This is a peer-reviewed, post-print (final draft post-refereeing) version of the following published document, This is the peer reviewed version of the following article: Knowles, Sarah C L and Wood, Matthew J and Alves, Ricardo and Sheldon, Ben C (2014) Dispersal in a patchy landscape reveals contrasting determinants of infection in a wild avian malaria system. Journal of Animal Ecology, 83 (2). pp. 429-439, which has been published in final form at http://onlinelibrary.wiley.com/doi/10.1111/1365-2656.12154/abstract. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving. and is licensed under All Rights Reserved license:

Knowles, Sarah C L, Wood, Matthew J ORCID: 0000-0003-0920- 8396, Alves, Ricardo and Sheldon, Ben C (2014) Dispersal in a patchy landscape reveals contrasting determinants of infection in a wild avian malaria system. Journal of Animal Ecology, 83 (2). pp. 429-439. doi:10.1111/1365-2656.12154

Official URL: http://onlinelibrary.wiley.com/doi/10.1111/1365-2656.12154/abstract DOI: http://dx.doi.org/10.1111/1365-2656.12154 EPrint URI: http://eprints.glos.ac.uk/id/eprint/570

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This is a peer-reviewed, post-print (final draft post-refereeing) version of the following published document:

Knowles, S. C., Wood, M. J., Alves, R., & Sheldon, B. C. (2014). Dispersal in a patchy landscape reveals contrasting determinants of infection in a wild avian malaria system. Journal of Animal Ecology, 83(2), 429-439.

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The URL for the published version is http://dx.doi.org/10.1111/1365-2656.12154

Disclaimer

The University of Gloucestershire has obtained warranties from all depositors as to their title in the material deposited and as to their right to deposit such material.

The University of Gloucestershire makes no representation or warranties of commercial utility, title, or fitness for a particular purpose or any other warranty, express or implied in respect of any material deposited.

The University of Gloucestershire makes no representation that the use of the materials will not infringe any patent, copyright, trademark or other property or proprietary rights.

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PLEASE SCROLL DOWN FOR TEXT. Accepted Article Section :Parasite andDisease Ecology Editor : Mike Boots type Article :Standard Paper Accepted Date : 14-Sep-2013 Revised Date :05-Sep-2013 Received Date :09-Feb-2013 This article This protectedis by Allcopyright. rights reserved. 10.1111/1365-2656.12154 doi: version between Pleaseof and Versionthis tothe lead Record. this differences article cite as through thebeen typesetting,copyediting, pa This article hasbeen accepted for publicationand undergone fullpeer review but has not infection in a wild avian malaria system

[email protected] Plasmodium Keywords avian of and Timing infection malaria location head: Running 3 2 1 Knowles L. C. Sarah Dispersal in a patchy landscape rev Cheltenham GL50 4AZ, UK Place, London 1PG, UK W2 UK 3PS, Department ofInfectious Disease Epidemiology, Imperial College London,St Mary's Campus, Norfolk Edward Grey Institute, Department Zoology,of University of SouthOxford, Parks Road, Oxford OX1 Department ofNatural and Social Sciences, Universityof Gloucestershire, Francis Close Hall, , haemosporidia, host, parasite, maternal effects, GIS, territory territory GIS, effects, maternal parasite, host, , haemosporidia, 1,2 , Matthew J. Wood J. Matthew , gination and process, which proofreading may 1,3 eals contrasting de eals contrasting , RicardoAlves 1 andBen C. Sheldon terminants of 1

Accepted Article This article This protectedis by Allcopyright. rights reserved. diseases), the spatial location of infection, and the relative importance of the of parasite location of infection,spatial and importance diseases), the relative where hostsorvector-borne are (e.g. parasites mobile systems host-parasite for parasites in wild coevolution. However, the host-parasite is critical to understanding when, where exactly hostswith how Understanding infected and become 1. Summary systems. inmulti-parasite processes predicting such of the complexity also illustrate they processes, coevolutionary many for predictions species-specific parasite this implies Because stages. life-history atdifferent acting potentially parasites, these two from pressures selection hosts in bemay to divergent findings These subject this population suggest 4. event. dispersal major this during occurs infection that indicating potentially distance, dispersal with postnatal associated ispositively probability and infection unpredictable, another ( parasite species of distribution the Conversely, spatial dispersal. postnatal through infection avoid potentially and exposure their alter principle in could hosts stable, temporally is parasite this of distribution the because and territories, on breeding settled have birds after occurs infection that indicate ( species Forone species. parasite malaria sympatric two between markedly differs infection of and timing location the showthat We 3. two. the between dispersal postnatal byaswellas sites, orbreeding at natal experienced by conditions determined is parasites malaria avian by which infection to extent wetest the blue tits, of population referenced aspatially from dataset longitudinal asix-year using Here, 2. uncertain. often are stages, life-history host at successive exposure

