Accepted Article Running title: Germany Freising, 85354 1, Liesel-Beckmann-Straße Weihenstephan, Sciences Life of School Germany Freising, 85354 2, Strasse Liesel-Beckmann Weihenstephan, Sciences Life of School Germany Neuherberg, 85764 1, Landstr. Ingolstädter (EUS), Simulation Environmental Germany Freising, 85354 2, Hans-Carl-von-Carlowitz-Platz Weihenstephan, Sciences Life of School Management, Ecosystem This by is protectedarticle reserved. Allrights copyright. doi: 10.1111/1365-2656.12995 lead to differences between this version and the throughbeen the copyediting, pagination typesetting, which process, may and proofreading hasThis article been accepted publicationfor andundergone peerfull but review not has Tel: 8161 71 +49 Email:4148 [email protected] Weihenstephan, Hans-Carl-von-Carlowitz-Platz 2, Freising,85354 Germany. Sciences Life of School Management, Ecosystem and Ecology of Department Group, Research Corresponding Author: 4 3 2 1 Sharon E. Zytynska herbivore an aphid mutualistic and variation chemical plant of Effect Ecology Community ToC category: Daniel Stouffer Handling Editor: Article :Research type Article MR MATTHIAS (OrcidSENFT : 0000-0003-3478-4774) ID DR ELIZABETH SHARON ZYTYNSKA (Orcid 0000-0002-0174-3303)ID : Schnitzler Technical University of Munich, Animal Breeding Research Group, Department of Animal Sciences, Sciences, Animal of Department Group, Research Breeding Animal Munich, of University Technical Sciences, Plant of Department Group, Research Genetics Population Munich, of University Technical Unit Research Pathology, Plant ofBiochemical Institute GmbH, München Zentrum Helmholtz and ofEcology Department Group, Research Ecology Terrestrial Munich, of University Technical 2 , Saurabh Dilip Pophaly Plantchemodiversity and aphid genetics 1 , Yasemin Guenay , Yasemin Journal of Animal Ecology Sharon E Zytynska, Technical University of Munich, Terrestrial Ecology Ecology Terrestrial Munich, of University Technical Zytynska, E Sharon 3 , ChristineWurmser 1 , Sarah Sturm

ants on the local population genetic structure of of structure genetic local population on the ants 1 Version of Record. Please Version as this cite ofRecord. article , Mary V. Clancy V. Mary , 4 and Wolfgang W.Weisser 2 , Matthias Senft, Matthias 1

1 , Jörg-Peter , Jörg-Peter Accepted Article (VOCs) for host-plant recognition (Bruce, WoodcockWadhams & 2005;Beyaert & HilkerThus, 2014). compounds organic volatile species-specific than rather recognition chemical ratio-odour use insects (Iason, &Hartley Dicke 2012; &HilkerBeyaert 2014; Kessler 2015). Current evidence suggests that communities associated of structure the on effects strong have to shown been have environments yet constitutive (non-induced, present) always compoundscanmore be that across stable variable 2003), Hilker & (Dicke feeding herbivore to due plants in induced compounds of role the on focused is work Much 2009). Loon van & Dam van (Hopkins, in Brassicaceae glucosinolates e.g. interactions, plant-insect multitrophic on effects strong have to known well are compounds certain 2001); (Fiehn population single a in species a within individuals among even diverse, chemically highly interest, e.g. plant architecture or nutrient value (reviewed in Whitham of trait genetically-based a in vary that plants comparing by or markers, molecular of use via the different genetically as aredefined that individuals of sets comparing by studied is this Often, 2016). Whitham 2011; Preziosi & Shuker Rowntree, in (reviewed and microbes as communities on variation genetic plant of effects the for particular in genetics, community of area the in studied well been has structure community 2010; Rowntree, Shuker Preziosi & ecologThe 2011). effects indirect metabolomics, variation, Keywords of interactions with other species in a community context (Tétard-Jones context community a in species other with of interactions Individuals within aspecies can differ from one another, and leads this tovariationoutcome in the Introduction This by is protectedarticle reserved. Allrights copyright. Abstract 5. 4. 3. 2. 1.

can be enhanced through indirect interactions with a third species. species. third a with interactions indirect through enhanced can be not only at species the level but also genetic at the level within species, and that effect this intraspecific plant that emphasize Our results ( tansy plant host oftheir (metabotypes) metabolites non-volatile and (chemotypes) genotypes across host-plant individuals associatedis withvariation in plantthe volatiles local( of the aphid We presentevidence that distribution host preferences of aphid-mutualist ants. ants. aphid-mutualist of preferences host genotypes, their antmutualists, and other predatorswas assessed across the plants. aphid of distribution The diversity. chemical high exhibit that plants host distributed patchily- ~200 containing site field a from years two across collected aphids genotyped We species variation, with genotypessome better adapted tosomeplant variants others. than variable herbivore growth across rates host different plants. Herbivores also within-exhibit Plant variationcan affectherbivores directly and indirectlyvia athird species, resulting in Plants exhibit impressive genetic and chemical chemical and genetic impressive exhibit Plants non-random distribution of individuals across host-plants. host-plants. across individuals of distribution non-random create a spatially-heterogeneous habitat for specialized herbivores potentially leading to communitieswell is known. Whenvariation there is at the local populationthis level, can within species, and the importanceof plant intraspecific variation for structuring ecological Tanacetum vulgare

: ant, aphid, chemical ecology, population genetics, species interactions,within-species ). Furthermore, these interactions in the field were influenced by plant- by werein influenced field ). Furthermore, the interactions these diverse asinvertebrate ical importance of intraspecific variation for for variation intraspecific of importance ical variation can structure ecological communities communities ecological can structure variation diversity, not just between species but also also but species between just not diversity, Metopeurum fuscoviride Metopeurum et al. et et al. et etal. s, vertebrates, plants, plants, s, vertebrates, 2012). Plants arealso 2012; Crutsinger 2007;Zytynska ) etal.

