Supplementary Materials
Detailed methods for literature selection and analysis
Using Google Scholar, we employed combinations of broad search terms (e.g., virus-host-vector
interactions, plant virus, insect vector, non-persistently transmitted virus, persistent-circulative virus,
persistent-propagative virus, plant virus chemical ecology, vector behavior, vector performance) and
specific search terms (family and species names of viruses and their vectors) to identify a primary set of
literature that examined any aspect of insect vector attraction, settling and feeding, and performance in
relation to infected and healthy plants. References cited within each identified paper were then
assessed to identify additional papers addressing these three interactions. Finally, this expanded set of
papers was re-entered into Google Scholar to identify still other papers that cited this literature. We
believe that this sampling procedure, combining both search terms and human assessment of additional
literature, was adequate to capture a large proportion of the relevant peer-reviewed literature. Our final
list comprised 55 individual papers (studies of PT viruses were considerably better represented in this
study, as only 14 of the 55 studies examined NPT viruses). Working with this literature, we parsed each
study into individual experiments, each addressing a single virus strain or isolate by host species (or
cultivar) by vector interaction (224 experiments total). All experiments in the 55 papers were included in
this total except (i) those employing transgenic plants expressing viral genes (a subset of experiments
from Jiménez-Martínez et al. 2004 a&b and Medina-Ortega et al. 2009)—because the expression of viral
genes by transgenic plants may influence virus-vector-plant interactions and thereby confound results
(Jiménez-Martínez et al. 2004 a&b); and (ii) those employing vector responses to macerated plant tissue
extracts as sources of odor cues (some experiments in Fereres, Kampmeier & Irwin 1999)—because such
extracts are not necessarily good approximations of the cues available to vectors in nature. Additionally,
we did not include one paper where the authors did not identify the virus species and family (Kennedy
1951, Nature 168: 825-826), one paper where the host plant was bypassed and vectors were injected
with virions to make them viruliferous (as this may have unintended effects on vector physiology)
(Sylvester and Richardson 1969, Virology 37: 26-31), and one paper (Stumpf and Kennedy 2005) where
the inclusion of a large number of biotic and abiotic factors in the analysis (and inconsistent pooling of
data across these factors) prevented us from drawing conclusions about the overall effects of each virus
isolate on a thrips vector (the isolates are instead represented in our analysis by the later Stumpf and
Kennedy 2007 paper). Virus strains or serotypes in our synthesis were designated according to the
names provided by the authors, including standard (e.g. BYDV strain MAV [BYDV-MAV]) or alternative
(e.g. “CMV-common” from common strain of CMV) naming conventions. Isolates for which strain names
were not provided were designated by the location where the study was performed (e.g. PLRV used in
studies performed at Wageningen University was called PLRV-Wageningen to distinguish it from the
PLRV isolate used in studies at the University of Idaho). Otherwise, strains were designated “unknown”
(e.g. “PVY-unknown” for unidentified Potato virus Y) or named for the host from which they were
isolated (if stated).
Each of the 224 experiments identified was categorized as pertaining to one of the three types of
virus-host-vector effects (attraction, settling and feeding, and performance) that related to the three
hypotheses presented above. Results of each were then further categorized based on outcomes: For
experiments measuring attraction or settling and feeding, results were categorized as demonstrating a
vector preference for virus-infected plants, a preference for healthy plants, or no preference. For assays
of vector performance, results were categorized as indicating a positive, neutral, or negative effect on
vector performance (i.e., development, survival, or fecundity). Where equal numbers of positive and
negative effects were observed in a single experiment, the experiment was categorized as neutral (for
example, an aphid vector has slightly higher fecundity on virus infected plants, but significantly lower
longevity). In the absence of further knowledge of the ecology of the organisms involved, it is difficult to
determine the relative contributions of different performance parameters to overall virus transmission
and our approach to dealing with conflicting measures in a single experiment is the most conservative.
Results for each transmission mechanism are presented as the number of experiments falling into each
category within the three virus-host-vector interactions (Figs 2 through 4; Supplementary Tables 1
through 3). We have also color-coded individual virus species in our figures to reveal the extent to which
overrepresentation of particular interactions may contribute to the overall pattern observed. Tabulated
results were evaluated for departure from an expected even distribution of effects (positive: neutral:
negative, or virus-infected: no preference: healthy) across the three interaction types using chi-square
tests (see figure captions). To examine the distribution of experiments among different plant virus
lineages in the categories of vector performance and vector settling and feeding preference, results are
presented based on virus taxonomy in Table 1.
Supplementary Table 1: References used to construct Figure 2, virus identifiers, and pathosystems
described in each reference.