P. circumflexum P. relictum ), our analyses ), our analyses ) is Accepted Article This article This protectedis by Allcopyright. rights reserved. 2009), acting at various stages throughout an individual’s lifetime. Elucidating the the Elucidating lifetime. an individual’s stages throughout at various acting 2009), Wolinska and King Mitchell and Read 2005, et 2005, al. (Mackinnon effects parental and will be environmental traits related a by of genetic, underpinned combination infection- in variation phenotype, anywith As 2001). (Combes infections parasitic to andsusceptibility exposure their in markedly vary individuals populations, natural In Introduction ability to disperse (Heeb et al. 1999, Fellous et al. 2011) or to compete for and settle settle and for tocompete or 2011) etal. 1999, Fellous al. et (Heeb disperse to ability infection hosts’ reduce example, may in probability. For variation infection spatial within-population influence significantly and could spatial scales, at small important bemay etal. Hostmovements particularly 2006). Farnsworth et 2006, al. (Bodker prevalence variation play in a driving role spatial in therefore can diseases, borne vector- for vector movements as well as movements, host and life-histories, their over hosts mayacquire locations infection at arange of when infections are long-lasting, andparticularly hosts are mobile, if However, locations. sampling across exposure parasite in variation environmental reflect to assumed often is prevalence infection in variation spatial the parasites vectors, andtheir of known affect distribution are to and abiotic stage, suchas notsessile. hosts factors, are climate habitat, Since and life-history a to particular known beexposure confined isnot when to particularly difficult, be can infected become where wildhosts when and Understanding to parasitism. evolve in response behaviour and life-histories how hostphysiology, to understanding andisfundamental system, host-parasite any in a challenge key constitutes operate, whichatthey stages the life-history and theseof factors, relative contributions

Accepted Article This article This protectedis by Allcopyright. rights reserved. instance, how hosts encounter parasites in the hosts time andspace howparasites toaffect instance, encounter is expected For processes. coevolutionary host-parasite understanding for critical is infection of context life-history and spatiotemporal the elucidating challenging, Although habitats. in marginal prevalence infection increased or hosts infected of clustering to leading territories, quality high on Avian malaria parasites ( parasites Avian malaria for. be selected may 2010) al. et (Little or tolerance resistance host or 2001), al. et (Boulinier choice or mate settlement dispersal, biased of parasite including avoidance mechanisms behavioural cases, Insuch bebeneficial. unlikely such to are transfer as antibody effects maternal short-lived inlife, acquired later infections for Conversely, 2009). Schmid-Hempel and Sadd 2003, al. et Grindstaff 2001, al. et (Gasparini transfer antibody maternal suchas effects maternal adaptive of evolution may the selection favour parents, affecting as are parasites life andtotheir similar offspring exposed reliably those early in acquired generally infections are instance, evolve.if hosts For mechanisms defence of type the will influence hosts parasites encounter at which history stage life- the Furthermore, 2009). and Nuismer Gandon etal.2007, Foster 2004, Ebert and (Kawecki adaptation local host-parasite for potential and the et al.2011) 2009, Best al. et Mealor 2007, Wild and (Boots host resistance and virulence parasite of evolution 2009, Bensch et al. 2009, Marzal et al. 2011). Spatial variation in the prevalence of of prevalence the in variation Spatial 2011). al. et Marzal 2009, et al. Bensch 2009, etal. Hellgren 2004, Fallon and (Ricklefs coevolution and interaction host-parasite aspects of many investigating for system usedas amodel parasites, vector-borne these parasites has been widely documented, at broad geographic scales has widelyparasites these at geographic asbeen documented, broad well as Plasmodium are spp.) a group globally widespread of

Accepted Article This article This protectedis by Allcopyright. rights reserved. (Valki infections chronic are haemosporidian mobile, arehighly birds since However, 2011). et al. 2007, Sehgal etal. 2003, Wood and Åkesson (Bensch populations host within for the other species ( theother species for scenarios could drive spatial variation in variation spatial coulddrive scenarios transmission several Thus thisstudy). from data below for see 2005; al. et (Matthysen between successive being movements breeding attempts generally far more limited with breed, to settling and nest the fledging between occurs event dispersal major the and breeding, during are territorial tits unclear. Blue remains as adults, inlater life vs. in life early experienced conditions of importance relative the and each species, for occurs where infection whenand patterns, spatial Despitesuchcontrasting al. 2013). species ( parasite malaria two common oneof for location breeding to according probability work on spatial this hasconsistent in population variation infection demonstrated Previous this host process. of in dispersal role andthe potential infection, determines stages life-history at different exposure how to ascertain parasites malaria by affected of blue tits( population awild, spatially referenced study of a long-term weusedata from infection. Here determine life-history stages different events at how understanding yet for essential life are rare, times throughout multiple sampled studies, onlypopulations once. Longitudinal in which are captured individuals or with individuals are cross-sectional, parasites onthese existingstudies of majority the Moreover, unknown. isoften hosts’life-history of infectionwithin and location dispersal (3) infection of hosts before postnatal dispersal (with or without spatial or spatial without (with dispersal postnatal hostsbefore of infection (3) dispersal postnatal by natal sites limited across followed inexposure sites (2) spatial variation breeding parasites at to in exposure variation spatial (1) including: sites, breeding ū nas 2005), and vector ecology is often not well understood, the exact timing exact the timing wellnot understood, often is ecology vector and 2005), nas Plasmodium circumflexum Plasmodium P. relictum ) (Wood et al. 2007, Knowles et al. 2011, Lachish et et Lachish 2011, etal. Knowles et al. 2007, ) (Wood ), while there is little spatial structure in prevalence prevalence in structure islittle spatial while there ), P. circumflexum P.