Accepted Article This by is protectedarticle reserved. Allrights copyright. 1984; Caillaud (Service host-preference and performance aphid influence these among interactions chemotype) or genotype-by- (genotype-by-genotype, plant-aphid that shown consistently have chemotypes) genoty aphid different using experiments Controlled camphor &Müller(Kleine levels 2011). of levels higher containing ( plants goldenrod on found were aphids More numbers. aphid on compounds field has been studied ina few systems, predominantly assessing the impact of dominantchemical Tosh &Hardie 2006; Döring 2014). The effect of plant chemical variation on aphid populations in the (Powell, plants by emitted chemicals various from cues including cues, of combination a on based is decision its host, anew choosing is aphid an When activity). risk high (a host-plants between walking only produce winged dispersal morphs forweeks afewyear per after which dispersal is limited to often and growth), colony clonal (fast months summer the during asexually reproduce they addition, changes host-plant in quality, and interactwith multiple other species in environment. the In Aphidson feed phloem the sapof arestricted number of planthosts, arehighly responsive to communities. plant-associated in variation plant of role the study to ideal are systems Aphid-based nature. in see we that all members of aninteractingcommunity, that leads structuringthe to of ecologicalcommunities by experienced interactions, indirect and direct these of sum overall the is It plants. host individual colonising populations herbivore of dynamics the influence can interactions different these All 1999). Tumlinson & (Paré feeding herbivore to response in released immediately and synthesised occur throughconstitutive emission of compounds plant the in (Senft & Agrawal The emission 2017). VOCs can attract enemies of plant –whichcan natural to plants (Züst antagonistic to mutualistic from ants and aphids between relationship the changed cases some de toxic a of levels high with plants on by ants or antagonistic natural enemies (reviewed inZytyns preferences, and indirectly affect aphid survivalvia altering interactions with their mutualistic ants or host-plant (performance) rate growth population their influence can directly variation plant species inmultitrophic systems. example, For for aphid herbivores that feed on plant phloem sap, on influences indirect and direct have can chemical) or (genetic variation within-species Plant traits). associated (or compounds of mixture complex whole the rather but trait) based genetically- (or chemical single a of abundance the as just be considered not should variation plant drive speciation events. potentially and herbivores, and their variants plant between coevolution to lead can associations the evolutionary speciestrajectoryof a (Stireman, NasonHeard In & 2005). extreme cases, such or lead genotypes, of distribution a of evolution for material raw the is variation Genetic genotype). (aphid aphid the in variation and chemotype) (plant plant the in variation to due differ could plants host across of aphids distribution the that suggest interactions Such 2014). with higher linalool levels (Linhart etal. 1995; Zytynska 1995; Preziosi & 2011; Kanvil,Powell &Turnbull 2014; Zytynska β -pinene (Williams Avakian2015), & thyme( plants to reduced mixing of genotypes within a population, can influence can influence population, a within genotypes of mixing reduced to et al. et and2005), tansy plants ( fensive chemical led to reduced aphid numbers, and in in and numbers, aphid reduced to led chemical fensive species and therefore interactions that the interactionsthat alter speciestherefore and ka &Weisser2016). Reduced visitation of aphids pes and plant variants variants plant and pes Tanacetum vulgare L vulgare Tanacetum et al. et 2019) or via compounds compounds via or 2019) (genotypes, varieties, Thymus vulgaris L. vulgaris Thymus Solidago altissima L. altissima Solidago .) with lower lower with .) et al. et )

) Accepted Article 11°46'1.19"), individually 200 around contains and E 48°25'1.51"; N (Altenhausen: Germany Freising, near located is used we site field The 2017). ge and wasps parasitoid including enemies natural the black garden ant, ant, garden the black aphid specialized of genetically identicalour field shoots18±8.7 (inwere there shoots The plant (mean±SE)). per patches in grow plants Tansy sites. less-managed and well-drained on growing site), single a within plants 100 (over common locally but rare regionally is and Eurasia, to native is that plant herbaceous site. field and system Study Methods and Material 2017). Zytynska & Weisser (Senft, individuals plant different across we observed ants of abundances chemotyp plant by genotype aphid any if determine popula aphid the of structuring fine-scale to lead 2016; Clancy volatilechemical compounds in the plants on aphid-ant interactions in this system (Clancy non- and volatile both of effects strong the on Based population. a within plants neighbouring across i.e. scale, small very a at plants, host across genotypes aphid of distribution the influence Here we explore how plant chemical variation, both in volatile and non-volatile metabolites, can system. this in specialists aphid the on effects indirect and direct strong have can variation (Senft experiment manipulation controlled growth and survival, mediated via interactionswith 2000; Senft, Weisser &Zytynska 2017). The role of plant volatilechemotypes onaphid population of growth population the benefited and success colonisation This by is protectedarticle reserved. Allrights copyright. (Clancy variation chemical plant to responded (Clancy diversity chemical of aspects two these of effects disentangle can we where system unique a to leading metabotype, chemicals. Interestingly, was nothere association between plantvolatile chemotype and constitutive plant in differences from resulted rather but feeding, aphid by induced chemicals preferred’ volatilechemotypes) (Clancy by a colonised were profiles) metabolomic similar metabolomic profiling of the leaves–that all plantscertain of metabotypes (clusters of plants with (Clancy season aphids byspecialized plants on the structures storage fromspecialized emitted putatively- being as identified (terpenes), VOCs of profile the in variation plant-to-plant that shown invertebrate Balint community 2011; Müller & (Kleine structure a single population (Clancy within even compounds chemical non-volatile and volatile their in variation high exhibit plants These chemical variability in terpenoids, whichgenetic has a basis (Keskitalo, LindenValkonen & 1998). by larger the interacting community. Tansy plants ( mediated be could associations these how asked and plants host different across genotypes of aphid distribution on the site field natural a in variation chemical plant tansy of effect the investigated We etal. et al. et Metopeurum fuscoviride Metopeurum 2018;Senft 2016). In addition to variation in the VOCs, we showed–through untargeted untargeted showed–through we VOCs, the in variation to addition In 2016). Lasius niger et al. et al.

