Previous studies have shown that vector-borne pathogens can alter the phenotypes of their hosts and vectors in ways that influence the frequency and nature of interactions between them, with significant implications for the transmission and spread of disease. For insect-borne pathogens, host odors are particularly likely targets for manipulation, because both plant-and animal-feeding insects use volatile compounds derived from their hosts as key foraging cues. Here, we document the effects of a widespread plant pathogen, Cucumber mosaic virus (CMV), on the quality and attractiveness of one of its host plants (Cucurbita pepo cv. Dixie) for two aphid vectors, Myzus persicae and Aphis gossypii. Our results indicate that CMV greatly reduces host-plant quality-aphids performed poorly on infected plants and rapidly emigrated from them-but increases the attractiveness of infected plants to aphids by inducing elevated emissions of a plant volatile blend otherwise similar to that emitted by healthy plants. Thus, CMV appears to attract vectors deceptively to infected plants from which they then disperse rapidly, a pattern highly conducive to the nonpersistent transmission mechanism employed by CMV and very different from the pattern previously reported for persistently transmitted viruses that require sustained aphid feeding for transmission. In addition to providing a documented example of a pathogen inducing a deceptive signal of host-plant quality to vectors, our results suggest that the transmission mechanism is a major factor shaping pathogen-induced changes in host-plant phenotypes. Furthermore, our findings yield a general hypothesis that, when vector-borne plant or animal pathogens reduce host quality for vectors, pathogen-induced changes in host phenotypes that enhance vector attraction frequently will involve the exaggeration of existing host-location cues.Cucumber mosaic virus | odor cues | parasite manipulation | pathogens | plant volatiles V ector-borne parasites can induce changes in the traits of their primary hosts that affect the frequency and nature of interactions between hosts and vectors (1-7). These changes can strongly influence rates of disease transmission and thus have significant implications for ecology, agriculture, and human health (4,7,8). A large body of literature has debated the criteria by which such parasite-induced changes in host phenotypes may be classified as manipulative adaptations or as by-products of infection coincidentally beneficial to the parasite (9, 10) and has further debated which, if either, of these possibilities should be considered parsimonious when conclusive evidence is lacking (10). Although adaptation for the purpose of manipulation (or the absence of such adaptation) can be difficult to establish firmly, it seems clear that natural selection will rarely be indifferent to pathological effects of infection that significantly influence parasite transmission (10, 11). Thus, it is reasonable to explore whether otherwise similar parasites that differ in their mode of ...
Summary1. Vector-borne pathogens and parasites can induce changes in the phenotypes of their hosts that influence the frequency and nature of host-vector interactions and hence transmission, as documented by both empirical and theoretical studies. To the extent that implications for transmission play a significant role in shaping the evolution of parasite effects on host phenotypes, we may hypothesize that parasites exhibiting similar transmission mechanisms -and thus profiting from similar patterns of interaction among hosts and vectors -will have correspondingly similar effects on relevant host traits. Here, we explore this hypothesis through a survey and synthesis of literature on interactions among plant viruses, their hosts, and insect vectors. 2. Insect-vectored plant viruses that differ in their modes of transmission benefit from different patterns of interaction among host plants and vectors. The transmission of persistently transmitted (PT) viruses requires that vectors feed on an infected host for a sustained period to acquire and circulate (and sometimes replicate) virions, then disperse to a new, healthy host. In contrast, non-persistently transmitted (NPT) viruses are effectively transmitted when vectors briefly probe infected hosts, acquiring virions, then rapidly disperse. 3. Based on these observations, and empirical evidence from our previous work, we hypothesized that PT and NPT viruses will exhibit different effects on aspects of host phenotypes that mediate vector attraction to, arrestment on and dispersal from infected plants. Specifically, we predicted that both PT and NPT viruses would tend to enhance vector attraction to infected hosts, but that they would have contrasting effects on vector settling and feeding preferences and on vector performance, with PT viruses tending to improve host quality for vectors and promote long-term feeding and NPT viruses tending to reduce plant quality and promote rapid dispersal. 4. We evaluated these hypotheses through an analysis of existing literature and found patterns broadly consistent with our expectations. This literature synthesis, together with evidence from other disease systems, suggests that transmission mechanisms may indeed be an important factor influencing the manipulative strategies of vector-borne pathogens, with significant implications for managing viral diseases in agriculture and understanding their impacts on natural plant communities.
Plant viruses possess adaptations for facilitating acquisition, retention, and inoculation by vectors. Until recently, it was hypothesized that these adaptations are limited to virus proteins that enable virions to bind to vector mouthparts or invade their internal tissues. However, increasing evidence suggests that viruses can also manipulate host plant phenotypes and vector behaviors in ways that enhance their own transmission. Manipulation of vector-host interactions occurs through virus effects on host cues that mediate vector orientation, feeding, and dispersal behaviors, and thereby, the probability of virus transmission. Effects on host phenotypes vary by pathosystem but show a remarkable degree of convergence among unrelated viruses whose transmission is favored by the same vector behaviors. Convergence based on transmission mechanism, rather than phylogeny, supports the hypothesis that virus effects are adaptive and not just by-products of infection. Based on this, it has been proposed that viruses manipulate hosts through multifunctional proteins that facilitate exploitation of host resources and elicitation of specific changes in host phenotypes. But this proposition is rarely discussed in the context of the numerous constraints on virus evolution imposed by molecular and environmental factors, which figure prominently in research on virus-host interactions not dealing with host manipulation. To explore the implications of this oversight, we synthesized available literature to identify patterns in virus effects among pathogens with shared transmission mechanisms and discussed the results of this synthesis in the context of molecular and environmental constraints on virus evolution, limitations of existing studies, and prospects for future research.
