Interactions between a spider mite and a virus revealed via effects on their host plant

Interactions between a spider mite and a virus revealed via effects on their host plant | bioRxiv /* */ /* */ <!-- <!-- /*! * yepnope1.5.4 * (c) WTFPL, GPLv2 */ (function(a,b,c){function d(a){return"[object Function]"==o.call(a)}function e(a){return"string"==typeof a}function f(){}function g(a){return!a||"loaded"==a||"complete"==a||"uninitialized"==a}function h(){var a=p.shift();q=1,a?a.t?m(function(){("c"==a.t?B.injectCss:B.injectJs)(a.s,0,a.a,a.x,a.e,1)},0):(a(),h()):q=0}function i(a,c,d,e,f,i,j){function k(b){if(!o&&g(l.readyState)&&(u.r=o=1,!q&&h(),l.onload=l.onreadystatechange=null,b)){"img"!=a&&m(function(){t.removeChild(l)},50);for(var d in y[c])y[c].hasOwnProperty(d)&&y[c][d].onload()}}var j=j||B.errorTimeout,l=b.createElement(a),o=0,r=0,u={t:d,s:c,e:f,a:i,x:j};1===y[c]&&(r=1,y[c]=[]),"object"==a?l.data=c:(l.src=c,l.type=a),l.width=l.height="0",l.onerror=l.onload=l.onreadystatechange=function(){k.call(this,r)},p.splice(e,0,u),"img"!=a&&(r||2===y[c]?(t.insertBefore(l,s?null:n),m(k,j)):y[c].push(l))}function j(a,b,c,d,f){return q=0,b=b||"j",e(a)?i("c"==b?v:u,a,b,this.i++,c,d,f):(p.splice(this.i++,0,a),1==p.length&&h()),this}function k(){var a=B;return a.loader={load:j,i:0},a}var l=b.documentElement,m=a.setTimeout,n=b.getElementsByTagName("script")[0],o={}.toString,p=[],q=0,r="MozAppearance"in l.style,s=r&&!!b.createRange().compareNode,t=s?l:n.parentNode,l=a.opera&&"[object Opera]"==o.call(a.opera),l=!!b.attachEvent&&!l,u=r?"object":l?"script":"img",v=l?"script":u,w=Array.isArray||function(a){return"[object Array]"==o.call(a)},x=[],y={},z={timeout:function(a,b){return b.length&&(a.timeout=b[0]),a}},A,B;B=function(a){function b(a){var a=a.split("!"),b=x.length,c=a.pop(),d=a.length,c={url:c,origUrl:c,prefixes:a},e,f,g;for(f=0;f<d;f++)g=a[f].split("="),(e=z[g.shift()])&&(c=e(c,g));for(f=0;f<b;f++)c=x[f](c);return c}function g(a,e,f,g,h){var i=b(a),j=i.autoCallback;i.url.split(".").pop().split("?").shift(),i.bypass||(e&&(e=d(e)?e:e[a]||e[g]||e[a.split("/").pop().split("?")[0]]),i.instead?i.instead(a,e,f,g,h):(y[i.url]?i.noexec=!0:y[i.url]=1,f.load(i.url,i.forceCSS||!i.forceJS&&"css"==i.url.split(".").pop().split("?").shift()?"c":c,i.noexec,i.attrs,i.timeout),(d(e)||d(j))&&f.load(function(){k(),e&&e(i.origUrl,h,g),j&&j(i.origUrl,h,g),y[i.url]=2})))}function h(a,b){function c(a,c){if(a){if(e(a))c||(j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}),g(a,j,b,0,h);else if(Object(a)===a)for(n in m=function(){var b=0,c;for(c in a)a.hasOwnProperty(c)&&b++;return b}(),a)a.hasOwnProperty(n)&&(!c&&!--m&&(d(j)?j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}:j[n]=function(a){return function(){var b=[].slice.call(arguments);a&&a.apply(this,b),l()}}(k[n])),g(a[n],j,b,n,h))}else!c&&l()}var h=!!a.test,i=a.load||a.both,j=a.callback||f,k=j,l=a.complete||f,m,n;c(h?a.yep:a.nope,!!i),i&&c(i)}var i,j,l=this.yepnope.loader;if(e(a))g(a,0,l,0);else if(w(a))for(i=0;i (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0];var j=d.createElement(s);var dl=l!='dataLayer'?'&l='+l:'';j.src='//www.googletagmanager.com/gtm.js?id='+i+dl;j.type='text/javascript';j.async=true;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-M677548'); Skip to main content Home About Submit ALERTS / RSS Search for this keyword Advanced Search New Results Interactions between a spider mite and a virus revealed via effects on their host plant View ORCID Profile Vandana Gupta , Marion Szadkowski , David Carbonell , View ORCID Profile Benoît Moury , View ORCID Profile Alison B. Duncan doi: https://doi.org/10.1101/2025.09.13.675757 Vandana Gupta 1 Institut des Sciences de l’Évolution, Université de Montpellier , CNRS, IRD, Montpellier, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Vandana Gupta Marion Szadkowski 2 INRAE, Pathologie Végétale , F-84140 Montfavet, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site David Carbonell 1 Institut des Sciences de l’Évolution, Université de Montpellier , CNRS, IRD, Montpellier, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site Benoît Moury 2 INRAE, Pathologie Végétale , F-84140 Montfavet, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Benoît Moury Alison B. Duncan 1 Institut des Sciences de l’Évolution, Université de Montpellier , CNRS, IRD, Montpellier, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Alison B. Duncan For correspondence: alison.duncan{at}umontpellier.fr Abstract Full Text Info/History Metrics Supplementary material Preview PDF Synthesis Plants are commonly host to multiple parasites simultaneously. Interactions among parasites in coinfections can have consequences for both host and parasite fitness. We investigated reciprocal interactions between tomato spotted wilt virus (TSWV) and a non-vector spider mite, Tetranychus urticae , in coinfections on tomato plants. We compared the number of T. urticae emerging as adults and the virus titre of two TSWV isolates (France81 and LYE1137vir) quantified by DAS-ELISA in single and coinfections. We also measured host plant traits including height, fresh weight, chlorophyll content, and the number of flowers in both single and coinfection treatments and in uninfected control plants. Plant height, weight and number of flowers were lower for France81-infected plants than for LYE1137vir-infected and uninfected plants. This strain that was more virulent also had overall higher viral loads, but there was no direct link between viral load and host traits. We found that the most virulent TSWV isolate (France81) facilitated spider mites by increasing the number of offspring per unit of plant height. In contrast, there was no effect of T. urticae on the load of either TSWV isolate. T. urticae did however reduce plant height, thus in coinfection there was an additive effect of virulence compared to singly infected plants. Although we do not find that T. urticae impacts TSWV titre in coinfection, our results do indicate that coinfection could negatively impact both isolates via effects on virulence. Coinfection with the most virulent isolate may accelerate host death due to elevated T. urticae growth on relatively smaller plants. In addition, for both viral isolates, further reductions in plant height in coinfection, may also in time lead to increased T. urticae competition for plant resources and earlier plant death. Our results indicate the importance of simultaneously exploring the life-history traits of both parasites and the host, in single and co-infections, to get a proper idea of both potential direct and indirect effects between all players. Importantly, parasite fitness may be severely reduced via indirect effects of coinfection mediated via impacts on host virulence if the host dies sooner than in single infections. Introduction Parasite-parasite interactions in coinfections can have wide-reaching consequences for life-history traits, epidemics and evolution ( Alizon, de Roode & Michalakis 2013 ; Duncan et al . 