( Tansy ( Tansy Metopeurum fuscoviride Metopeurum etal. 2018). The two common twoThe mutualistic alsothis 2018). species system ant in 2016; Clancy L.,common or the red ant Tanacetum vulgare 2019), we asked whether plant chemical variation could also could also variation chemical plant whether we asked 2019), et al. is obligatorily is ant-tended &Weisser2000), (Flatt often by etal. 2018). Importantly, 2018). theseeffectswere not a result of et al. et etal. 2019).work This indicates that plant chemical tion at thetion genetic at level. wantedWe further to phids at the peak of the season (even on ‘less ‘less on (even season of the peak the at phids neralist predators (Senft, Weisser&Zytynska Tanacetum vulgare Tanacetum identifiable tansy plants (Fig. S1) of which 172 of S1) (Fig. plants tansy identifiable leaves, affected thefiel leaves, affected 2018), and this can influence the associated associated the influence can andthis 2018), ants and predators, was recently confirmed in a a in confirmed recently was andpredators, ants 2016), and the presence of ants increased 2016), of presence ants the and e associations were influenced by the varying varying the by influenced were associations e Stroyan (Aphididae)) in the early part of the the of part early the in (Aphididae)) Stroyan L.) is a chemically diverse, perennial perennial diverse, chemically a is L.) Myrmica rubra Myrmica M. fuscoviride et al. et 2016). Recently, 2016). we have L.) are characterised by high byhigh characterised are L.) d colonization of tansy of tansy colonization d aphids (Flatt & Weisser Weisser & (Flatt aphids L., and has a myriad of of myriad a has and L., et al. et

Accepted Article autocorrelation. spatial of effects confounding infer would detected if which field, the in profiles metabolomic and volatile plant of clustering ofgeographic extent the determine to used were tests Mantel compounds. variable more or abundant the resulting PEP determine tovalues clusteringif our analysis was biased towards the either more on samples plant the across deviation) (standard variation and concentration compound of effect re was variable each which in models of proportion explanatory variable andcalculates posterior a effectprobability (PEP),which isequivalent to the mult runs BMA Essentially, individuals). plant (87 (Clancy analysis metabolome (Raftery ‘BMA’ package R the in implemented as (BMA) Averaging Model Bayesian we used clustering, chemotype plant the on compounds volatile individual 22 the of influence relative the To test another. one from different significantly were groupings the that show to used was Conservation) Pisces Package, inv3.3.0 R in RStudiov0.99.896. ANOSIM (Analysis Similarity,of using the Community Analysis chemotype and metabotype plant groupings, using package the ‘pvclust’ (Suzuki& Shimodaira 2015) so aphids, by colonized were that collected from every plant that hosted aphids (up to five colonies per plant) once in 2014 (15 2014 in once perplant) colonies five to (up aphids hosted that plant every from collected was months) summer the during asexually reproduce aphids as clone, same the therefore and aphid mother same the from produced likely aphids, of group close (a colony per aphid One mummies). antpreference), (for arrival weeks aphid before LC-MS by (Clancy by LC-MS This by is protectedarticle reserved. Allrights copyright. ( on presence ant thissurvey data from used we analysis, For thecurrent October)2017). ZytynskaWeisser & growing fieldthroughout (Senft, 2014 site to season (May the collection. sample aphid and data survey Field Zytynska 2017). & Weisser (Senft, aphids of distribution aheterogeneous to leading seasons both across by aphids were visited each week 2014 and in four times in 2015; importantly, of only them werecolonized87 (Clancy compounds, emittedspecialised from storage struct Plant chemical andclustering analysis. 1996). Hales & (Sunnucks procedure salting-out the using extracted was DNA Aphid DNA extraction. °Cuntil -20 at ethanol 100% in stored were aphids All July. early in once 2015 (11 in season the across times four aphids collected and plants the revisited we 2015, In years. across Due naturethe to plant, the it of as regrowsin same the location year,each plants could be followed et al. et al. et th June, 9 June, 2016)), and secondary metabolite information mass of 1020 features as identified using 2015). 2015). This analysiswas not possible for the 1020 mass features from the untargeted et al. et th July, 23 July, 2018) (for 2018) details more seeAppendix 1).Our focuswas onlyon those plants rd July, and 6 and July, et al. et we performed new cluster analyses on these 87 plants to obtain obtain to plants 87 these on analyses cluster new performed we 2018) due to model saturation from limited degrees of freedom offreedom degrees limited from saturation model due to 2018) th We used plant the volatilechemical information on 22 August); plant size and aphid number data were collected collected were data number aphid and size plant August); We conducted an intensive weekly survey in this this in survey weekly intensive an conducted We and specialist natural enemy abundance (parasitoid (parasitoid abundance enemy natural specialist and iple linear models with each compound as an an as compound each with models linear iple tained (seeAppendix 2for details). Wetested the ures on the plant (identified using GC-MS, from from GC-MS, using (identified plant onthe ures L. niger L. and and M. rubra th ) in the July). July). Accepted Article simulated P-values,with 1.0x 10 analysed were ‘metabotype’, or chemotype’, ‘plant and genotype’ ‘aphid between associations Non-random groups. metabotype or classes chemotype individuals across all sampling collectedtimes) on all plants within each of the different plant wi aphids number of the of table a contingency Analysisof the association between aphid genotypes and plant chemo(metabo)types. clusters. genetic mean) clustering using Nei’s (1972) original distancewas used toshow relationship the among aphid year separately, to allow comparisons. UPGMA (Unweighted Pair Group Methodwith Arithmetic each andfor years across data pooled the on both analysis ranthe We chosen. was number group K=n+1 was closezero to (i.e. no further information obtained by splittingintomore groups), this ofnumbers Criterion) wascalculated fordifferent ge fine-scale for looking were we Since ‘poppr’. package the in clustering hierarchical K-means used we clusters, genotype into aphids the cluster To genotypes (MLGs), were obtained using the package ‘poppr’ R(Kamvar, in Brooks Grünwald& 2015). analysis. data genetic Aphid 1.75) (SoftgeneticsCollege, LLC, PA,State USA). (version GeneMarker software the using analyzed was data Fragment min. 2 for °C 72 at step final run at for 95°C 2 mins, 30cyclesof for 95°C °C 15 sec, for 60 15sec, for 15secs,72 °C and thena 20 to up mix, primer specific MyTaq™, Units 2 UK), (Bioline, Buffer Germany). The final multiplex PCR conditions were: 1 an ABI3130xlGenetic Analyzer (Applied BiosystemsLife - TechnologiesGmbH, Darmstadt, an HEX, 6-FAM, dyes: fluorescent three each, using mu two to leading PCR-multiplex a develop to chosen instructions (Illumina Inc., Diego, San USA). Microsatellites were identified and 18primer were pairs manufacturer’s the to according 100bp of length aread with cell flow paired-end a on conducted was 2500 HiSeq™ Illumina the using sequencing generation Next adapters. Illumina for Oligos Illumina® (New England BioLabsGmbH, FrankfurtMain, amGermany), with Multiplex NEBNext for Kit Prep Library DNA Ultra™ NEBNext® the using prepared was library the Briefly, 3). Appendix metabolomics data. metabolomics to statistical limitationswere not we able perform analysisthis on the1020mass features from the Due results. analysis contingency the to compared and cluster, genotype aphid or class chemotype plant the and compound the between associations any determine to models linear posthoc we ran models, the of >5% in retained compounds all For clustering. genotype aphid the in variation explained compounds volatile 22 the of which identify to method BMA the used we structuring, To identify individual chemicals within of chemotypesinterest the associated with aphid genetic This by is protectedarticle reserved. Allrights copyright. for primers development. microsatellite and sequencing genome Aphid deemed significant when above the critical value for 1df at 1df value critical for deemed significant whenthe above combinations individual with analysis, Chi-square post-hoc using assessed were contributions M. fuscoviride M.

