pathways. We did, however, document effects of E. tracheiphila on induced responses to herbivory that may influence host-plant quality for (and hence pathogen acquisition by) cucumber beetles.

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It is increasingly clear that microbial plant symbionts can influence interactions between their plant hosts and other organisms. However, such effects remain poorly understood, particularly under ecologically realistic conditions where plants simultaneously interact with diverse mutualists and antagonists. Here, we examine how the effects of a plant virus on indirect plant defences against its insect vector are influenced by co-occurrence of other microbial plant symbionts. Using a multi-factorial design, we manipulated colonization of soya bean using three different microbes: a pathogenic plant virus (bean pod mottle virus (BPMV)), a nodule-forming beneficial rhizobacterium ( Bradyrhizobium japonicum ) and a plant growth-promoting rhizobacterium ( Delftia acidovorans ). We then assessed recruitment of parasitoids ( Pediobious foveolatus (Eulophidae)) and parasitism rates following feeding by the BPMV vector Epilachna varivestis (Coccinellidae). BPMV infection suppressed parasitoid recruitment, prolonged parasitoid foraging time and reduced parasitism rates in semi-natural foraging assays. However, simultaneous colonization of BPMV-infected hosts by both rhizobacteria restored parasitoid recruitment and rates of parasitism to levels similar to uninfected controls. Co-colonization by the two rhizobacteria also enhanced parasitoid recruitment in the absence of BPMV infection. These results illustrate the potential of plant-associated microbes to influence indirect plant defences, with implications for disease transmission and herbivory, but also highlight the potential complexity of such interactions.