The pathogen causing Dutch elm disease makes host trees attract insect vectors

McLeod, Geoff; Gries, Regine; Reuß, Stephan H. von; Rahe, J. E.; McIntosh, Rory L.; König, Wilfried Α.

doi:10.1098/rspb.2005.3202

Cited by 68 publications

(55 citation statements)

References 22 publications

(22 reference statements)

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“…Pathogen-insect symbioses commonly play important roles in the invasion and successful spread of alien species into new environments (von Broembsen 1989, McLeod et al 2005, Lu et al 2010, Himler et al 2011. The symbiotic partners (e.g., fungi, nematodes, bacteria, or viruses) can facilitate the establishment and population increase of their insect vectors in nonnative habitats (Jiu et al 2007, Himler et al 2011.…”

Section: Introductionmentioning

confidence: 99%

A native fungal symbiont facilitates the prevalence and development of an invasive pathogen–native vector symbiosis

Zhao

Lü

Niu

et al. 2013

Ecology

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Abstract. Invasive pathogen-insect symbioses have been extensively studied in many different ecological niches. Whether the damage of symbioses in different introduced regions might be influenced by other microorganisms has, however, received little attention. Eight years of field data showed that the varied levels of the nematode and beetle populations and infested trees of the invasive Bursaphelenchus xylophilus-Monochamus alternatus symbiosis were correlated with patterns in the isolation frequencies of ophiostomatoid fungi at six sites, while the laboratory experiments showed that the nematode produced greater numbers of offspring with a female-biased sex ratio and developed faster in the presence of one native symbiotic ophiostomatoid fungus, Sporothrix sp. 1. Diacetone alcohol (DAA) from xylem inoculated with Sporothrix sp. 1 induced B. xylophilus to produce greater numbers of offspring. Its presence also significantly increased the growth and survival rate of M. alternatus, and possibly explains the prevalence of the nematode-vector symbiosis when Sporothrix sp. 1 was dominant in the fungal communities. Studying the means by which multispecies interactions contributed to biogeographical dynamics allowed us to better understand the varied levels of damage caused by biological invasion across the invaded range.

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Section: Introductionmentioning

confidence: 99%

A native fungal symbiont facilitates the prevalence and development of an invasive pathogen–native vector symbiosis

Zhao

Lü

Niu

et al. 2013

Ecology

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“…Changes in the odor cues emitted by hosts appear particularly likely to influence the transmission of insect-vectored pathogens, because both plant-and animal-feeding insects typically use volatile chemical cues to locate their hosts (16-21). Moreover, pathogen infection is known to alter host odor profiles in both plants and animals and to influence subsequent odormediated interactions between infected individuals and other organisms (3,12,(22)(23)(24)(25)(26).Relatively few studies have investigated the role of odor cues in the transmission ecology of insect-vectored diseases. Increased attraction of sandflies to Leishmania-infected hamsters was attributed to changes in host-derived volatiles (16), and it is thought that odor cues also might explain a recent report that Kenyan children harboring the transmissible gametocytes of the malaria parasite Plasmodium falciparum attracted significantly more mosquitoes than uninfected children or those harboring the nontransmissible stage of the parasite (6).…”

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confidence: 99%

Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts

Mauck

Moraes

Mescher

2010

Proc. Natl. Acad. Sci. U.S.A.

462

561

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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 ...

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“…They are caused by fungi in the Ophiostomatales, Microascales and Hypocreales, and have vectors in the Scolytinae (ambrosia and bark beetles), Platypodinae (ambrosia beetles) and Hylesininae (bark beetles) subfamilies of the Curculionidae (Coleoptera) (73,102,144). Some of these problems, such as Dutch elm disease (DED), have a long history, have been extensively researched, and are fairly well understood (23,56,70,113,149,168,169). In contrast, other similar diseases developed recently and are poorly or partially understood (2,3,42,51,73,89,94,98,114,127,137,154,158, 164,165).…”

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confidence: 99%

Destructive Tree Diseases Associated with Ambrosia and Bark Beetles: Black Swan Events in Tree Pathology?

et al. 2013

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Diseases that are associated with ambrosia and bark beetles comprise some of the most significant problems that have emerged on trees in the last century. They are caused by fungi in the Ophiostomatales, Microascales and Hypocreales, and have vectors in the Scolytinae (ambrosia and bark beetles), Platypodinae (ambrosia beetles) and Hylesininae (bark beetles) subfamilies of the Curculionidae (Coleoptera) (73,102,144). Some of these problems, such as Dutch elm disease (DED), have a long history, have been extensively researched, and are fairly well understood (23,56,70,113,149,168,169). In contrast, other similar diseases developed recently and are poorly or partially understood (2,3,42,51,73,89,94,98,114,127,137,154,158, 164,165). Significant data gaps may exist for the ecology, epidemiology and management of the latter diseases.The emergence and unexpected importance of these tree diseases are discussed in thisarticle. An underlying factor in most of these interactions is the absence of a coevolved history between the so-called "naïve" or "new encounter" host trees and the pathogens and/or beetles (27,128,174). For the ambrosia beetles, these interactions are associated with susceptibility to what are typically benign fungi and atypical relationships with healthy trees (ambrosia beetles favor trees that are dead or stressed). Interestingly, the pathogens for both the ambrosia and bark beetle-associated diseases often have symbiotic relationships with the insects that are not based on phytopathogenicity. Some of the most alarming and damaging of these diseases are considered below as "black swan events" (155).Black Swans. Before 1697, improbable events and situations in Europe were known as "black swans" (at the time, all swans known to Europeans were white) (134). In that year, the black swan, Cygnus atratus, was discovered in Western Australia (38). Thereafter, "black swan" developed as a metaphor for a supposed impossibility that is contradicted with new information.For example, John Stuart Mill used black swan logical fallacy when identifying falsification, a key component in the scientific method (68).In a recent book, Taleb (155) developed Black Swan Theory (BST). Unlike the "black swan" to which Mill referred (68), BST focuses on unexpected events of large magnitude and consequence (155). Taleb (155) recognized such events in diverse fields including finance, history, science and technology. He suggested that black swan events: 1) have extreme impacts; 2) lie outside the realm of regular expectations (they are rare); and 3) are unpredictable.Although all ambrosia and bark beetle-associated diseases are not black swan events, several do fulfill the above criteria since they have large impacts, are uncommon surprises and are unpredictable (2,3,51,56,73,89,94,98,114,137,154,158, 164,165) (Table 1). They are typically understood and appreciated only with the benefit of hindsight and subsequent research.The Beetles and Beetle-associated Tree Diseases. The order Coleoptera contains more species than any other or...

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The pathogen causing Dutch elm disease makes host trees attract insect vectors

Cited by 68 publications

References 22 publications

A native fungal symbiont facilitates the prevalence and development of an invasive pathogen–native vector symbiosis

A native fungal symbiont facilitates the prevalence and development of an invasive pathogen–native vector symbiosis

Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts

Destructive Tree Diseases Associated with Ambrosia and Bark Beetles: Black Swan Events in Tree Pathology?

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