The transmission of insect-vectored diseases entails complex interactions among pathogens, hosts and vectors. Chemistry plays a key role in these interactions; yet, little work has addressed the chemical ecology of insect-vectored diseases, especially in plant pathosystems. Recently, we documented effects of Cucumber mosaic virus (CMV) on the phenotype of its host (Cucurbita pepo) that influence plant-aphid interactions and appear conducive to the non-persistent transmission of this virus. CMV reduces host-plant quality for aphids, causing rapid vector dispersal. Nevertheless, aphids are attracted to the elevated volatile emissions of CMV-infected plants. Here, we show that CMV infection (1) disrupts levels of carbohydrates and amino acids in leaf tissue (where aphids initially probe plants and acquire virions) and in the phloem (where long-term feeding occurs) in ways that reduce plant quality for aphids; (2) causes constitutive up-regulation of salicylic acid; (3) alters herbivore-induced jasmonic acid biosynthesis as well as the sensitivity of downstream defences to jasmonic acid; and (4) elevates ethylene emissions and free fatty acid precursors of volatiles. These findings are consistent with previously documented patterns of aphid performance and behaviour and provide a foundation for further exploration of the genetic mechanisms responsible for these effects and the evolutionary processes that shape them.
The ecological consequences of inter-individual variation in plant volatile emissions remain largely unexplored. We examined the effects of inbreeding on constitutive and herbivore-induced volatile emissions in horsenettle (Solanum carolinense L.) and on the composition of the insect community attracted to herbivore-damaged and undamaged plants in the field. Inbred plants exhibited higher constitutive emissions, but weaker induction of volatiles following herbivory. Moreover, many individual compounds previously implicated in the recruitment of predators and parasitoids (e.g. terpenes) were induced relatively weakly (or not at all) in inbred plants. In trapping experiments, undamaged inbred plants attracted greater numbers of generalist insect herbivores than undamaged outcrossed plants. But inbred plants recruited fewer herbivore natural enemies (predators and parasitoids) when damaged. Taken together, these findings suggest that inbreeding depression negatively impacts the overall pattern of volatile emissions - increasing the apparency of undamaged plants to herbivores, while reducing the recruitment of predatory insects to herbivore-damaged plants.
Vector-borne plant pathogens frequently alter host-plant quality and associated plant cues in ways that influence vector recruitment and pathogen acquisition. Furthermore, following acquisition by the vector, pathogens may influence subsequent vector behavior either directly or via effects on the host plant. Given that such effects have significant implications for pathogen acquisition and inoculation, selection might be expected to favor patterns of pathogen effects on host-vector interactions that are conducive to transmission. Consequently, we might also expect to observe broad similarity in the effects of pathogens sharing similar modes of transmission. Here we discuss some specific hypotheses arising from these expectations and the implications of recent empirical findings. On the whole, this evidence is consistent with the expectation that pathogen effects on host-vector interactions are often (though not always) adaptive with respect to transmission.
Recent research suggests that plant viruses, and other pathogens, frequently alter host-plant phenotypes in ways that facilitate transmission by arthropod vectors. However, many viruses infect multiple hosts, raising questions about whether these pathogens are capable of inducing transmission-facilitating phenotypes in phylogenetically divergent host plants and the extent to which evolutionary history with a given host or plant community influences such effects. To explore these issues, we worked with two newly acquired field isolates of cucumber mosaic virus (CMV)-a widespread multi-host plant pathogen transmitted in a non-persistent manner by aphids-and explored effects on the phenotypes of different host plants and on their subsequent interactions with aphid vectors. An isolate collected from cultivated squash fields (KVPG2-CMV) induced in the native squash host (Cucurbita pepo) a suite of effects on host-vector interactions suggested by previous work to be conducive to transmission (including reduced host-plant quality for aphids, rapid aphid dispersal from infected to healthy plants, and enhanced aphid attraction to the elevated emission of a volatile blend similar to that of healthy plants). A second isolate (P1-CMV) collected from cultivated pepper (Capsicum annuum) induced more neutral effects in its native host (largely exhibiting non-significant trends in the direction of effects seen for KVPG2-CMV in squash). When we attempted cross-host inoculations of these two CMV isolates (KVPG2-CMV in pepper and P1-CMV in squash), P1-CMV was only sporadically able to infect the novel host; KVPG2-CMV infected the novel pepper host with somewhat reduced success compared with its native host and reached virus titers significantly lower than those observed for either strain in its native host. Furthermore, KVPG2-CMV induced changes in the phenotype of the novel host, and consequently in host-vector interactions, dramatically different than those observed in the native host and apparently maladaptive with respect to virus transmission (e.g., host plant quality for aphids was significantly improved in this instance, and aphid dispersal was reduced). Taken together, these findings provide evidence of adaption by CMV to local hosts (including reduced infectivity and replication in novel versus native hosts) and further suggest that such adaptation may extend to effects on host-plant traits mediating interactions with aphid vectors. Thus, these results are consistent with the hypothesis that virus effects on host-vector interactions can be adaptive, and they suggest that multi-host pathogens may exhibit adaptation with respect to these and other effects on host phenotypes, perhaps especially in homogeneous monocultures.
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