2024 ), including in plant pathosystems ( Tollenaere, Susi & Laine 2016 ; Dutt, Andrivon & Le May 2021 ). The co-occurrence of different parasites in the same host are often non-random ( Norberg et al . 2012 ). Priority effects, whereby infection with a particular parasite changes the host environment, can increase or decrease the likelihood of infection by a second ( Halliday, Umbanhowar & Mitchell 2017 ; Karvonen, Jokela & Laine 2019 ; Fragata et al . 2022 ) and coinfection can increase onward transmission from a host ( Susi et al . 2015 ). The impact of coinfection on parasite fitness and virulence (defined here as parasite-induced harm to the host) may depend upon whether interactions are competitive or facilitative and/or the interaction mechanisms ( Alizon, de Roode & Michalakis 2013 ; Zele et al . 2018 ). Theoretical models illustrate that competition for shared host resources can result in lower, and facilitation (when it makes the host easier to exploit) in higher virulence in coinfected hosts ( Eswarappa, Estrela & Brown 2012 ). This is nicely illustrated in a meta-analysis showing that overall outcomes for microparasite load in mice is negative when they compete with helminths for the same resource (red blood cells), but positive when interactions are mediated via negative cross-talk between branches of the host immune system ( Graham 2008 ). However, theoretical models also highlight that outcomes may depend on the symmetry of the interaction ( Eswarappa, Estrela & Brown 2012 ), the functional response of the immune system to parasites ( Fenton & Perkins 2010 ) and trade-offs between different branches of the immune system ( Fenton, Lamb & Graham 2008 ). Note that outcomes for the evolution of parasite virulence in coinfections may be different ( Choisy & de Roode 2010 ; Alizon, de Roode & Michalakis 2013 ). There are a wealth of studies investigating interactions between plant microparasites (viruses, bacteria) and arthropod pest/parasite species (often plant ectoparasites), both vector and non-vector. For instance, plant viruses often positively affect the fitness of non-vector spider mite and whitefly species sharing their host plant by increasing the number of offspring ( Belliure, Sabelis & Janssen 2010 ; Mauck, De Moraes & Mescher 2010 ; Nachappa et al . 2013 ; Ángeles-López, Rivera-Bustamante & Heil 2018 ), but see ( Gadhave et al . 2019 ). This positive effect of plant viruses is likely linked to virus-induced changes in plant physiology, which improve host quality for their vectors and in turn increase viral transmission ( Blanc & Michalakis 2016 ). These changes can also incidentally benefit non-vectors ( Nachappa et al . 2013 ; Chisholm et al . 2018 ). As in animal hosts, these interactions between parasites (including viruses, vectors and non-vectors) can be mediated via the host immune system, shared resources (which may become public goods) or feedback effects on host traits ( Graham 2008 ; Alizon, de Roode & Michalakis 2013 ). There may be antagonistic cross-talk between different immune pathways ( Thaler, Fidantsef & Bostock 2002 ), whereby viruses activate the salicylic acid (SA) immune pathway in plants which downregulates the jasmonic acid (JA) pathway and prevents an effective immune response against arthropod parasites ( Zarate, Kempema & Walling 2007 ; Zhang et al . 2012 ). Viruses can also increase the level of free amino acids circulating in their host plants, which may be a beneficial resource for other co-infecting parasites ( Nachappa et al . 2013 ; Ángeles-López et al . 2017 ). In the same way, these non-vector parasites may impact fitness of the vectored parasite directly and/or indirectly via interactions with the vector or host. A tomato spotted wilt virus (TSWV; Orthotospovirus tomatomaculae, genus Orthotospovirus , family Tospoviridae ) vector, the western flower thrips Frankliniella occidentalis , has higher fitness in coinfection with the non-vector Tetranychus urticae because it preys upon the latter ( Agrawal, Kobayashi & Thaler 1999 ). Conversely, competition with a non-vector (cotton bollworms) negatively affects vector (whitefly) fitness ( Zhao et al . 2019 ), and pre-infestation of tobacco plants with cotton bollworms can cause avoidance behavior in whiteflies, and thus negatively affect the subsequent transmission of tomato yellow leaf curl virus ( Begomovirus coheni ) ( Li et al . 2017 ). Other studies have also shown that non-vector arthropods can impact viral titer ( Ángeles-López, Rivera-Bustamante & Heil 2018 ; Chisholm et al . 2018 ). We studied reciprocal interactions between TSWV and T. urticae during coinfection on tomato plants ( Solanum lycopersicum , family Solanaceae ). TSWV has been shown to facilitate T. urticae , increasing fecundity and the number of offspring becoming adult ( Belliure, Sabelis & Janssen 2010 ; Nachappa et al . 2013 ; Gupta et al . 2025 ). However, it is not clear whether T. urticae can impact TSWV population growth. One study found no effect of T. urticae on TSWV titre when measured at a single time point ( Nachappa et al . 2013 ). Here, we investigated the effects of T. urticae infection on the viral titre of two different TSWV isolates at two time points using quantitative DAS-ELISA. We also compared the effect of single infections (with TSWV or T. urticae ) and coinfection on plant traits (height, fresh weight, flower number and chlorophyll content). We do not find any effect of T. urticae infection on the titre of either TSWV isolate. We replicate findings showing that TSWV has a positive effect on T. urticae , with more offspring becoming adults per cm of plant height. We found that coinfection reduced plant height for the less virulent viral isolate only. Material and Methods Biological System Tomato spotted wilt virus TSWV is a tripartite plant RNA virus with two ambisense (i.e. both positive and negative polarity) RNAs and one negative-sense RNA ( Best 1968 ; Van den Hurk, Tas & Peters 1977 ) strand. It can infect > 1000 species of plants and is vectored by at least nine species of thrips (order Thysanoptera) ( Riley et al . 