, we genome-sequenced one field-collected aphid (for full details see see details full (for aphid field-collected one genome-sequenced we , Basic descriptive molecular statistics, such the as number multi-locusof 7 replicates, as the frequency table was larger than 2 by 2. Individual Individual 2. by 2 than larger was table frequency the as replicates, thin each genetic cluster (pooled number of of number (pooled cluster genetic each thin netic structuring, the BIC (Bayesian Information Information BIC (Bayesian the structuring, netic groups (K). When the difference between K=n and and K=n between difference the When (K). groups d TAMRA, alongside the ROX size standard run on run standard TAMRA, size d theROX alongside using a Fisher’s Exact test using Monte Carlo Carlo Monte using test Exact Fisher’s a using ltiplex combinations with nine primer pairs in μ l DNA l diluted 1:4,x MyTaq™ 5 Reaction α =0.05, i.e. 3.84. In order to develop new microsatellite microsatellite new develop to order In μ l with molecular grade water, We created Accepted Article bias in the chemotype clustering analysis due to highly abundant compounds (F compounds abundant highly dueto analysis clustering chemotype the in bias plants were not similar more to each other (Mantel test, P=0.112;r=0.050, Fig. S2a). wasThere no was sp i.e. no there distance, chemical based on which plants the belong. Overall, plantswith chemotype similar profiles were notspatiallyclustered main class (from Clancy class (from main analysing all 172 plants, and so arelabelled 1.1, 1.2,1.3, 2.1, 2.2, 2.3, 3.1, 4.1and 4.2to show the chemotypeclasses (ANOSIM: r=0.812, These P<0.001). still main fit classesthe obtained from al. plants (aphid colonized and empty plants) into four main volatilechemotype classes (1-4)(Clancy plants in fieldthe site (61/172 inand 2014 50/172 2015). Inin previous work, weclustered 172 all Plant chemo/metabotypes. Results colonisation. aphid colo aphids before plants different onthe present on GLM binomial a using preference ant we analysed pres ant of To effect explain any data. the represents best is that chosen are associationsconsidering by 2-factor all interactions (Everitt1992).From this,the optimal model chemotype, aphid plant presence, ant factor (e.g. are These interactions. potential all for accounting interest, of model possible each for calculated are deviances presence/absence), ant –by chemotype plant by – genotype aphid (i.e. tables contingency 3-way such For metabotype). (or chemotype plant and genotype, aphid presence, parasitoid) (or of ant effect the analyse to used were errordistribution poisson with (glm) models linear generalised and frame, data a to of the plantsr=0.034, [Mantel test: P=0.004; (Clancy profile metabolome and volatile the between association (no metabotype and chemotype for plant and second for those plants without without plants those for and second with plants for created was table contingency one dataset, This by is protectedarticle reserved. Allrights copyright. the for example, For metabotype). (or chemotype plant each on genotype each aphid within of aphids number the counted that set data each for tables contingency separate created Followingmethods for analysingcontingency tables using log-linear 1992),models we (Everitt first plant. a on aphids parasitized of presence the used we analysis wasp parasitoid the For colonisation. beca preference ant of measure a as colonization parasitoid wasps.the Weused interactions, we used onlythe 2014data that included informationon interacting ants and chemotype –plant genotype aphid on the species interacting of effects potential To explore species. interacting by mediated associations chemotype –plant genotype Aphid plants. the in compounds of profile whole the highly variable compounds (F compounds variable highly 2016). 87plantsThe 2016). that hosted aphids exhibited finer-scale clustering, with nine distinct final et al. et Across theyears two of data collection, aphids colonized 172 of 87 the followed2016), sub-class bythe (identified in the current analyses) to 1,20 presence presence ( antspecies each of =0.09, P=0.772) in the plants (Fig. S3a). Thus, clustering was due to due to was clustering Thus, S3a). (Fig. plants the in P=0.772) =0.09, ence through ant preferencechemo/metabotypes to different plant then considered in a a considered in then L. niger before aphid colonisation. Separate models were run run were models Separate colonisation. aphid before atial autocorrelation and neighbouring autocorrelation and therefore atial use ants were almost always present after aphid aphid after present always werealmost ants use nised, controlling for the number of weeks before before of weeks number controlling the for nised, genotype) can be considered independent or there orthere independent considered be can genotype) et al. the number of times ants of each species were were species each of ants of times number the multinomial context todetermine if each In R, were 2018)). these convertedtables L. niger L. niger L. present before aphid colonisation colonisation aphid before present and M. rubra 1,20 ) before aphid aphid ) before =0.52, P=0.478) or L. niger