infection probability acrossprobability infection Cyanistes caeruleus Cyanistes ) Accepted Article This article This protectedis by Allcopyright. rights reserved. dispersal (2) infection occurring during postnatal dispersal (3) infection occurring at occurring at (3) infection dispersal postnatal during occurring (2) infection dispersal postnatal subsequent by spatial pattern this of by disruption followed natal sites, at exposure in variation spatial (1) including: observation, this underlie could exposure host of scenarios possible several al2013), et (Lachish sites breeding across Similarly,infected birds. whilst non- and infected of settlement non-random by followed risk) infection in variation status, and whether this is modulated by dispersal distance. Most strikingly, our Most dispersal our strikingly, whether distance. thisstatus, isandby modulated parents and canin between drive offspring theirinfection similarity environment whether a shared status, to examine ininfection associations parent-offspring also testfor sites. or breeding while natalWe occurs are at often they infection more whether test thisshould place, and that time at risk exposure for a proxy therefore in local viaa their vicinity bite mosquito hosts infected of areservoir from infection acquire birds that Assuming effects. these or distance and natal breeding may dispersal sites, howtheir modulate surrounding population breeding the among prevalence local parasite by predicted best is adult a breeding as probability infection whether wetest population, inthis bred later birds that hatched on locally of data years’ Usingsix infection. of and timing location the alone to infer data using hostinfection approach, wean alternative took dispersal), and bitingrate distribution, competence, spatial vector (e.g. life-history stages different exposure risk at be used to predict malaria ecology that could about vector knowledge of theabsence In remain uncertain. malariatransmission avian for responsible species the vector here, studied population hosts. Inthe among infection transmitting and between acquiring because vectors long perhapsdistances fly examined, the scale on exposure in variation nospatial (4) date, to examined that than smaller exposure inparasite variation environmental scale with the of sites, breeding P. relictum , and that these prevalence measures are are measures prevalence these that and , prevalence is not spatially predictable predictable is notprevalence spatially

Accepted Article This article This protectedis by Allcopyright. rights reserved. Field procedures procedures Field andMethods Materials population. single host this within pressures sympatric two when by come toand be ininfected hosts these how key suggest differences results are commonly detected in this population (based on cytochrome cytochrome on (based population this in detected commonly are of clades divergent Two was used. method acetate ammonium astandard whilst 2006-9 in kits(Qiagen), extraction DNeasy extracted wasDNA using all DNA 2004-2005, was from blood Genomic samples.extracted from samples For parents and their in recruits infections malaria Diagnosing monitored. be could population breeding the to recruitment their that such ringed were nestlings born nestbox- All characteristics. plumage by determined age and patch brood a of (male) or absence (female) onthe presence based were sexed Adults cycle. in theirannual or all brachial Thus birds jugular werevenepuncture. at astandardised sampled point by licence under were taken blood samples and entrance, the nestbox of front nets in traps, orwith orusing by within nestbox 6 hand day post-hatch, mist either the and 15 was between whentheirbrood were captured parents all possible, Where attempts. all reproductive for was determined hatched) egg first which the on date (date hatch that such intervals, regular at monitored were site study atthe nestboxes all (c.1160) (April-June), year each season breeding the During in nestboxes. annually breed pairs tit blue 250-450 whereapproximately UK, Oxford, near woodland deciduous mixed a 385ha 1˚20’W), (51˚46’N, in was2004-9 conducted in TheWoods study Wytham Plasmodium species, suggesting they may exert divergent selection selection exertdivergent may they suggesting species,

Plasmodium b sequences sequences parasite parasite Accepted Article This article This protectedis by Allcopyright. rights reserved. qPCR diagnosis was available. Samples taken between 2005-7 were screened by were screened 2005-7 taken between Samples was available. diagnosis qPCR only samples parental) and (recruit 2008-9 and for available, was diagnosis PCR nested 2004, only in taken samples (parental) for 2004). Thus al. et (Waldenström screened wereSamples ausing from 2004-7 additionally nested cyt assay. this qPCR using were screened 2005-9 from All samples product. specific parasite- wells a contained positive anyof the three replicate as if diagnosed sample Plasmodium Knowles in described as exactly performed were reactions qPCR 1˚C. approximately by differ which products, their qPCR of melting temperature the according to diagnosed al. 2012). et (Lachish negatives islow false rate of the also suggests inthissystem occupancy modelling of any are positive, unlikely. Application cases where false positives of these tested very rare the in repeated were plates and PCRs inall were used controls negative multiple Since infected. as was recorded individual an diagnosis positive a gave assays both onewhere if or methods diagnoses were from available: malaria infection both of measure aconsensus used we accuracy diagnostic to maximise however 2011), al. et (Knowles agreement of level high a show two methods These methods. both and determining the infecting species; species; infecting the determining and quantifying and assay detecting for (q)PCR aquantitative used hereon. We from classification morphospecies their by them to we refer simplicity relictum morphospecies, well-defined to two which nested by PCR), correspond obtained and et al. anda wells DNA replicate copies zeroacross counts), three (including P. circumflexum P. (2011), with parasitaemia scored as the average number of of as number scored the average with parasitaemia (2011), (Palinauskas et al. 2007, Knowles et al. 2011). For For al. et 2011). Knowles etal. 2007, (Palinauskas P. relictum and