2011 ). TSWV can infect the whole plant including roots, leaves, petals and stems ( Tiberini et al . 2025 ) and probably fruits as well. Symptoms of TSWV include chlorotic spots or lesions on their host plants as well as systemic necrosis and stunted growth, and may ultimately lead to plant death ( Mandal et al . 2006 ; Pappu, Jones & Jain 2009 ; Tiberini et al . 2025 ). In our laboratory, we mechanically inoculated plants using leaf extracts from TSWV-infected plants. Briefly, to do this, 1 g of infected leaves was crushed with 4 mL of phosphate buffer (Na 2 HPO 4 .12H 2 O 0.03 M plus 0.2% w/v sodium diethyldithiocarbamate – DIECA) and 90 mg of active charcoal with a pestle and mortar, before adding 75 mg of silicon carbide (Carborundum), which is an abrasive powder. The inoculum was rubbed gently with a finger onto the surface of the first fully expanded tomato plant leaf before being rinsed 15-20 minutes later. Plants were checked for infection using TSWV ImmunoStrips (Agdia, France). Virus-free plants in the experiment were exposed to a simulated infection in which virus-free leaves were crushed with the same buffer, mixed with active charcoal and Carborundum and applied to the first fully expanded leaf in the same way as for virus inoculations. This was done to control for any effect of plant wounding during inoculation, which may impact spider mite or plant traits independently of TSWV infection. For experiments, two virus isolates from the collection at the XXXXX were used (France81 and LYE1137vir). Isolate France81 was collected from a pepper plant ( Capsicum annuum ) in Bouches-du-Rhône (France) in 2008 ( Tentchev et al . 2011 ). LYE1137vir was initially collected from a tomato plant ( S. lycopersicum ) in Drôme (France) in 1996 and subsequently inoculated once onto a pepper ( Capsicum chinense ) accession carrying the Tsw resistance gene. No additional passages were performed for either viral isolate, with the isolates being stored as leaf pieces in liquid nitrogen before being transferred to the XXXX in October 2022, following re-inoculation onto tomato plants (cultivar Monalbo) from frozen. At the XXXX, they were maintained by serial transfer every ∼14 days onto 3-week-old tomato plants (cultivar Moneymaker) in the lab for 5 successive infection cycles before use in this experiment. The spider mites Tetranychus urticae is a generalist spider mite species feeding on >1000 species of plants, many of agricultural importance ( Helle & Sabelis 1985 ). They are haplo-diploid herbivores and complete their life cycle in 13-14 days under our laboratory conditions. Females lay eggs that hatch into juveniles ∼4 days later. The juvenile period includes one nymph stage and two deutonymph stages. The T. urticae used in this experiment were from an outbred population created by crossing males and females from three different populations collected in Portugal (see ( Godinho et al . 2020 ) for more details). Samples of this population were transferred to XXX in December 2021 with additional mites transferred and added to the population in November 2022. They were then maintained on three tomato plants (cultivar Moneymaker) in big plastic boxes (dimensions-520 mm x 300 mm x 250 mm) with one plant being changed weekly. Populations were maintained at 25 ± 2°C on a 16: 8 light: dark cycle. To obtain equally aged females for the experiment, 13 groups of 50 mated females were placed together on a cut tomato leaf placed in a jar of water 14 days prior to the experiment to lay eggs. The experiment used the Moneymaker F 1 hybrid tomato cultivar grown in an isolated arthropod-free environment at 25 ± 3°C. The main experiment: Interactions between T. urticae and tomato spotted wilt virus in coinfection on tomato plants This experiment measured how coinfection affected tomato plant life-history traits as well as traits of both TSWV and T. urticae . There were a total of two spider mite treatments (presence/absence) combined with three virus treatments (isolate France81/ isolate LYE1137vir/no virus). Seventy-two plants were inoculated with each of the two virus isolates three weeks after sowing and 24 control plants were mock-inoculated (i.e. simulating infection) with a sap extract from healthy tomato leaves as described above. A higher number of plants were inoculated with TSWV as viral titre was measured at multiple time points (6, 13, 21 and 27 days post inoculation (dpi)) and required the culling of plants. Fourteen dpi, we transferred 20 adult T. urticae females onto 24 plants infected with each of the two virus isolates and onto 8 control, mock-inoculated plants. The T. urticae females were placed in two groups of 10 on a single leaflet of two different leaves (above the inoculated leaf). The mites were isolated on their respective leaflets using a muslin leaf cage (dimensions: 70mm x 90 mm x 10 mm) as in XXXX and plants were placed in large plastic boxes (500 x 340 x 400 mm). The plants from different treatments were randomised across boxes following the transfer of mites. We counted the number of male and female adult T. urticae using a binocular microscope on the 28th day following viral inoculation. Note that for plants that were coinfected with TSWV, some leaves were removed on day 27 to measure viral titre. Eggs and other developmental stages prior to counting adults were not measured as it was not possible to remove and replace the muslin bags without disrupting the mites. Measuring virus titre using Quantitative DAS-ELISA (Double Antibody Sandwich – Enzyme-Linked Immunosorbent Assay) Quantitative DAS-ELISA (qELISA) was used to compare the within-plant titre of TSWV between tomato plants. We sampled virus-infected plants on days 6, 13, 21 and 27 by cutting and transferring 1 g of the uppermost leaves into extraction bags (Bioreba, Reinach, Switzerland) that we placed immediately in a fridge at 4°C. The following day, samples were taken to the XXXX, for qELISA. We followed the ELISA protocol in Legnani et al. (1995) ( Legnani et al . 