et Accepted Article This by is protectedarticle reserved. Allrights copyright. (Clancy identified previously (A-E) clusters metabotype five same the into grouped plants the profile, metabolomic non-volatile plant bytheir aphids hosted that plants clustering After other clusters, which showed stronger differentiation differentiation stronger showed which clusters, other three the than S5) 5; Fig. and 2, 1, (clusters individuals more contained and related closely more showed wasthere six a evidence statistical that for analysis clustering hierarchical K-means While data. overall the as structuring similar showed data and2015 2014 the both points; time all across pooled clusters, genetic six into clustered The aphids site. field the across genotypes aphid of clustering spatial no indicating S2c), Fig. 0.481; = P 0.002, r=- test (Mantel site field the within plants between distance geographic and aphids of distance genetic the between association no was There 1). (Table population aphid the within diversity total, weidentified 228MLGs (multi-locus genotypes) from aphids,349 indicating high genetic and 204aphids from occupied the 50 plants in 2015 (total 349 aphids from individual87 plants). In structure. genetic population Aphid and Fig.visualizationfor S4 a of multiplex the mixes). details primer for S1 Table (see PCR-multiplexes two of development successful the to °C, leading 18microsatellites were thefinal detected. of All perfectcontaining (only pure repeats), and imperfect28,381 (containing mutations) microsatellites] development. microsatellite and sequencing genome Aphid similar plants across field the site (Mantel test, r=0.038, P=0.019; Fig. S2b). metabolically of clustering no hence and autocorrelation spatial for evidence no was there Again,

We collectedWe 145 aphids from the 61 occupied plants in2014, had the same optimal annealing temperature of 60 60 of temperature annealing optimal same the had phid genetic clusters, three of these clusters were clusters these of three clusters, genetic phid from others all (clusters4, 3, and Fig 6; S5). A totalofA microsatellites 30,753 [2,372 et al. et 2018). 2018). Accepted Article 2015 11 2014 15 Year This by is protectedarticle reserved. Allrights copyright. Table 1. ( ( of amounts higher with associated was cluster genetic aphid This compounds. individual different of concentration the in changes associations. The main result here showed that of models >5% in retained were that hydrate) plant chemotype classes (Fishers Exact Test: P=1.0 ×10 and clusters genetic particular from aphids between associations non-random foundstrong We a particular volatilechemotype (Fisher’s Exact testP=0.775). to belong not did metabotype one of plants i.e. metabotype, and chemotype volatile plant between chemo/metabotypes. plant and genotypes aphid between Association were also observed (Fig. 1). Other notable notable associat Other observedwere 1). also (Fig. expected than cluster this from aphids more where S7), (Fig. 4.1 class chemotype the within plants dihydrocarvone, of 52.4%; Nevertheless,S3b). Fig. we identified nine compounds (eucalyptol, ( retained in than more the half models (eucalyptol with aPEP of 56.3% and ( were compounds two only that showed we clustering, genetic aphid the on plants fromthe emitted compounds volatile 22 the of impact individual the assess to (BMA), Averaging Model Bayesian Using 4.2 theat start of the season and in later the 2.2 season. classes 0.896, P r= 0.001). = From data, the 2015 we found these aphids more often onchemotype often chemically-distinct on two plant chemotypeclasses and (2.2 4.2: betweenANOSIM chemotype more significantly found was that 4 cluster genetic aphid except class, chemotype plant a single on expected than often more found each were clusters aphid other All 1a). Fig. 4.1; class chemotype plant on 1 cluster genetic from (aphids class single a on expected than often less observed being cluster one only with chemotypes, plant certain on expected than common more were aphids that showed associations of majority The 1). (Table associations non-random significant found we also Z Standard Error Error Standard SE, aphids. 271 from is data metabotype points; time different the across analysis) (contingency rarefaction. Chemo/metabotype-aphid genotype columns give results of Fisher’sExact tests by size sample in differences for controls genotypes) (multi-locus MLGs of number Expected 6 9 23 )-sabinene hydrate (Fig. S6). These compounds were also all found in higher concentrations in in concentrations higher in found all werealso compounds These S6). (Fig. hydrate )-sabinene olddt 8 39 2 1. 13) 1.0×10 (1.35) 19.2 228 349 87 Pooled data collection collection Summary of aphidsamples collected and in2014 2015. th th Date of of Date rd th th Ags 0 1 5 50(.0 008 0.027 0.018 2.2×10 15.0(0.00) 15 17.9(1.57) 72 21 106 10 42 August July Jn 2 1 9 90(.0 006 0.479 0.026 5.4×10 (0.00) 19.0 (1.21) 19.4 19 108 21 145 12 61 June July Jl 1 6 7 69(.4 000 0.011 0.0002 (1.54) 16.9 37 56 21 July α -copaene, terpineol, of plants of plants Number colonies colonies aphid of Number Z )- β β -terpineol, ( -terpineol, -cubebene, germacrene-D, germacrene-D, -cubebene, MLGs MLGs and could explain some of the genotype-chemotype genotype-chemotype the of some explain could and aphid genetic cluster 6 is most associated with with associated most is 6 cluster genetic aphid ions include there being more aphids from genetic genetic from aphids more being there include ions E )-dihydrocarvone, )-dihydrocarvone, -7 MLGs (SE) ; Fig. 1a). Within sampling times and years, expected α -pinene, and ( and -pinene, α Chemotype- There was no association -copaene, ( genotype genotype Fisher’s P Fisher’s aphid aphid Z )- Z β )- -terpineol with a PEP PEP a with -terpineol -7 -6 -6 β 2.0×10 0.006 0.003 -terpineol, ( -terpineol, ) β Z