P. circumflexum Plasmodium can be reliably bereliably can parasites, parasites, b PCR P. P. Accepted Article This article This protectedis by Allcopyright. rights reserved. for the first few weeks of life, and as breeding adults are territorial and forage in the the in forage and territorial are adults as breeding and life, of weeks few the first for titsare tothe nestbox et Since al. confined 2006). in (Wilkin 2004-5 GPS differential ±3m of an using accuracy mapped to were digitally as precision these some with are known in all nestboxes of yWytham (xand locations coordinates) The exact territories breeding and natal Defining sites breeding and natal Characterising year. Figure 1 provides a schematic overview the analytical approach, which is which approach, analytical the a overview schematic 1provides Figure year. appropriate in the territories breeding or natal at their estimates prevalence local these agiven for recruits of infection status wewhether occurred, tested infection where andwhen and time. To ascertain place that specific riskat exposure of malaria a measure as territory each surrounding blue tits adult breeding among malaria of prevalence local used interpolated the We exposure measures ofmalaria risk atnatal sites Deriving and breeding of Thiessen blue the areawhen calculating for polygons tits. this at of species this site) studies parallel from (inferred titterritories great included we 1986) Perrins and (Minot species the two between occurs competition interspecific and population, in this withtits blue are interspersed titterritories great Since 2007). et al. area(Wilkin territory of measure an individual-specific provides polygons these of v7.8. The area Professional MapInfo software GIS using the season, breeding ineach nestboxes occupied between equidistant lines boundary placing by formed were polygons) (Thiessen polygons years, tessellated natal during its and breeding territory anindividual’s estimate To adult. as abreeding andphase nestling own coordinates givean accurate descriptionof an individual’s location bothduring their these 2005), al. et 2000, Stauss Daenzer etal. theof nest (Naef vicinity immediate Plasmodium

wasspecies by best predicted Accepted Article This article This protectedis by Allcopyright. rights reserved. PCR, as described in Wood Wood in PCR, as described qPCR and data nested from infection consensus using 2004-2009, seasons breeding theof each in adults breeding among prevalence malaria of maps interpolated create to was used v7.8) Professional (MapInfo software GIS below. detail in described territory in was eachyear territory then forthe eachof extracted, two each within prevalence local estimated interpolations, prevalence these on polygons) adults were used, to maximise statistical power. power. statistical tomaximise used, were adults breeding usingall natal interpolations only, at the site local prevalence considering analyses adults in2004). In breedingwere in this dataset as noindividuals wascomplete interpolation natal but recruits, excluded interpolation (breeding different were natal and interpolations of the breeding asthe resolution these analyses, from were excluded hatched in2004 recruits For the same reason, resolution. comparable were of measures these recruits,to ensure excluded datathat infection using derived were andbreeding measures local at natal sites,both of prevalence estimates power explanatory the compared that in analyses Thus, recruits). were individuals of 17-29% year (each of malaria interpolations resolution will the recruits influence of exclusion the However, interpolations. toprevalence contribute andunable to not sampled year birth, and of therefore in all weretheir nestlings risk,as recruits malaria territory does not potential problem of circularity dataset. This apply measures of natal to the all in recruits datafrom infection excluding always derived were territory breeding atthe of prevalence this, interpolations To achieve circularity. some entail would this as prevalence, interpolated when generating not beincluded statusshould infection individual’s focal the infection status, predicts recruit sites at breeding prevalence local whether testing prevalence. When interpolated territory-level of measures tothese torefer isused ‘localprevalence’ term paper, the this Throughout separately. et al. et (2007). By overlaying territory boundaries (Thiessen (Thiessen boundaries territory overlaying By (2007).

Plasmodium species Accepted Article This article This protectedis by Allcopyright. rights reserved. model. the minimum adequate leaving p>0.05, terms remove to sequentially tests ratio likelihood using models full of simplification stepwise backwards involved selection stated, otherwise model Unless in results extremely alland gavesimilar cases(resultsnot also performed shown). were GLMs recruit, one only contributed (76%) broods of majority the since However, effect. a random as entered was brood variable, wasresponse the parasitaemia or status infection recruit where brood), per recruits (mean=1.3 dataset tothe recruits multiple contributed broods some Since 2011). Team, Core Development (R 2.13.2 distance median and IQR in this dataset: postnatal 678m (325-1246m) n=447; n=447; (325-1246m) 678m postnatal dataset: IQRinthis and distance median inblue distances tits dispersal postnatal (dispersal much than shorter generally are attempts breeding between distances Since dispersal capturedbreeding. first where wasand which in an individual asa nestling, the nestbox nestbox it was raised the between distance the as Euclidean wasdefined distance dispersal Postnatal dispersal postnatal Measuring P. circumflexum P. the parasite species, were for two performed and analyses pseudoreplication, to avoid analyses in wasincluded each recruit for capture breeding first the Only (4%). older or (18%) year-olds as2 time thefirst for captured being the remainder yearlings, as time for the first breeding were captured (78%) The majority inanalyses. were included 2005-2009 as adultsand between caught hatched in2004-2008 of 447 totalA recruits analyses statistical and Dataset in thissystem. event dispersal major the reflects dispersal postnatal n=111), (0-88m) 48m breeding and P. relictum P. , separately. All analyses were performed in , R were analyses All version performed separately.