(Full citations for Supplementary Tables 1-3 can be found at the end of this document)
Supplementary Table 2: References used to construct Figure 3, virus identifiers, and pathosystems
described in each reference.
Supplementary Table 3: References used to construct Figure 4, virus identifiers, and pathosystems
described in each reference.
References employed in our analyses and used to construct Supplementary Tables 1-3 (and Figures 2-4
in the main text).
Ajayi, O. & Dewar, A.M. (1983) The effect of barley yellow dwarf virus on field populations of the cereal
aphids, Sitobion avenae and Metopolophium dirhodum. Annals of Applied Biology, 103, 1-11.
Araya, J.E. & Foster, J.E. (1987) Laboratory study on the effects of barley yellow dwarf virus on the life
cycle of Rhopalosiphum padi (L.). Zeitschrift fuer Pflanzenkrankheiten und Pflanzenschutz, 94,
578-583.
Alvarez, A.E., Garzo, E., Verbeek, M., Vosman, B., Dicke, M. & Tjallingii, W.F. (2007) Infection of potato
plants with potato leafroll virus changes attraction and feeding behaviour of Myzus persicae.
Entomologia Experimentalis et Appicata, 125, 135-144.
Baker, P.F. (1960) Aphid behavior on healthy and on yellows-virus-infected sugar beet. Annals of
Applied Biology, 48, 384-391.
Bautista, R.C., Mau, R.F.L., Cho, J.J. & Custer, D.M. (1995) Potential of tomato spotted wilt tospovirus
plant hosts in Hawaii as virus reservoirs for transmission by Franklinella occidentalis. Phytopathology,
85, 953-958.
Belliure, B., Janssen, A., Maris, P.C., Peters, D. & Sabelis, M.W. (2005) Herbivore arthropods benefit from
vectoring plant viruses. Ecology Letters, 8, 70-79.
Belliure, B., Janssen, A. & Sabelis, M.W. (2008) Herbivore benefits from vectoring plant virus through
reduction of period of vulnerability to predation. Oecologia, 156, 797-806.
Blua, M.J. & Perring, T.M. (1992a) Alatae production and population increase of aphid vectors on virusinfected host plants. Oecologia, 92, 65–70.
Blua, M.J. & Perring, T.M. (1992b) Effects of zucchini yellow mosaic virus on colonization and feeding
behavior of Aphis gossypii (Homoptera, Aphididae) alatae. Environmental Entomology, 21, 578-585.
Blua, M.J., Perring, P.A. & Madore, M.A. (1994) Plant virus-induced changes in aphid population
development and temporal fluctuations in plant nutrients. Journal of Chemical Ecology, 20, 691–707.
Castle, S. J. & Berger, P.H. (1993) Rates of growth and increase of Myzus persicae on virus-infected
potatoes according to type of virus-vector relationship. Entomologia Experimentalis et Applicata, 69,
51-60.
Castle, S.J., Mowry, T.M. & Berger, P.H. (1998) Differential settling by Myzus persicae (Homoptera,
Aphididae) on various virus-infected host plants. Annals of the Entomological Society of America,
91, 661-667.
Costa, H.S., Brown, J.K. & Byrne, D.N. (1991) Life history traits of the whitefly, Bemisia tabaci
(Homoptera, Aleyrodidae) on six virus-infected or healthy plant species. Environmental Entomology,
20, 1103-1107.
DeAngelis, J.D., Sether, D.M. & Rossignol, P.A. (1993) Survival, development, and reproduction in
western flower thrips (Thysanoptera, Thripidae) exposed to impatiens necrotic spot virus.
Environmental Entomology, 22, 1308-1312.
Donaldson, J.R. & Gratton, C. (2007) Antagonistic effects of soybean viruses on soybean aphid
performance. Environmental Entomology, 34, 918-925.
Eckel, W., Randi, V. & Lampert, E.P. (1996) Relative attractiveness of Tobacco etch virus-infected and
healthy flue-cured tobacco plants to aphids (Homoptera, Aphididae). Journal of Economic
Entomology, 89, 1017-1027.
Eigenbrode, S.D., Ding, H., Shiel, P. & Berger, P.H. (2002) Volatiles from potato plants infected with
Potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera, Aphididae).
Proceedings of the Royal Society of London B, 269, 455-460.
Ellsbury, M.M., Pratt, R.G. & Knight, W. (1985) Effects of single and combined infection of arrowleaf
clover with Bean yellow mosaic virus and a Phytophthora sp on reproduction and colonization by pea
aphids (Homoptera, Aphididae). Environmental Entomology, 14, 356-359.
Fereres, A., Kampmeier, G.E. & Irwin, M.E. (1999) Aphid attraction and preference for soybean and
pepper plants infected with potyviridae. Annals of the Entomological Society of America, 92, 542548.