-cubebene, and and -cubebene, )-sabinene )-sabinene Metabotype- ( genotype Fisher’s P Fisher’s aphid aphid E )- -7

) Accepted Article This by is protectedarticle reserved. Allrights copyright. ×10 P=2.0 Test: Exact (Fishers plants the among genotypes of effect a strong detected we also Similarly, combination of compounds. the rather but effect compound single a unlikely is structuring aphid the on effect any again, clusters also showed increased/decreased levels plant other associations, these Despite S7). S6, (Fig. concentrations eucalyptol by higher influenced of levels cluster 3on plants withinchemotype class 1.2 than expected (Fig. 1), whichcould be driven by lower of the mid- three tolate-season sampling 2015 points, and singlethe time-point (Table in 1). 2014 Thes 1b). (Fig. E metabotype from 6 genotype aphid were collectedfrom plants of metaboty more often α -pinene (Fig. S6, S7), or the association between aphids in cluster 5 and plants in 3.1 3.1 in plants and 5 cluster in aphids between association the or S7), S6, (Fig. -pinene

plant metabotype on the distribution of aphid aphid of distribution the on metabotype plant of one or more of these compounds and thus, thus, and compounds these of more or one of pe C; aphid genotype 5 from metabotype B; and, B;and, metabotype from 5 genotype aphid C; pe e associations were also significant within each each within significant also were associations e -7 ). Here, aphids from genotype cluster 2 2 cluster genotype from aphids ). Here, Accepted Article collected ineach year, andthe total, are we aphids where combination single the grey) combinations where show the aph (fromChi-square number with expected Numbe random. at expected than often plan colonised clusters genetic different werestruct Aphids groups. metabotype chemotype, and metabotype. plant(b) 1. Figure

Distribution of aphid genotyp aphid of Distribution e e u u r t t T T i re observed less often than expected. Number of aph of Number than expected. often observed less re formula) underneath in parentheses. Coloured cells ( cells Coloured in parentheses. underneath formula) s show the observed number of aphids in each categ each in aphids of number observed the show s s across plants as associated with (a) plant volatile volatile plant (a) with associated as plants across s shown toright the the of tables. s from different chemotype classes, and metabotype and classes, chemotype different from s ds were observed more often than expected, and in in and expected, often were more than observed ds red intored six geneti different he plants clustered into nine chemotype classes and and classes chemotype nine into clustered he plants c groups (clusters). Aphid (clusters). c groups

w w o o s s s non- ids ids five five from from ry, ry, more hite hite Accepted Article 2). chem plant different across of aphids number the This by is protectedarticle reserved. Allrights copyright. patrolling aphid before ( arrival than expected fromgenetic this cluster on on aphid geneticcluster 5and plant chemotypeclass depended 3.1 on explorin further When 2). (Fig. B from metabotype L. niger observed onplants, 82%of these compared toonlyof% 44 plants withinclass (Fig. 2.1 2). Further, colonisation, pr the on depended metabotypes and chemotypes plant different the across genotype per collected aphids of number The species. ant this without aphids no with plants from aphids 50 to compared ants, scouting which on plants from aphids 76 collected We tables. contingency for models log-linear using associations We tested potential the impact of interactingon species aphidgenotype plant – chemotype species. interacting by mediated associations chemo/metabotype –plant genotype Aphid expected even when no ants had been observed been ( had whenexpected noants even than aphids more with role, a play to found still was preference aphid while 2); (Fig. plants on these of ants presence increased the by enhanced was 4.1, class chemotype in plants and 6 cluster genetic frequently by aphids from genotypecluster 5(t=2.95, P=0.004; Fig. S8). on plants from chemotypeclass 2.1(t=4.34, Fig.P<0.001; S8), and on plants colonized more rates parasitism higher was there example, For aphid. and plant of combinations certain in success parasitism higher was there that rather but colonize, aphids where can influence wasps parasitoid bothchemotype metabotype)and parasitoidand (Table is presence unlikely2) mean that to the (i.e. chemo(metabo)type or plant presence, parasitoid and genotype aphid between The interaction by exclusion competitive of effects confounding through potentially 2), (Fig. significant statistically not presence The distribution. nest byant explained arenot associations these thus and 2017), Zytynska & Weisser (Senft, presence of Myrmicarubra L. niger niger L. L. niger L. also exhibited preferences across plant metabotypes, with ants observed on 78 % of plants plants of % 78 on observed ants with metabotypes, plant across preferences exhibited also (Senft, Weisser &Zytynska 2017). L. niger L. L. niger niger L. ants had been observed before aphid colonisation, and 48 aphids from plants with no no with plants from aphids 48 and colonisation, aphid before observed been had ants ants showed some variation acrosschemotypes and metabotypes but this was ants ( ants ants were found more often on plantschemotype found were ants on often from more 4.1, class with ants Χ M. rubra M. 2 =8.22, P=0.004). Ant nests were distributed throughout the field site Χ 2 =5.54, P=0.020). Similarly, the association between aphids in ants had less impact on the distribution of aphids, only altering altering only aphids, of distribution the on impact less had ants ly those plants where ants had observed been had ants where plants ly those otypes, but not across plant metabotypes (Table (Table metabotypes plant across not but otypes, Χ g data, found we the the that association between 2 =5.22, P=0.022), effectthis was stronger in the esence of these ants (Table 2). Before aphid aphid Before 2). oftheseants (Table esence M. rubra before aphid colonisation and 74 74 and colonisation aphid before L. niger L. ants, with more aphids aphids more with ants, Accepted Article This by is protectedarticle reserved. Allrights copyright. ● chemo(metabo)types plant across genotype per of aphids Lines inbold important represent the informationof on role the interacting species on numberthe from aphids of numbers different that analyses earlier confirms simply this as out, greyed are interaction plant x aphid and the separately (for 2014data only). main The effects interact and individual the determine were runto distribu error poisson with were GLMs, run Models aphids of number the on species of interacting effect the understand Table 2.