Accepted Article This article This protectedis by Allcopyright. rights reserved. covariate), to test which more strongly predicted recruit infection status. Under the the Under status. infection recruit predicted strongly which more test to covariate), aas year natal with (again inamodel terms both included wethen Results), (see were not strongly collinear and natal breeding sites atindividuals’ local prevalence or sites breeding incontrolling for natal analyses, univariate year. Since estimates of natal at prevalence local by predicted was status infection recruit whether test to used were error structure with abinomial (GLMMs) mixed models linear Generalized breeding sites were also run with parasitaemia (log-transformed (log-transformed with parasitaemia were run also sites breeding covariate. a year as natal including distance, dispersal and postnatal prevalence natal site between interactions status infection we that predicting included recruit models fitted distance. dispersalinfection on status may postnatal testthis depend To possibility, predicts prevalence local site which natal to theextent stable, spatiotemporally period. breeding or infection moreduring the likely nestling/fledging whether analysis occurs test can this recruits, for infection of source as the birds act adult local that assumption Two additional analyses were performed to place our results in context. To assess the the To assess context. in placeourresults to performed were analyses additional Two in detectability. differences infection patterns seenwith infection probability couldbedriven byparasitaemia-related any whether assess to variable, response asthe individuals) among infected copies spatiotemporal consistency in prevalence for each each for prevalence in consistency spatiotemporal If infection occurs after postnatal dispersal, and if infectionriskis if dispersal, and after postnatal infectionIf occurs These models predicting infection status from local prevalence at natal and natal and at prevalence local status from infection predicting models These

Plasmodium species, we examined Plasmodium DNA Accepted Article This article This protectedis by Allcopyright. rights reserved. autocorrelation in prevalence across breeding sites both sites for breeding across in prevalence autocorrelation spatial of level the weexamined Second, territory. on the same repeatedly breeding by individuals bedriven a birds to not could yearling positive correlation ensure a pair years was different by where nestbox of first inhabited only usingthe years, consecutive in occupied at territories prevalence local in estimated the correlation association between maternal (but not paternal) infection and offspring infection in a in infection and offspring infection not paternal) (but maternal between association pushthe would offspring mothers to from protective antibodies of Transfer status. infection in associations parent-offspring influence also could processes biological Other distance. dispersal and postnatal variables parental infection between terms interaction of significance this assessingthe by for tested distance. dispersal We with to diminish postnatal increasing association positiveany parent-offspring predict would scenario Thelatter sites. natal their from far disperse donot offspring but adults, as breeding exposed they if are both or period), breeding period/parents nestling recruit’s at the (e.g. during andtime the same areexposed they place if occur could offspring and parents between infection status in association positive birth. year A of recruit’s inthe as diagnosed was known), parents both status of the (where parents infected of number the total or parent either of status infection by was above which occur that byautocorrelation chance. could spatial of level the whether toassess the data, of permutations Monte Carlo 999 from was constructed envelope asimulation each semivariogram, For infected. was pair breeding the current atleastone of if positive was deemed nestbox geoR. A package using both omnidirectionaland directional semivariograms constructed intheR negative direction, whereas heritability of malaria susceptibility would push the the push would susceptibility malaria heritability of whereas direction, negative Binomial GLMMs were used to test whether recruit infection status was predicted waspredicted status infection recruit whether test usedto were GLMMs Binomial

Plasmodium species, Accepted Article This article This protectedis by Allcopyright. rights reserved. clustering of this parasite in the northern part of the site (Knowles et al. 2011, Lachish Lachish etal.2011, thesite (Knowles of part northern inthe thisparasite clustering of consistent spatial showing years. Inline with previous findings this parasite across of distribution spatial and the consistent 0.663), 0.546 to CI: 95% r=0.608, coordinate: y 0.636; to 0.513 CI: 95% r=0.578, coordinate: (x coordinates nestbox breeding natal andrecruits’ between by correlations dispersal, as evidenced postnatal strong ( positively correlated is territories breeding and natal at individuals’ prevalence local This isbecause 1). this analyses andbreeding sites (Table natal at bothparasite univariate in recruits’ P. circumflexum ofP. location circumflexum Timing and infection parasitaemia, both considering all both considering parasitaemia, and offspring status parental infection between theassociation also examined models. inthese were age controlled for recruit (as a covariate) We and Natal year expected. is distance dispersal postnatal on recruit association the of dependence no effects, genetic or only transfer antibody direction. a positive With in association Results Results effects. analyses parental from of were excluded they and therefore infection status, parental rearing natal and of relative influence the compare to effectively was insufficient recruits these for data The of the study. course the during experiments manipulation size or brood cross-fostering nest due to natal intheir notraised were (19%) recruits 84 et al.2011). (Knowles parasitaemia is which to known year, influence sampling same the by infected were offspring

infection probability was positively predicted by the local prevalence of by prevalence local wasof predicted the positively probability infection r =0.385, 95% CI: 0.291 to 0.472), likely due to a limited extent of extent to alimited likely due to 0.472), 0.291 CI: =0.385, 95% Plasmodium Plasmodium infections and cases where parent and and where andparent cases infections

