The phytosanitary emergency caused by the spread of Xylella fastidiosa in the Mediterranean has raised demands for a better understanding of the ecology of its presumed and candidate insect vectors. Here, we present the results of a two-year survey carried out in olive groves across southern, eastern and Central Spain and northeastern Portugal. Several sampling methods were tested and compared to select the most appropriate to estimate population levels of potential vectors of X. fastidiosa. The spittlebugs Philaenus spumarius and Neophilaenus campestris (Hemiptera: Aphrophoridae) were the main species associated with olive groves. Both species were widely present on herbaceous ground vegetation within the olive groves; P. spumarius mainly associated with Asteraceae and N. campestris with Poaceae. Due to the patchy distribution of spittlebugs within the olive groves, sweep nets were the most effective and least time-consuming sampling method for the estimation of population size both in the ground cover and tree canopies. Trends in population density showed that spittlebugs can be abundant on ground vegetation but very rare on olive canopies. Spittlebugs disperse in late spring to non-cultivated hosts that act as natural reservoirs. In late fall, adults return to the olive groves for oviposition. However, olive trees may act as transient hosts for spittlebugs and high population densities of these insect vectors should be avoided in areas where X. fastidiosa is present.
Plant pathogens are able to influence the behaviour and fitness of their vectors in such a way that changes in plant-pathogen-vector interactions can affect their transmission. Such influence can be direct or indirect, depending on whether it is mediated by the presence of the pathogen in the vector's body or by host changes as a consequence of pathogen infection. We report the effect that the persistently aphid-transmitted Cucurbit aphid-borne yellows virus (CABYV, Polerovirus) can induce on the alighting, settling and probing behaviour activities of its vector, the cotton aphid Aphis gossypii. Only minor direct changes on aphid feeding behaviour were observed when viruliferous aphids fed on non-infected plants. However, the feeding behaviour of non-viruliferous aphids was very different on CABYV-infected than on non-infected plants. Non-viruliferous aphids spent longer time feeding from the phloem in CABYV-infected plants compared to non-infected plants, suggesting that CABYV indirectly manipulates aphid feeding behaviour through its shared host plant in order to favour viral acquisition. Viruliferous aphids showed a clear preference for non-infected over CABYV-infected plants at short and long time, while such behaviour was not observed for non-viruliferous aphids. Overall, our results indicate that CABYV induces changes in its host plant that modifies aphid feeding behaviour in a way that virus acquisition from infected plants is enhanced. Once the aphids become viruliferous they prefer to settle on healthy plants, leading to optimise the transmission and spread of this phloem-limited virus.
The genetic variability of a Cucurbit aphid-borne yellows virus (CABYV) (genus Polerovirus, family Luteoviridae) population was evaluated by determining the nucleotide sequences of two genomic regions of CABYV isolates collected in open-field melon and squash crops during three consecutive years in Murcia (southeastern Spain). A phylogenetic analysis showed the existence of two major clades. The sequences did not cluster according to host, year, or locality of collection, and nucleotide similarities among isolates were 97 to 100 and 94 to 97% within and between clades, respectively. The ratio of nonsynonymous to synonymous nucleotide substitutions reflected that all open reading frames have been under purifying selection. Estimates of the population's genetic diversity were of the same magnitude as those previously reported for other plant virus populations sampled at larger spatial and temporal scales, suggesting either the presence of CABYV in the surveyed area long before it was first described, multiple introductions, or a particularly rapid diversification. We also determined the full-length sequences of three isolates, identifying the occurrence and location of recombination events along the CABYV genome. Furthermore, our field surveys indicated that Aphis gossypii was the major vector species of CABYV and the most abundant aphid species colonizing melon fields in the Murcia (Spain) region. Our surveys also suggested the importance of the weed species Ecballium elaterium as an alternative host and potential virus reservoir.
Identification of the determinants of pathogen reservoir potential is central to understand disease emergence. It has been proposed that host lifespan is one such determinant: short-lived hosts will invest less in costly defenses against pathogens, so that they will be more susceptible to infection, more competent as sources of infection and/or will sustain larger vector populations, thus being effective reservoirs for the infection of long-lived hosts. This hypothesis is sustained by analyses of different hosts of multihost pathogens, but not of different genotypes of the same host species. Here we examined this hypothesis by comparing two genotypes of the plant Arabidopsis thaliana that differ largely both in life-span and in tolerance to its natural pathogen Cucumber mosaic virus (CMV). Experiments with the aphid vector Myzus persicae showed that both genotypes were similarly competent as sources for virus transmission, but the short-lived genotype was more susceptible to infection and was able to sustain larger vector populations. To explore how differences in defense against CMV and its vector relate to reservoir potential, we developed a model that was run for a set of experimentally-determined parameters, and for a realistic range of host plant and vector population densities. Model simulations showed that the less efficient defenses of the short-lived genotype resulted in higher reservoir potential, which in heterogeneous host populations may be balanced by the longer infectious period of the long-lived genotype. This balance was modulated by the demography of both host and vector populations, and by the genetic composition of the host population. Thus, within-species genetic diversity for lifespan and defenses against pathogens will result in polymorphisms for pathogen reservoir potential, which will condition within-population infection dynamics. These results are relevant for a better understanding of host-pathogen co-evolution, and of the dynamics of pathogen emergence.
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