P<0.10,**P<0.01, *P<0.05, ***P<0.001 Summary of using log-linear models used to analyse 3-way contingency tables to to tables contingency 3-way analyse to used models log-linear using of Summary number of aphids aphids number of Response: ln 8 84 009 4 41 <0.001*** 0.019* 74.1 0.003** 11.8 42.3 0.009** 15.4 4 4 20 5 <0.001*** <0.001*** 0.019* 80.6 0.003** 0.200 81.0 <0.001*** 18.4 23.1 7.3 74.1 0.009** 0.002** 42.9 15.4 5 40 8 8 4 5 20 <0.001*** 5 x Plant Aphid 80.6 <0.001*** Para Plant x <0.001*** <0.001*** 0.019* 80.6 86.2 37.1 0.200 <0.001*** Para Aphid x 0.012* 18.4 5 74.1 7.3 12.9 <0.001*** Plant 0.003** 1 44.8 17.8 62.3 5 40 Aphid genotype 8 8 4 Parasitoids 1 4 <0.001*** 5 <0.001*** 20 62.3 5 x Plant Aphid <0.001*** 80.6 <0.001*** <0.001*** MR xPlant <0.001*** 0.019* 80.6 39.2 88.4 MR x Aphid 18.4 0.003** 5 17.8 Plant 5 8 40 Aphid genotype 8 Ant ( 5 <0.001*** Aphid x Plant 80.6 LN x Plant LN xAphid 5 Plant Aphid genotype Ant ( M. rubra M. L. niger L. 1 . .1* 64 0.012* 6.4 1 0.012* 6.4 1 ) 1 . .3* 47 0.031* 4.7 1 0.031* 4.7 1 ) fCis P f h-q P Chi-sq df P df Chi-sq different genotypes were collected on different plant variants. variants. plant different on collected were genotypes different Chemotype Metabotype Metabotype Chemotype of aphid genotype and plant chemo(metabo)type, ion effects of plant chemotype and metabotype metabotype and chemotype plant of effects ion tion on the number of aphids. Separate models models Separate of aphids. number on the tion 4 4.0 0.405 0.405 4.0 4 Accepted Article withpotential the speciation todrive (St overco-evolutionaryseasons multiple r evoluti have could This field. the in level this work toshow thatplant chemical va Zytynska 2014; Turnbull & Powell Kanvil, ( individuals) distinct or morphologically experiments, controlled in documented al. &Preziosi(Rowntree,Whi 2011; Shuker structure the of impact ecological strong wit Plant level. genetic the at population variation chemical plant that indicating field. associations mediated These were associated with the distribution of aphid che within-species plant We found that Discussion were ants which on groups the highlight colonise were never that plants includes we of thenumber control for to further which present wereants before aph the different plant volatile chemotypes and ( ants of presence The 2. Figure 2019). Interactionsva2019). between plant Lasius n Lasius m e e e e c c t r i i o S t o S t i i o d ireman, Nason & Heard 2005). 2005). &Heard Nason ireman, riation can structure herbivore populations at the ge the at populations herbivore can structure riation ger by interactions with aphid-tending mutualistic ants, ants, mutualistic aphid-tending with interactions by hin-species variation is now widely accepted as havin as accepted widely now is variation hin-species metabotypes. et al. et associatedof communities and speciesinteractions d colonisationd data (2014 only). Analysis used binomi ould have both direct and indirect effects on the aph the on effects indirect and direct both have ould sponsescould lead towards host-associated differen plants. the half than less on observed iants (genotypes or chemotype) have only before before be chemotype) only have or (genotypes iants ks planta was empty before aphidcolonisation, and ham genotypes across host-plants at the small scale of a s a of scale small the at host-plants across genotypes erviceCaillaud 1984; ical variation of volatile and non-volatile compounds compounds non-volatile and of volatile variation ical nary consequences, for example if such interactions interactions such if example for consequences, nary ften using highly-differentiated plants (e.g. crop vari crop (e.g. plants highly-differentiated using ften across the whole the across season. The intercept to isset 50 and and etal. 2014), but not under natural conditions. natural ex We under not but 2014), Myrmica rubra 2012; Balint Datashows percentage ofplantsthe et al. et et al. ) before aphid colonisation a colonisation aphid before ) 1995; Zytynska Preziosi & 2016;Crutsinger 2016; S S o n e t % i c e g g t tend tend ingle ingle persist al GLM al was was d iation enft 2011; n etic n ross a ties , to et