species, whilst controlling for for controlling whilst species, Accepted Article F (Pearson’s year site the following atthe same prevalence predicted positively year and a one strongly at given nestbox in prevalence risk: in repeatability infection spatial strong is there territories, individual of level atthe we find here 2013), et al. This article This protectedis by Allcopyright. rights reserved. (Fig. S2). Thus postnatal dispersal direction, as well as distance, will likely affect the affect as will as well distance, likely direction, dispersal postnatal Thus (Fig. S2). was negative degrees) (90 direction in anorth-south whereas autocorrelation degrees), (0 axis east-west the along autocorrelation spatial positive indicated semivariograms for of autocorrelation spatial evidence limited provided semivariogram anomnidirectional across sites. breeding prevalence Although in autocorrelation spatial examine to semivariograms plotted we probability, infection Z=5.90, p<0.001), we tested whether the effects reported above were either driven by driven were either above reported effects the whether wetested p<0.001), Z=5.90, test signed-rank n=323; 258-983m, Males:Wilcoxon 531m, n=214; 499-1568m, 952m, Females: distance: and dispersal for IQR (Median thispopulation with sex in associated strongly distance is dispersal postnatal Since territories. breeding on their settled circumflexum that indicate results these Together, 2a). (Fig. dispersal postnatal increasing with butdiminished probability, effect predicted substantially this and infection positively strongly prevalence site natal was short, distance dispersal 2). When (Table distance dispersal on postnatal clearly was dependent topredict infection recruit site prevalence natal of ability the Moreover, 1). (Table significant remained prevalence site breeding only infection status, predicting recruit model same the in entered were sites breeding χ prevalence*Dispersal*Sex (Natal females than males for strongly more probability on prevalence natal of the influence modulated dispersal significant A 3-way suggested weresex sex-dependent. or interaction differences 2 1,155 1 =3.84, p=0.050). To explore the spatial scale over which dispersal could alter alter could which dispersal scaleover spatial the To explore p=0.050). =3.84, = 169.74, p<0.001). When local prevalence of of local prevalence 169.74, p<0.001). = When infections are likely acquired after postnatal dispersal, once birds have birds have once dispersal, postnatal after acquired likely are infections P. circumflexum

P. circumflexum P. circumflexum P. (Fig. S1), directional directional S1), (Fig. at both nataland infection infection r =0.72, P. P. Accepted Article infected: of parents (Number infection status recruit predicted infected still parents significantly site breeding females (Sex*Breeding site prevalence interaction: interaction: prevalence site (Sex*Breeding females p=0.162, n=305; Paternal status: Paternalp=0.162, status: n=305; exposure was controlled for, by inclusion of of inclusion by for, controlled was exposure whererecruit natalin their models site. However, from distances that dispersed short offspring and those parents among infection to exposure of level common a by driven distance distance infected*dispersal was 3; parents (Fig. Number distance short postnatal dispersal circumflexum with Infection behaviour. were bydispersal affected also postnatal associations positive parent-offspring these 3). However, status (Table infection by maternal to extent and a lesser status alone, infection paternal with parasite, were this infected by were infected S1). here (Table reported patterns the drive not do differences parasitaemia suggesting individuals, infected among parasitaemia predicted strongly natal prevalence nor Neither breeding local prevalence predicted predicted prevalence site that breeding sexes, and found two for the differentially sites infection predicted at breeding prevalence local whether wetested behaviour, settlement site breeding in Since the sexes differ probability. whichmay canalter infectionextent to dispersal This article This protectedis by Allcopyright. rights reserved. positive but had less predictive power in these models (Maternal status: status: (Maternal these models in predictive less power had positive but remained status’ of individual infection parent effect The exposure. similar by generated and offspring parental between χ χ 2 2 1 1 =4.15, p=0.042, n=266), indicating that this association is at least partly partly is atleast association this that indicating n=266), p=0.042, =4.15, = 9.57, p=0.002, n=266). Thus, there may be a positive association association positive be a may there Thus, n=266). p=0.002, 9.57, =

was more strongly predicted by the number of infected parents when parents infected of number by the predicted strongly was more as a model term (instead of a dispersal interaction term), the number of of number the term), interaction adispersal of (instead term a model as P. circumflexum P. P. circumflexum P. circumflexum was positively predicted by how many of their parents howby many their was predicted parents positively of χ 2 1 = 4.01, p=0.045, n=309). n=309). p=0.045, = 4.01, infection status more strongly for males than males for strongly statusmore infection

P. circumflexum P. The likelihood that recruiting blue tits that recruiting The likelihood infection status over and above that that and above over status infection χ

2 1 =12.18, p<0.001, n=442 Fig. S3). S3). Fig. n=442 p<0.001, =12.18, local prevalence at their attheir prevalence local P. circumflexum P. χ 2 1 = 1.95, P.

Accepted Article ability of breeding site prevalence for site for breeding prevalence of ability predictive altered the sex that evidence wasno There also semivariograms. directional S1) (Fig. and both omnidirectional sites, across breeding probability considering in autocorrelation spatial for evidence wasno There p=0.858). χ (Dispersal*Sex: was sex-dependent distance of postnatal dispersal main effect This article This protectedis by Allcopyright. rights reserved. among males (Natal prevalence*Sex: prevalence*Sex: (Natal males among positive and slightly females among being negative slightly sexes, among the differed of prevalence site natal effect thereevidence that the was effects, some sex these in of probability a had higher site their natal from further had dispersed that that individuals for distance dispersal and postnatal prevalence natal site between significant interaction was et There no al. 2013). parasite this years across (Lachish spatial distribution of broad-scale the in similarity little showing population this from findings previous with same site the following year (Pearson’s (Pearson’s year following site the same and natal breedi across individuals’ prevalence local inestimated correlation was no 1). There (Table model the same in entered were both terms whenor analyses univariate in either sites, breeding natal or For nestbox, local even at same years: the across in itsspatial distribution showed little consistency parasite this is limited, dispersal even though because likely which is 0.066), to 0.145 2 relictum infection of P. location and Timing 1 P. relictum =0.38, p=0.540) or of a 3-way interaction (Natal prevalence*Dispersal*Sex: prevalence*Dispersal*Sex: (Natal interaction a 3-way of or p=0.540) =0.38, P. relictum P. relictum infection (Table 2, Fig. 2b). In analys 2b).In 2, Fig. (Table infection (Table 2), but a main effect of dispersal distance was found, indicating indicating wasfound, of dispersal effect distance 2),but a main (Table , recruit infection status was not predicted by local prevalence at either prevalence bylocal wasnotpredicted infection status , recruit P. relictum prevalence in at the did prevalence one year prevalence not predict ng territories for this parasite ( parasite this for ng territories χ 2 r 1 P. relictum =-0.07, F =-0.07, =4.54, p=0.033), but no evidence that the that evidence no but p=0.033), =4.54,

1,155 es considering the potential role of role potential the es considering (Sex*Breeding site prevalence prevalence site (Sex*Breeding =0.73, p=0.395). This is inline =0.73, p=0.395). P. relictum P. r =-0.040, 95% CI: - CI: 95% =-0.040, infection infection χ 2 1 =0.03, Accepted Article interaction: interaction: This article This protectedis by Allcopyright. rights reserved.