Fereres, A., Lister, R.M., Araya, J.E. & Foster, J.E. (1989) Development and reproduction of the English
grain aphid (Homoptera, Aphididae) on wheat cultivars infected with Barley yellow dwarf virus.
Environmental Entomology, 18, 388-393.
Fereres, A., Shukle, R.H., Araya, J.E. & Foster, J.E. (1990) Probing and feeding behavior of Sitobion
avenae (F) (Hom., Aphididae) on three cultivars infected with Barley yellow dwarf virus. Journal of
Applied Entomology, 109, 29-36.
Fiebig, M., Poehling, H.M. & Borgemeister, C. (2004) Barley yellow dwarf virus, wheat, and Sitobion
avenae: a case of trilateral interactions. Entomologia Experimentalis et Applicata, 110, 11-21.
Guo, J.Y., Ye, G.Y., Dong, S.Z. & Liu, S.S. (2010) An invasive whitefly feeding on a virus-infected plant
increased its egg production and realized fecundity. PLoS ONE, 5, e11713.
Hodge, S. & Powell, G. (2008) Do plant viruses facilitate their aphid vectors by inducing symptoms that
alter behavior and performance? Environmental Entomology, 37, 1573-1581.
Hodge, S., Hardie, J. & Powell, G. (2010) Parasitoids aid dispersal of a non-persistently transmitted plant
virus by disturbing the aphid vector. Agricultural and Forest Entomology, 13, 83-88.
Hodgson, C. J. (1981) Effects of infection with the cabbage black ringspot strain of Turnip mosaic virus
on turnip as a host to Myzus persicae and Brevicoryne brassicae. Annals of Applied Biology, 98, 114.
Jiménez-Martínez, E.S., Bosque-Pérez, N.A., Berger, P.H. & Zemetra, R.S. (2004a) Life history of the bird
cherry-oat aphid, Rhopalosipum padi (Homoptera, Aphididae), on transgenic and untransformed
wheat challenged with Barley yellow dwarf virus. Journal of Economic Entomology, 97, 203-212.
Jiménez-Martínez, E.S., Bosque-Pérez, N.A., Berger, P.H., Zemetra, R.S., Ding, H. & Eigenbrode, S.D.
(2004b) Volatile cues influence the response of Rhopalosiphum padi (Homoptera, Aphididae) to
Barley yellow dwarf virus-infected transgenic and untransformed wheat. Environmental
Entomology, 33, 1207-1216.
Jiu, M., Zhou, X.P., Tong, L., Xu, J., Yang, X., Wan, F.H. & Liu, S.S. (2007) Vector-virus mutualism
accelerates population increase of an invasive whitefly. PLoS ONE, 2, e182.
Lowe, S. & Strong, F.E. (1963) The unsuitability of some viruliferous plants as hosts for the green peach
aphid, Myzus persicae. Journal of Economic Entomology, 56, 308-309.
Liu, L., Zhao, H., Jiang, K., Zhou, X.P. & Liu, S.S. (2009) Differential indirect effects of two plant viruses on
an invasive and an indigenous whitefly vector, implications for competitive displacement. Annals of
Applied Biology, 155, 439-448.
Liu, J., Li, M., Li, J.M., Huang, C.J., Zhou, X.P., Xu, F.C. & Liu, S.S. (2010) Viral infection of tobacco plants
improves performance of Bemisia tabaci but more so for an invasive than for an indigenous biotype of
the whitefly. Journal of Zhejiang University-Science B (Biomedicine and Biotechnology), 11, 3040.
Macias, W. & Mink, G.I. (1969) Preference of green peach aphids for virus-infected sugarbeet leaves.
Journal of Economic Entomology, 62, 28–29.
Mann, R.S., Sidhu, J.S., Butter, N.S., Sohi, A.S. & Sekhon, P.S. (2008) Performance of Bemisia tabaci
(Hemiptera, Aleyrodidae) on healthy and Cotton leaf curl virus infected cotton. The Florida
Entomologist, 91, 249-255.
Maris, P.C., Joosten, N.N., Goldbach, R.W. & Peters, D. (2004) Tomato spotted wilt virus infection
improves host suitability for its vector Frankliniella occidentalis. Phytopathology, 94, 706-711.
Mauck, K.E., De Moraes, C.M. & Mescher, M.C. (2010) Deceptive chemical signals induced by a plant
virus attract insect vectors to inferior hosts. Proceedings of the National Academy of Sciences, 107,
3600-3605.
Mayer, R.T., Inbar, M., McKenzie, C.L., Shatters, R., Borowicz, V., Albrecht, U., Powell, C.A. & Doostdar,
H. (2002) Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivores, and
phytopathogens. Archives of Insect Biochemistry and Physiology, 51, 151-169.