1995 ), using TSWV-specific polyclonal antibodies prepared at the XXXX with TSWV isolate LYE51, a tomato isolate collected in 1991 in Berre (Bouches-du-Rhône, France), as an antigen. For each plant, the 1 g of apical non inoculated leaves was ground in a phosphate buffer (1:4 wt/vol). Fivefold dilutions of each plant extract in buffer were tested using DAS-ELISA (from dilution factor 0.2 to 6.4×10 -5 w/v) and absorbance values were measured at 405 nm (A 405 ). The relative virus load of each sample was estimated using curves representing the relationship between the dilution factor and A 405 , within the dilution range where the curves decreased linearly and were parallel among samples, with the help of a home-made program using R version 4.3.2. A common plant sample present on each ELISA plate as a control enabled the virus titre to be standardized across plates. Host plant traits We measured the height of plants that were collected for measuring viral titre on days 13, 20 and 28 as well as of mock-inoculated plants on these days by measuring from just above the cotyledon insertion to the highest branch division. We measured the weight, chlorophyll content, and number of flowers of plants in the different treatments that remained in the experiment on day 28. Note the weight of virus infected plants that were culled was also measured on days 13 and 20. Chlorophyll content was measured using a single-photon avalanche diode (SPAD) (Konica Minolta, France). This was done by taking three separate measures on the leaf immediately above the leaf that was inoculated with TSWV (lower leaf), and the leaf above those with T. urticae (upper leaf). Statistical analyses All analyses were done in JMP Pro 18.0.2. All models were simplified in a stepwise fashion removing non-significant terms. Virus isolate and coinfection with T. urticae were included in models as fixed factors and day of sampling as a continuous variable. Complete statistical models are shown in tables in the Supplementary materials (Tables S1 – S7). Note that Quantification of host traits We used two separate models to investigate the effect of coinfection on plant height. In the first model, we used a Generalised Linear Mixed Model (GLMM) to investigate how height changed through time in single infections for plants inoculated with the different viral isolates versus mock-inoculated plants. In the second model, we used a GLMM to test the effect of virus treatment, coinfection with T. urticae , day of sampling, and the interactions among them on days 20 and 27 post viral inoculation. As multiple measures of height were taken from mock-inoculated plants on the different time points, replicate plant nested within parasite treatments were included in these models as a random term. We used General Linear Models (GLM) with a Gaussian error structure to measure the effect of virus infection, coinfection with spider mites and their interaction on plant weight and chlorophyll content in both upper and lower leaves on day 28. We used a GLM with a Poisson distribution, corrected for overdispersion, to measure the effect of virus and coinfection with spider mites on the number of flowers on day 28. Virus titre using qELISA We used two separate GLMs with a Gaussian error structure to investigate how virus titre changed through time. In the first, we investigated how virus titre in single virus infections was affected by viral isolate and time (days 7, 13, 20 and 27), and the interaction between them, in plants without T. urticae . In the second, we investigated how coinfection with T. urticae , virus isolate and time (days 20 and 27), and the pairwise and 3-way interactions between the three variables affected virus titre. Effect of TSWV on T. urticae life-history traits We used GLMMs with a negative binomial error structure and log link function to test whether virus isolate and leaf (lower versus higher) and their interaction affected the total number of adult offspring and adult daughters. Plant replicate number was included in these models as a random factor. We tested whether offspring sex ratio (across both leaves) was affected by viral isolate using a GLM, corrected for overdispersion, with a binomial error structure and logit link function. In separate GLMs with a Gaussian error structure, we analysed the number of adult and female offspring per cm of plant height in the different virus and control treatments. Quantitative relationships between host traits, viral load and number of spider mites To visualise the covariation among all quantitative host (height, weight, number of flowers and mean chlorophyll content on higher and lower leaves) and parasite traits (number of adult females and log relative viral concentration) we used principal components analysis (PCA) on standardised data for plants infected with virus and T. urticae on days 20 and 27. Note that measures of weight, flowers, chlorophyll content and T. urticae females were only available for day 27. Finally, we used path analysis by extracting standardised beta-coefficients from regression analyses to investigate if there were any relationships between standardised log relative viral load, plant height and the number of adult daughter spider mites on day 27. Results Effect of virus and spider mite infection on host plant traits There were significant effects of virus infection (F 2, 85 = 89.11, p < 0.001), day of sampling (F 2, 102 = 105.49, p < 0.001) and their interaction (F 4, 106 = 6.47, p < 0.001) on plant height in single virus infection and mock-inoculation treatments ( Figure 1 ). Virus-infected plants were smaller than mock-inoculated plants, however the virus isolates affected plant height differently. Plants infected with France81 were significantly smaller than control plants across sampling dates, but the relative height difference of plants infected with LYE1137vir changed through time, being closer to France81-infected plants 14 dpi, but more similar to control plants 28 dpi ( Figure 1 ). Download figure Open in new tab Figure 1: Effect of tomato spotted wilt virus infection through time on mean (± standard error) height of plants a) inoculated with TSWV isolate France81, b) inoculated with TSWV isolate LYE1137vir, and c) mock inoculated, either infected (black circles) or not (open circles) with T. urticae. Small circles represent individual replicates on the different days. In the second model including coinfection with T. urticae , as before there was a significant effect of virus isolate (F 2, 109 = 108.84, p < 0.001), day of sampling (F 1, 122 = 79.56, p < 0.001) and their interaction (F 2, 126 = 5.73, p = 0.0042). Infection with T. urticae also reduced plant height (F 1, 111 = 12.10, p = 0.0007). There was no significant interaction between virus isolate and mite (virus*mite; F 2, 107 = 2.80, p = 0.0653, virus*mite*day; F 2, 122 = 0.32, p = 0.7267) indicating that the impact of T. urticae on plant height in coinfection was the same on virus and uninfected plants (see Table S1). Plant weight was significantly reduced