χ was notsignificant ( distance and dispersal parents infected of number for found were status infection andoffspring parental between No associations significant S1). parasite (Table of this prevalence natal or breeding local either by predicted was not parasitaemia 2 relictum Discussion Discussion vectors. exposure to infective affects howby this driven presumably dispersal, of and extent parasites isthepattern with infection these of determinant an important suggest that Ourresults hosts. also ontheir selection with, and impose may interact parasites two sympatric two for markedly differ to seems life-history host’s the during occurs infection occurs in awild Most we blue population. that significantly, tit the pointshow at which likely most parasites avianby malaria infection at which location and stage life-history the we examined movements, dispersal their birds and on wild data Using longitudinal status and offspring parasitaemia were found were ( parasitaemia found and offspring status maternal infection noassociations between separately, species were considered ( parasitaemia offspring pooled for status infection Maternal 1 =0.01, p=0.903, n=266). n=266). p=0.903, =0.01,

χ 2 P. relictum Plasmodium 1 =2.83, p=0.092, n=54). n=54). p=0.092, =2.83,

χ species, leading to contrasting predictions about how these these how about predictions contrasting to leading species, 2 1 χ =0.22, p=0.643, n=442). with n=442). p=0.643, As =0.22, 2 1 =2.36, p=0.124, n=109). Similarly, when the two n=109). Similarly, parasite p=0.124, =2.36, P. relictumP. (Table 3), and the interaction between the between andthe interaction (Table 3), Plasmodium P. circumflexum P.

showed no association with noassociation showed P. circumflexum, P. relictum P. circumflexum, P. ; χ 2 1 =1.01, p=0.315, p=0.315, =1.01, P. relictumP. P.

Accepted Article This article This protectedis by Allcopyright. rights reserved. obtain. Thus, although predicting the transmission period from vector ecology from period the transmission predicting although obtain. Thus, can isto oftenand lacking be wilddifficult systems, malaria for parameters, avian vector ecological on crucial these therefore and transmission, for responsible aboutthe mosquitoes likelywill Knowledge vary. also timing transmission use, their malaria remain uncertain. Spatial variation in in variation Spatial uncertain. remain malaria transmitting for responsible the species but 2012), (Alves, woodland in the present is mosquitoes of assemblage diverse a here, studied population tit blue In the so. do to information insufficient is often there practice in in theory, possible is parameters al. (Beaudoin autumn and spring between time some place takes transmission suggest mosquitoes and birds European in prevalence malaria avian of dynamics seasonal the Dataon the of vectors ecology onresponsible. will the depend specific and critically isnot well transmission avian understood, of thetiming malaria regions, In temperate infection of malaria location and Timing divergent transmissionbiology for two sympatric Thissuggested transmission. of and timing location likely the infer to infection and movements onhost data longitudinal using approach, analternative adopted with associate species mosquito species, mosquito no of one withhowever theabundance particular association as Moreover, vector competence. biting and habits, lifespan, dispersal, dynamics, their seasonal vectors, of distribution spatial will on the and timing location Transmission depend territories. breeding on dispersal, andsettlement of fledging, phase, periods theincluding nestling stages, life-history host several different encompasses this passerines, non-migratory , 1971; Cosgrove 1971; , et al. et , 2008; Ferraguti et al. 2013; Inci et al. 2012). However, for Inciet for al. However, 2013; et al.2012). , 2008;Ferraguti Plasmodium P. relictum P. circumflexumP. prevalence (Alves, 2012). Hence, we Hence, 2012). (Alves, prevalence species vary species the vector in they species Plasmodium

species. prevalence shows some et et Accepted Article This article This protectedis by Allcopyright. rights reserved. results strongly suggest infectionwith suggest strongly results (Fig.2a).These 2km exceeded dispersal postnatal once power nopredictive had but tobreed, settling before distances short that dispersed recruits among infection predicted natal site prevalence distance: dispersal postnatal on was highly contingent this predict infection, positively sites did at natal whileprevalence and sites, breeding P. circumflexum in the same study site (Sepil et al. 2013) suggest the possibility of genetic effects on effects genetic of possibility the suggest 2013) al. et (Sepil site study same in the tits ingreat infection and malaria MHCsupertypes between of associations analyses recent Indeed, 1997). et al. (Boulinier systems bird-ectoparasite in been found as has present, isalso similarity in susceptibility genetic Thismay that indicate for. controlled circumflexum offspring variation when in significant remained association this However, positive dispersing. by parents their of fate the escape potentially can offspring and that status, parents and between canin drive offspring theirinfection similarity environment that ashared 2a).Thissuggests distance (Fig. dispersal postnatal increasing with declined association this positive but were infected, parents their of many how circumflexum P. during territory eventual their to close time more spend or earlier, territories breeding at arrive males that indicate could females than males for strongly more infection predicted prevalence site breeding that The finding 2012). (Alves, fledging after July (Cosgrove the inability to detect circumflexum in peak an autumn of observation the including population, this from findings previous with agreement is in This territories. breeding their to, near least at are or on, etal. exposure (local prevalence at their breeding site) was statistically was statistically site) their breeding at prevalence (local exposure (Cosgrove transmission to novel reflect thought prevalence transmission. Offspring infection status was positively predicted by predicted positively was status infection Offspring transmission. , 2006), and data showing total mosquito abundance peaks mid- in abundance mosquito total showing anddata , 2006), infection was strongly predicted by local prevalence at recruits’ at recruits’ by prevalence local predicted was strongly infection Plasmodium infection in blood samples from 14-day old nestlings old nestlings 14-day from samples blood in infection P. circumflexum P.