Accepted Article ( This by is protectedarticle reserved. Allrights copyright. Woodcock 2005;Beyaert & HilkerIndeed, 2014). thatwe found thenot it is most dominant & Wadhams (Bruce, associations these drive that volatiles plant the of ‘plume’ or odour-ration potentially toxic compound will have astrongimpact highconcentrations, in most it is likely the any while and high, was diversity chemical system, our In 2003). Kumar & Prajapati Tripathi, (Imdorf invertebrates to toxicity andfumigant contact have to been found ( including compounds, plant by specific be explained could associations these of some that wefound chemotypes, volatile plant the Across of local extinction through predation inthis system (Senft, Weisser & Zytynska 2017). chance the reduce to found also were sizes population higher increased; are rates growth population is season the across plant on the and persisting plant a colonising successfully of probability the profile, volatile the on based ahost choose actively (Clancy they belonged chemotypes volatile which of irrespective metabotypes ‘preferred’ the to belonging plants all almost colonised on and later (Clancy season the of part early the in chemotypes volatile ‘preferred’ colonised aphids & Zytynska 2017), and stronger genotype-metabotype associations. previouslyWe showed that Weisser (Senft, persistence colony longer to leading rates growth population high with performance; onaphid metabolites secondary plant of role the highlights periods, three later the all in associations metabotypes and aphid genotypesvery inthe sampling first period insignificant but 2015, abundant are winged aphids when July in phase dispersal main the during preference) aphid in variation (indicating genotypes of aphid distribution the on chemotype volatile plant of effect astronger with this, support volatiles even before settling on, and probing,plant a(Powell, Tosh &Hardie 2006). resultsOur the detect can aphids the since metabolites, than 2010) Rodriguez-Saona & (Szendrei volatiles plant in variation by more driven be to likely is hosts plant to aphids dispersing of choice Active chemotype. (Clancy feeding aphid neither the plant volatile chemotypes menor the that showed work Ourprevious 2016). Weisser & (Zytynska studies experimental from various Host genotype preference host-preferences. specific distributed across whole fieldthe site, sugges we noof pattern spatial autocorrelation, with plantschemotypes of different metabotypes and found was there Since plants. the across genotypes aphid of distribution arandom with expected be would than metabotype, plant particular a on often more observed three and chemotype, plant a particular on abundantly more found was clusters genotype these of one but All groups. main six into clustered Weisser Loxdale,2009; Massonnet &Weisser 2010). Despite this high genetic variability, the aphids of genetic diversity, confirming resultsother from studies on the same species (Loxdale, Kigathi & levels high observed We aphids. the genotype to which with loci microsatellite nine of amplification We developed two successful multiplex-PCRmixes 18microsatellitefor loci, each allowing the variation chemical plant of effects Direct Z )-sabinene hydrate, hydrate, )-sabinene et al. et α -pinene and eucalyptol. Many of these chemical compounds have previously previously have compounds chemical of these Many and eucalyptol. -pinene 2016; Clancy (Senft, Weisser & Zytynska 2017). Th 2017). &Zytynska Weisser (Senft, Z et al. )- β -terpineol, ( -terpineol, 2018), 2018), and represent thus direct ‘base’ ofeffect the increased on certain ‘optimal’ metabotypes where where metabotypes ‘optimal’ certain on increased t that these associations are driven by aphid byaphid aredriven associations these that t tabotypes studied here were likely induced by by induced were likely here studied tabotypes et al. et of aphids to different plant variants is known known is variants plant different to aphids of 2018). Hence, while aphid genotypes might E )-dihydrocarvone, )-dihydrocarvone, e lack of association between plant plant between e lack association of etal. α -copaene, 1995; Isman 2000; etal. β -cubebene, -cubebene, 2016) 2016) Accepted Article communities. natural in impacts evolutionary and ecological cl our analyses enemypreferences, natural ant, and aphid, test empirically to needed are experiments controlled While ignored. often are species among trophic levels(Fronhofer implications research for inthe area of metacommunity ecologywhere interactions across multiple has This tansy. as such species plant host patchily-distributed for particularly chemo(metabo)type; non-induced plant individual the to enemies natural and ants, aphids, interacting the of response the to due host-plant individual the of level the at occur can interactions community that shows work metabolites (Jansen suchvolatiles as that attract natural enemies mutualistic ants. onStudies plant chemicals often focus on those induced the feedingby herbivores, with interactions by mediated as indirect, and aphid, and plant the between direct both was with plant within-species chemical variation inplantvolatile andnon-volatile chemicals. This effect associated was collection, data of years two across genotypes, aphid of distribution The site. field our across structuring genetic fine-scale exhibits population aphid the that show could we Overall, Conclusions occurs. chemo(metabo)types plant across genotypes aphid of dispersal ant-borne if see to experiments controlled in tested empirically be needto interactions such system, our tansy In metabotypes. plant in variation to related be may which 2017), suitability assessed is via aphid honeydewcomposition (Collins Leather& 2002; Züst & Agrawal host-plant that speculation with plant, onthe settles aphid the until them with stay and host-plants This by is protectedarticle reserved. Allrights copyright. presence. ant enhanced by just were others whereas arrival, aphid before observed been had ants these where plants to limited were combinations genotype chemotype-aphid plant Some 2017)). Zytynska & Weisser (Senft, by and metabotypes chemotypes volatile plant different for preference via potentially ants, mutualistic with interactions through structure, genetic population aphid influenced indirectly variation chemical Plant variation chemical plant of effects Indirect population scale) &Rodriguez-Saona (Szendrei &Hilker 2010; Beyaert &Card Webster 2014; 2017). the at (effective apatch within individuals among distinguish to it allow than rather scale), landscape the at (effective plants host of patch a find to herbivore specialist a for cues sufficient provide only may chemical dominant a as surprising not perhaps is This abundance. intermediate of those rather but clusters, genotype aphid and chemotype plant between associations the drive that chemicals etal. L. niger L. et al. 2009; 2009; Macel Lasius niger (the mutualist (the with the on effect the this strongest aphids in system 2015;Resetarits &Silberbush 2016), as well as genetic interactions etal. ants have previously been reported to move aphids among among aphids move to beenreported previously have ants 2010; Bernhardsson (Dicke & Baldwin(Dicke & 2010), or other plant secondary early show that these associations can have real real have can associations these that show early et al. et 2013; Marti et al. et 2013). Our Accepted Article This by is protectedarticle reserved. Allrights copyright. (Zytynska Data available the from Dryad Digital Repository http://dx.doi.org/10.5061/dryad.mm7bj56 Data accessibility revisions. to contributed authors all and SZ, by written draft first a SZ, by analyzed were data All CW. and SZ, MS, SP, SS, YG, by performed was development microsatellite and analysis This study was designed SZ, by JPS. WWWand Field was data collected SZ, by MSand MC.Genome contributions Author publication. for accepted when dataset supplementary data through Senft et al. (2017) and the molecular will data made be publically available as a SCHN 653/7-1 Forschungsgemeinschaft GermanResearch (DFG, Deutsche the by funded was project This site. field the on work to permission the Haslberger for Irene work extractions, forand field Moeller DNA Andreas for Lopez We thankJose Acknowledgements et al. et 2019). ). Chemical data available is through Clancy (2016), etal. Clancy al. et field2018, Foundation) (project numbers: WE 3081/25-1 and WE numbers: (project Foundation) Accepted Article Döring, T.F.(2014)How aphids find their host plants, anddon't. how they evolutionary to biology from molecular defences: plant Induced (2003) M. Hilker, & M. Dicke, Fronhofer, E.A., Klecka,Melián, J., C.J. &Alterm Flatt, &Weisser, T. effects of W.W.The (2000) mutualistic on aphid ants lifehistory traits. Fiehn, Combining O. 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