by virus infection (ᵡ 2 2 = 95.86, p < 0.001), especially for the France81 isolate, but not by the presence of spider mites (ᵡ 2 1 = 2.47, p = 0.1160) (Figure S1a). The number of flowers was also lower on virus-infected plants (ᵡ 2 2 = 17.20, p < 0.0001), but was unaffected by spider mites (ᵡ 2 1 = 2.10, p = 0.1477) ( Figure 2 ). Mean chlorophyll content in the upper leaves was lower in plants infected by both viral isolates than mock-inoculated plants, (ᵡ 2 2 = 25.31, p < 0.001; Figure S1b), but was not influenced by T. urticae (ᵡ 2 1 = 0.004, p = 0.9493). There was no effect of virus (ᵡ 2 2 = 5.55, p = 0.0623) or T. urticae (ᵡ 2 1 = 1.65, p = 0.1988) on the mean chlorophyll content of lower leaves. There were no significant interactions between virus infection and T. urticae infection for plant weight, number of flowers, or chlorophyll content (Table S2). Download figure Open in new tab Figure 2: Effect of tomato spotted wilt virus infection on mean (± standard error) number of flowers on plants singly inoculated with isolate France81, LYE1137vir or mock-inoculated in the presence (closed circles) or absence (open circles) of T. urticae . Small circles represent individual replicates Virus titre using qELISA There was a significant effect of virus isolate (ᵡ 2 1 = 17.60, p < 0.0001) and day of sampling (ᵡ 2 3 = 112.37, p < 0.001) on virus titre in single infections ( Figure 3a and 3b ). The titre of both isolates declined through time, but the France81 isolate had a higher titre than LYE1137vir. The interaction between viral isolate and day was not significant (ᵡ 2 3 = 1.59, p = 0.6627). In the second model, that included T. urticae, the effects of virus isolate (ᵡ 2 1 = 11.82, p < 0.0001) and day (ᵡ 2 3 = 11.94, p < 0.001) remained significant. There was no effect of coinfection with T. urticae on the viral titre of either viral isolate on days 21 or 27 ( T. urticae main effect: ᵡ 2 1 = 0.26, p = 0.6105; for all interaction terms with T. urticae p > 0.1321, Figure 3a and 3b ; Table S3). Download figure Open in new tab Figure 3: Effect on mean log relative virus titre (± standard error) through time for plants singly infected with TSWV a) isolate France81 or b) isolate LYE1137vir, with (black circles) or without (open circles) the spider mite T. urticae . Small circles represent individual replicates. Effect of TSWV on T. urticae life-history traits There was no effect of virus treatment on the total number of female (F 2, 29 = 2.18, p = 0.1314; Figure 4A ) or adult offspring (F 2, 30 = 1.60, p = 0.2187) (Figure S2a) or offspring sex ratio (ᵡ 2 2 = 2.46, p = 0.2928) (Figure S2c). There were, however, a higher number of females (F 1, 31 = 11.40, p = 0.0020) and adults (F 1, 31 = 12.38, p = 0.0014) on the upper leaf. There was no significant interaction between virus isolate and leaf level for the number of female (F 2, 29 = 0.15, p = 0.8608) or adult offspring (F 2, 29 = 0.03, p = 0.9680). As viral infection significantly reduced plant height ( Figure 1 ), we analysed the impact of virus treatment on the number of offspring per cm height of their host plants. These analyses revealed a significantly higher number of daughters (ᵡ 2 2 = 17.40, p = 0.0002), and adult offspring (ᵡ 2 2 = 15.01, p = 0.0006) per cm of plant height on plants infected with the viral isolate France81 compared to plants infected with LYE1137vir and control plants ( Figures 4b and S2b, Table S4). Download figure Open in new tab Figure 4: Effect of tomato spotted wilt virus infection on mean (± standard error) a) total number of T. urticae daughters on upper (triangles) and lower (circles) leaves and b) total number of daughters per cm of host height on mock-inoculated plants and plants infected with either TSWV isolate France81 or LYE1137vir. Small circles and triangles represent individual replicates. Quantitative relationships between host traits, viral load and number of T. urticae The PCA showed that axes 1 and 2 contributed 34.52% and 21.50% respectively to the variation in the data (see Table S5 for the variation explained by the 7 principle components). Axis 1 correlated positively with host plant weight and height and negatively with log relative viral load (Table S6). Axis 2 correlated positively with the number of T. urticae females on a plant and the chlorophyll concentration of the lower leaf and negatively with the chlorophyll concentration of the upper leaf (Table S6). On day 27, we could not detect a significant quantitative relationship between viral load, plant height and the number of adult daughters using structural equation modelling (standardised beta correlation coefficients and associated p-values for; virus load – plant height: –0.015, p = 0.3741; plant height – daughters: –0.20, p = 0.4363, virus load – daughters: 0.20, p = 0.4313). Discussion Our results show that infection with TSWV and T. urticae negatively affected host tomato plants in single and coinfections. Infection with TSWV, especially isolate France81, had a more negative effect on host plants, reducing plant height, weight and number of flowers and decreasing leaf chlorophyll content in upper leaves. T. urticae reduced plant height, with a trend for a greater reduction in plants coinfected with the TSWV isolate LYE1137vir. The systemic viral loads of the more virulent TSWV isolate, France81, were higher than those of isolate LYE1137vir. Further, facilitation of T. urticae was only observed in coinfection with TSWV isolate France81 when accounting for plant size, with more adult offspring per cm of host plant. Effect of single and coinfections on plant traits Both spider mites and TSWV are parasites of agricultural importance causing large economic losses on tomato and other crop species ( Park & Lee 2005 ; Pappu, Jones & Jain 2009 ; Sevik & Arli-Sokmen 2011 ; Meck, Walgenbach & Kennedy 2012 ; Meck, Kennedy & Walgenbach 2013 ). Once transmitted to their host plant, TSWV can infect the whole plant ( Tiberini et al . 2025 ), reduce the number and size of tomato fruit ( Moriones et al . 1998 ; Sevik & Arli-Sokmen 2011 ) and cause systemic necrosis and plant death ( Mandal et al . 2006 ; Tiberini et al . 2025 ). In our experiment, we found that TSWV-infected plants were shorter, weighed less, had fewer flowers and lower chlorophyll content in upper leaves than uninfected plants, and that the France81 isolate was more virulent, affecting these traits more severely than the LYE1137vir isolate. Other studies also found variation in the degree of necrosis and stunting ( Mandal et al . 