McKenzie, C.L. (2002) Effect of Tomato mottle virus (ToMoV) on Bemisia tabaci Biotype B
(Homoptera, Aleyrodidae) oviposition and adult survivorship on healthy tomato. Florida Entomologist,
85, 367-368.
Medina-Ortega, K.J., Bosque-Perez, N.A., Ngumbi, E., Jiménez-Martínez, E.S. & Eigenbrode, S.D. (2009)
Rhopalosiphum padi (Hemiptera, Aphididae) responses to volatile cues from Barley yellow dwarf
virus–infected wheat. Environmental Entomology, 38, 836-845.
Mesfin, T. & Bosque-Pérez, N.A. (1998) Feeding behaviour of Cicadulina storeyi China (Homoptera ,
Cicadellidae) on maize varieties susceptible or resistant to Maize streak virus. African Entomology, 6,
185-191.
Montllor, C.B. & Gildow, F.E. (1986) Feeding responses of two grain aphids to Barley yellow dwarf
virus-infected oats. Entomologia Experimentalis et Applicata, 42, 63-69.
Mowry, T. (1994) Russian wheat aphid (Homoptera, Aphididae) survival and fecundity on Barley yellow
dwarf virus-infected wheat resistant and susceptible to the aphid. Environmental Entomology, 23,
326-330.
Musser, R.O., Hum-Musser, S.M., Felton, G.W. & Gergerich, R.C. (2003) Increased larval growth and
preference for virus-infected leaves by the Mexican bean beetle, Epilachna varivestis Mulsant, a plant
virus vector. Journal of Insect Behavior, 16, 247-256.
Ngumbi, E., Eigenbrode, S.D., Bosque-Pérez, N.A., Ding, H. & Rodriguez, A. (2007) Myzus persicae is
arrested more by blends than by individual compounds elevated in headspace of PLRV-infected potato.
Journal of Chemical Ecology, 33, 1733-1747.
Ponsen, M.B. (1969) The effect of Potato leafroll virus on the biology of Myzus persicae. European
Journal of Plant Pathology, 75, 360-368.
Poulin, R. (1995) ‘‘Adaptive’’ change in the behaviour of parasitized animals, a critical review.
International Journal of Parasitology, 25, 1371–1383.
Power, A.G. (1996) Competition between viruses in a complex plant-pathogen. Ecology, 77, 1004–1010.
Rubinstein, G. & Czosnek, H. (1997) Long-term association of Tomato yellow leaf curl virus with its
whitefly vector Bemisia tabaci, effect of the insect transmission capacity, longevity and fecundity.
Journal of General Virology, 78, 2683-2689.
Srinivasan, R., Alvarez, J.M., Eigenbrode, S.D. & Bosque-Pérez, N.A. (2006) Influence of hairy
nightshade Solanum sarrachoides (Sendtner) and Potato leafroll virus (Luteoviridae, Polerovirus)
on the host preference of Myzus persicae (Sulzer) (Homoptera, Aphididae). Environmental
Entomology, 35, 546-553.
Srinivasan, R. & Alvarez, J.M. (2007) Effect of mixed viral infections (Potato virus Y-Potato leafroll
virus) on biology and preference of vectors Myzus persicae and Macrosiphum euphorbiae
(Hemiptera, Aphididae). Journal of Economic Entomology, 100, 646-655.
Stumpf, C.F. & Kennedy, G.G. (2007) Effects of Tomato spotted wilt virus isolates, host plants, and
temperature on survival, size, and development time of Frankliniella occidentalis. Entomologia
Experimentalis et Applicata, 123, 139-147.
Sylvester, E.S. (1973) Reduction of excretion, reproduction, and survival in Hyperomyzus lactucae fed
on plants infected with isolates of Sowthistle yellow vein virus. Virology, 56, 632-635.
Werner, B.J., Mowry, T.M., Bosque-Pérez, N.A., Ding, H. & Eigenbrode, S.D. (2009) Changes in green
peach aphid responses to Potato leafroll virus-induced volatiles emitted during disease progression.
Environmental Entomology, 38, 1429-1438.
Wijkamp, I., Goldbach, R. & Peters, D. (1996) Propagation of Tomato spotted wilt virus in Frankliniella
occidentalis does neither result in pathological effects nor in transovarial passage of the virus.
Entomologia Experimentalis et Applicata, 81, 285-292.
Williams, C.T. (1995) Effects of plant age, leaf age and virus yellows infection on the population
dynamics of Myzus persicae (Homoptera, Aphididae) on sugarbeet in field plots. Bulletin of
Entomological Research, 85, 557-567.