2006 ) and the lesion phenotype ( Qiu et al . 1998 ) induced by TSWV. Variation in viral traits may arise for a number of reasons. One possibility is that variation in virulence among traits was influenced by viral load. Parasite virulence can be decomposed into host harm caused due to exploitation/proliferation (actual density) and per parasite pathogenicity or malevolence (PPP; damage inflicted per individual parasite which is the slope of the relationship between density and harm) ( Raberg & Stjernman 2012 ; Wollein Waldetoft, Raberg & Lood 2020 ). Overall, we find that plants infected with the France81 isolate had higher systemic viral load, were smaller and had fewer flowers than plants infected with isolate LYE1137vir. However, we did not find that the slope of the relationship between viral load and harm (measured for height, weight and flowers) differed between the viral isolates (see Supplementary Table S7 for these additional analyses). This indicates that differences among isolates was mostly due to differences in proliferation, rather than per parasite pathogenicity. In contrast, Doumayrou ( Doumayrou et al . 2013a ) found that viral load and virulence were positively correlated within low or high viral accumulation phenotypes (but not across the whole set of phenotypes). Another recent study found that there was variation in exploitation and PPP for four different bacteria species infecting Drosophila melanogaster ( Acuna-Hidalgo et al . 2022 ). This variation in virulence may be maintained due to trade-offs with other life-history traits, as for other organisms ( Stearns 1989 ). Contrary to France81, TSWV isolate LYE1137vir is able to infect pepper plant varieties carrying the Tsw resistance gene. This enlarged host range is conferred by mutations in the TSWV gene that encodes the NSs protein, an inhibitor of general antiviral plant defenses ( Margaria et al . 2007 ). Consequently, it may be that lower viral loads and virulence of the LYE1137vir in tomato was a trade-off with its gain in capacity to infect Tsw pepper plants, due to pleiotropy or linkage between mutations in the NSs gene. Thus, a trade-off between a wider host range with virulence and viral load. Costs of generalism have been identified in other parasites between the ability to infect multiple hosts and other life-history traits such as infectivity and within-host growth ( Leggett et al . 2013 ; Kabengele et al . 2024 ). For instance, costs associated with overcoming host resistance have been observed in the bacterial blight Xanthomonas oryzae. pv. oryzae infecting rice ( Cruz et al . 2000 ) and the wheat fungus Puccinia striiformis f.sp.tritici ( Bahri et al . 2009 ), and are also associated with mechanisms enabling parasites to overcome drug resistance (e.g. in bacteria and plasmodium ( Melnyk, Wong & Kassen 2015 ; Segovia et al . 2025 )). Spider mites feed by injecting their stylet into the leaf and sucking out the cell contents ( Tomczyk & Kropczynska 1985 ) leaving chlorotic lesions on the leaf surface, which increase with T. urticae density ( Kant et al . 2004 ; Godinho et al . 2023 ). The degree of T. urticae leaf damage is negatively linked to marketability for Impatiens walleriana ( Alatawi, Margolies & Nechols 2007 ) and there were fewer tomato ( Meck, Kennedy & Walgenbach 2013 ; Liu, Legarrea & Kant 2017 ), cucumber ( Park & Lee 2005 ) and strawberry ( Nyoike & Liburd 2013 ) fruits at higher T. urticae infestations. Park & Lee ( Park & Lee 2005 ) linked this lower cucumber yield to reduced plant growth and leaf area (due to fewer leaves), but note that Liu et al (2017) ( Liu, Legarrea & Kant 2017 ) who observed fewer tomato fruits, did not find differences in total seed number or viability. We found that T. urticae reduced plant height, with a trend for a greater reduction when infected with the least virulent virus isolate, LYE1137vir, and for control (mock-inoculated) plants. Similarly, when only considering virus infected plants (Table S7), T. urticae caused a greater reduction in weight on LYE1137vir infected plants. One possibility is that France81 reduced plant size so much that it was not possible for T. urticae to have an additional effect while for LYE1137vir, its lower virulence may permit more of an additive effect of coinfection on the host. Whether coinfections induce generally more damage than single infections remains an open question. A meta-analysis of human parasites found that coinfections were more often reported to induce more damage ( Griffiths et al . 2011 ). However, general consensus is lacking across non-human hosts regarding (i) whether damage experienced by hosts in coinfections is higher or not than in single infections and (ii) whether coinfection effects are additive, or more or less than additive in terms of host damage, compared to single infections. Some studies report coinfections to be more virulent (e.g. ( Lass et al . 2013 )), others less virulent (e.g. ( Schurch & Roy 2004 )) and others report no change (e.g. ( Pollitt et al . 2015 )) on traits measured. Our study suggests that the effect of coinfections on virulence are additive, or explained by virulence of the virus. The application of general rules regarding coinfection outcomes such as higher or lower virulence relies on better understanding of the interaction mechanism ( Choisy & de Roode 2010 ; Alizon, de Roode & Michalakis 2013 ). These questions are relevant to analyse the immediate (ecological) consequences of virulence in coinfected hosts (as demonstrated in ( Graham 2008 )) as well as long-term consequences of coinfection for the evolution of parasite virulence ( Choisy & de Roode 2010 ; Alizon, de Roode & Michalakis 2013 ). Our lack of a strong effect of T. urticae and coinfection in general on tomato traits may be due to the time-scale of our experiment, with spider mites on plants for a total of 14 days. Economic loss (linked to yield and poor quality fruit) was estimated to be detectable after 4 weeks of T. urticae infestation in cucumber greenhouses ( Park & Lee 2005 ). As TSWV facilitates spider mite growth ( Belliure, Sabelis & Janssen 2010 ; Nachappa et al . 2013 ; Gupta et al . 2025 ), and higher T. urticae densities are associated with higher virulence ( Park & Lee 2005 ; Nyoike & Liburd 2013 ), it is possible that we would have observed that coinfections induced more damage if the experiment had lasted longer. Indeed, we did find that reductions in plant weight and height, were correlated ( Figure 5 ), despite only finding a significant effect of T. urticae on height. Download figure Open in new tab Figure 5: PCA for the five host traits (plant height, weight, number of flowers and mean chlorophyll content in lower and upper leaves), viral load and number of T. urticae adult females. Blue circles represent data from tomato plants infected with the France81 TSWV isolate and red circles the LYE1137vir TSWV isolate. Open and filled symbols represent the absence and presence of T. urticae , respectively. TSWV infection dynamics For both TSWV isolates, the plant systemic load was highest on day 7 before declining through time until day 27. Declines through time were also observed for cucumber mosaic virus, pepper mild mottle virus and pepper mottle virus in pepper plants ( Kim et al . 2010 ) as well as the daily rate at which new cells became infected for tobacco etch virus in tobacco ( Tromas et al . 2014 ). The observed decline in relative viral load may arise due to the plant immune system limiting TSWV growth ( Tromas et al . 2014 ). However, another study found an increase through time in the number of viral DNA segments in faba bean necrotic stunt virus ( Sicard et al . 2013 ). Coinfection with T. urticae did not change virus titre on days 21 and 27 for either of the TSWV isolates, indicating a neutral effect of spider mites on TSWV. This is consistent with previous findings for TSWV ( Nachappa et al . 2013 ), but is in contrast to other studies which found that non-vector arthropod parasites can impact plant viral titre ( Ángeles-López et al . 2017 ; Chisholm et al . 2018 ). Interactions between plant viruses and other coinfecting parasites may be mediated via different mechanisms, including negative immune cross talk between the JA and SA pathways and/or the increase of free amino acids. Note these are the mechanisms invoked for facilitation of T. urticae by TSWV ( Belliure, Sabelis & Janssen 2010 ; Nachappa et al . 2013 ). Angeles-Lopez et al (2018) attribute a negative effect of the whitefly, Trialeurodes vaporariorum, on pepper golden mosaic virus to reductions in amino acid levels in the phloem. Chisholm et al (2018) discuss how their finding of a positive effect of the weevil Sitona lineatus on pea enation mosaic virus may be via mechanisms linked to activation of the JA pathway, independent of any suppression of the SA pathway (which they did not find). It has been found that coinfection with rhizobacteria can reduce viral growth independently of effects on the SA pathway ( Ryu et al . 2004 ). In both these studies, that found an effect of non-vector arthropods on viral titre, inoculation of the plant by the virus occurred first, as in our study. This absence of a reciprocal effect between T. urticae and TSWV in our experiment may be attributed to different reasons. One possibility is that there is asymmetry in antagonistic immune cross talk ( Thaler, Fidantsef & Bostock 2002 ). This might occur if the order of infection determines activation patterns such that later-arriving parasites cannot induce a strong enough immune response to suppress already activated branches of the immune system. Plants were infected by T. urticae two weeks after inoculation with TSWV, which may have precluded any effect of spider mites on the plant immune system and the occurrence of negative immune cross-talk. If infection order had been reversed (i.e. T. urticae infection first), T. urticae -induced upregulation of the JA pathway may have prevented effective activation of the SA pathway against TSWV. Indeed, prior infection of tomato plants with T. urticae reduced T. evansi oviposition, likely due to prior induction of the JA pathway preventing its suppression by T. evansi ( Sarmento et al . 2011 ). However, there may exist an inherent asymmetry in the negative immune cross talk, such that induction of SA negatively affects JA but not always vice versa ( Thaler, Fidantsef & Bostock 2002 ). It is also possible that the spatial location of parasites in the plant affected the interaction. TSWV distribution in plants can be heterogeneous, due to the virus initially infecting the apical leaves before moving down to the lower leaves ( Mandal et al . 2007 ; Asano, Hirayama & Matsushita 2017 ; Gupta et al . 2025 ). Thus, leaves with spider mites may not have impacted leaves from which viral loads were measured. Other studies have found that interactions among plant parasites can be very local ( Spoel, Johnson & Dong 2007 ; Alba et al . 2015a ). Another possibility was that spider mite densities were too low to impact TSWV either via effects on the immune system and/or other mechanisms of interaction (e.g. free amino acids, see below). TSWV infection facilitates T. urticae We have previously shown that TSWV facilitates T. urticae on whole plants ( Gupta et al . 2025 ), but did not take into account the effects of virus infection on host traits and how this may affect T. urticae fitness. In this experiment, we found that TSWV infection reduced host height significantly, which in turn could possibly reduce the amount of plant resources available for T. urticae . Virus-infected plants (with the France81 isolate) were more than 12 cm shorter than uninfected plants when they were infected with T. urticae 14 dpi (mock plants 23.24 cm ± 0.85, France 81 infected plants 9.02 cm ± 0.85, LYE1137vir infected plants 10.79 cm ± 1.14), and ∼17 cm shorter when T. urticae became adult 27 dpi. Despite these virus-infected plants being smaller, there was no difference in the total number of T. urticae offspring becoming adult. However, when accounting for plant height, T. urticae had on average ∼3.5 more offspring per cm of plant on France81-infected plants than on LYE1137vir-infected or mock-inoculated plants (6.49 ± 0.90 SE offspring per cm of height on France81; 2.43 ± 0.55 SE offspring per cm of height on LYE1137vir; 3.08 ± 0.42 SE offspring per cm of height on mock). Plant height is a good proxy for the amount of plant material available, since it is strongly correlated with plant weight ( Figure 5 ). Thus, T. urticae produces more offspring per cm of host size when infected with TSWV viral isolate France81. Despite plants infected with France81 having higher viral titres, we did not find a relationship between TSWV titre and the number of T. urticae female adult offspring on day 28. This might be because viral titre on day 28 was too low giving us little power to detect a relationship. Although facilitation by France81 could be attributed to another viral trait, it is possible that more T. urticae offspring is linked to higher viral loads. As discussed above, facilitation of T. urticae by TSWV is thought to occur via antagonistic negative immune cross talk and/or higher nutritional availability in virus-infected plants in the form of elevated free amino acids ( Nachappa et al . 2013 ; Ángeles-López et al . 2017 ). The contribution of both these mechanisms to increases in spider mite offspring numbers may be related to viral titre in a dose-dependent manner. Previous work has shown that higher levels of SA induction impose greater suppression of the JA pathway ( Thaler, Fidantsef & Bostock 2002 ). If higher viral titre is associated with higher levels of SA induction, this could increase levels of facilitation via higher suppression of JA. Previous work has shown quantitative relationships between spider mites and different branches of the plant immune system. Alba et al., 2015 found that a higher T. evansi density suppressed the JA pathway more strongly and Ataide et al., 2016 showed that oviposition of T. evansi and T. urticae initially declined with increasing (artificially applied) levels of JA ( Alba et al . 2015b ; Ataide et al . 2016 ). Another study found that higher doses of Trypanosoma cruzi induced higher pro-inflammatory responses in mice ( Borges et al . 2013 ). Proxies to measure parasite virulence and transmission The use of proxies to measure virulence and parasite fitness is common, often for practical reasons. However, it is important to know how these proxies link to actual host and parasite fitness to better understand the ecological and evolutionary consequences for these traits ( Alizon & Michalakis 2015 ). This has been done for some parasites in plant and animal hosts (e.g. ( de Roode, Yates & Altizer 2008 ; Doumayrou et al . 2013a ; Godinho et al . 2023 ). Proxies for virulence in plants include plant height, weight, leaf surface area and leaf damage ( Doumayrou et al . 2013b ). A study by Doumayrou (2013) did find that reductions in plant leaf surface caused by cauliflower mosaic virus in two different plant species were correlated with host mortality ( Doumayrou et al . 2013b ). It is not completely clear in our system how measures of virulence, including tomato plant height and weight, link to host and parasite fitness ( Alizon & Michalakis 2015 ). In contrast, parasite induced changes in the number of flowers and chlorophyll content may have clearer consequences, especially for host fitness. There were fewer flowers on plants infected with the most virulent virus isolate, France81, which will have negative consequences for plant reproduction. This may be due to the host response diverting energy from reproduction to survival or not having enough energy to invest in reproduction ( Hurd 2001 ). Some parasites castrate their host to divert host resources to their own growth ( Lafferty & Kuris 2009 ). Although some plant viruses can castrate their host ( Vijayan et al . 2017 ), we do not think this is the case here as plants infected with the France81 virus isolate, with higher viral loads, were smaller; parasite-induced host castration can be associated with gigantism ( Cressler et al . 2014 ). It is less clear from our experiment if and how virulence links to viral and T. urticae fitness. In a previous study, we demonstrated that the number of T. urticae adult daughters can correlate positively with transmission, but that higher virulence (leaf damage) increases within host competition which, in turn, can also reduce the number of daughters if transmission opportunities are limited ( Godinho et al . 2023 ). Thus, if within-host T. urticae competition were higher under coinfection on smaller plants this could reduce transmission. The quantitative DAS-ELISA used to estimate systemic viral load is based on polyclonal antibodies that bind multiple virion epitopes, mostly of the nucleocapsid protein and the glycoproteins of the virus envelope and is therefore representative of the total virion load in the sampled leaf tissues. A positive correlation was found between TSWV titre in leaf tissue and transmission to the thrips vector ( Okazaki et al . 2010 ) (but see ( Pereira et al . 1989 ) in another system). This means that higher viral load may be associated directly with increased transmission, but it remains to be shown whether feedbacks due to increased virulence (if smaller plants means higher mortality) may in turn reduce transmission. Further, if reduced height is associated with higher mortality, there may also be an indirect effect of coinfection on viral transmission. If smaller plants die sooner, this may reduce the time window available for their transmission for both the spider mites and virus in coinfection ( Anderson & May 1982 ; Alizon et al . 2009 ). Summary Our results show the importance of measuring the life-history traits of all players, both parasites and the host, when investigating the effects of coinfection on parasite fitness. Our measurements for both TSWV viral titre and the number of T. urticae are not different in single or coinfection. It is only when we consider the differential effects of coinfection on host traits that consequences for parasite fitness are revealed. Notably, the most virulent TSWV isolate, France81, enables T. urticae to produce equivalent numbers of offspring on much smaller plants. Although we find no effect of T. urticae on viral load for either TSWV isolate, we postulate that negative effects of coinfection on plant traits may feedback to negatively impact virus fitness. This study highlights the importance of measuring the traits of all interacting species to garner a complete picture of how coinfection impacts both hosts and parasites. Statement of conflict The authors declare no conflict of interest. Funding This work was funded by an ANR grant (EVOLVIR: ANR-20-CE35-0013) to A.B.D and B.M. Acknowledgements We would like to thank Sophie Armitage for the suggestion of decomposing virulence into PPP and exploitation. We most sincerely thank Dr. Yannis Michalakis for the insightful discussions about the results, and the project. We would like to thank Sarah Grosjean, and Marie Challe for their help in maintaining the spider mite populations. Funder Information Declared Agence Nationale de la Recherche, https://ror.org/00rbzpz17 , ANR-20-CE35-0013 Reference list 1. ↵ Acuna-Hidalgo , B.A. , Silva , L.M. , Franz , M. , Regoes , R.R. & Armitage , S.A.O . ( 2022 ) Decomposing virulence to understand bacterial clearance in persistent infections . 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