occurs after birds have settled have settled birds occurs after et al. et , 2008), P. P. P. Accepted Article This article This protectedis by Allcopyright. rights reserved. pass through a patch where a patch pass through itis likely to the more disperses, an individual further - the distance dispersal of effect positive also the but infection status, predicts prevalence local site breeding nor natal neither why both explain could this infection, acquiring landscape the move throughout hosts If dispersal. postnatal during partly at least occur thisspecies of may transmission move’ andFirst,undermove’ move’‘vectors scenario,hypotheses. the ‘hosts ‘hosts the weterm which spatial predictability, of lack thisparasite’s for hypotheses exclusive non-mutually two propose We distance. dispersal postnatal with increased probability infection Instead, sites. breeding natal or either at local prevalence to In contrast relictum identified morphologically for range host mosquito known the Indeed, ecologies. different with species mosquito of range broader a of infection or season, biting a longer with species vector asingle of use arise through could period transmission that previous finding defined transmission period for defined transmission more not. A or infected itgets whereone time isat onwhether bird of any a influence the reduce period and longer transmission a to thiscould lead in of mosquitos Wytham, If 2012). al. et Santiago-Alarcon species; for than time-period longer a over occur may parasite seen for as season transmission well-defined a of suggestive prevalence in peak autumn strong et Loiseau et 2012). al. 2006, al. 2011, Westerdahl et al. (Bonneaud birds passerine other for found ashasbeen tits, infection in malaria from lab studies is three times higher than for for than higher isthree times lab studies from P. circumflexum P. P. circumflexum P. relictum P. (Cosgrove et al. 2008), also indicates that infection with this infection that 2008), al. indicates also et (Cosgrove P. relictum , P. relictum prevalence shows little seasonal variation, and no and variation, seasonal little shows prevalence P. circumflexum P. is being transmitted and acquire infection. Our Our acquire infection. and transmitted is being P. relictum infection probability wasby infection probability not predicted than than

is transmittedby a broader range P. relictum P. circumflexum P. P. circumflexum would also also be would . A longer longer . A (24 (24 vs. 8 P. Accepted Article predicted from another difference in their seasonal dynamics. While dynamics. While seasonal intheir difference another predicted from This article This protectedis by Allcopyright. rights reserved. affect the likelihood that dispersal could function as parasite avoidance mechanism mechanism avoidance parasite as function could dispersal that likelihood the affect will it example, For evolve. may hosts adaptations anti-parasite of type the determining in role plays akey occurs infection which host’s at life-history the of thestage First, species. these two for differ will processes coevolutionary host-parasite several suggest itispossible that hypothesis, move’ ‘vectors alternative an Under 2013). etal. (Hellgren transmission with persistent those than season, transmission defined well-awith species for more be expected would possible, and thus is transmission when responses) to exposed host immune more (and theblood are parasites in only is 2008). The thought beto phenomenon relapse aensuring adaptation parasite blood-stage population, inthis relapse’ a ‘spring and shows winter blood in inthe undetectable hypothesis cannot explain a positive effect of host dispersal distance on infection oninfection distance of host dispersal positiveeffect explaina hypothesis cannot This ‘vectors move’ here.. performed able we would itwith not the analyses be to detect exposure risk for case, a of it would provides assumption violatethat our prevalence local measure initial thiswere the infection. If of transmission and acquisition between distances move long The ecological differences between between differences The ecological Hanski (de Laet, securing a1985; breeding territory to susceptible more are lowquality example individuals if this,for drive could factors other However, probability. Evolutionary implications of species-specific transmission ecology ecology transmission of species-specific implications Evolutionary P. relictumP. P. relictum. P. infections are detectable throughout the year (Cosgrove et al. al. et year (Cosgrove the throughout detectable are infections P. relictum Thus, even if infection occurred at natal or breeding sites, sites, breeding natal or at occurred infection if even Thus, infection, and also have to disperse further before before further todisperse have and also infection, P. circumflexum P.

et al., 1991). 1991). al., et and and P. relictum P. relictum P. circumflexum P. found here here found vectors is is Accepted Article pattern in areas of low prevalence (Fig. 2a), optimal postnatal dispersal for avoidance of avoidance for dispersal postnatal optimal 2a), (Fig. prevalence low of in areas pattern reverse and the prevalence high of areas in sex) philopatric the least females, of of avoidance strategy dispersal for a facultative favour could selection that possible iswhile it here, studied population the example, in For infection probability. affects dispersal postnatal how determine events, dispersal host to relation in transmission of and timing distribution spatial parasite’s a that showing this, demonstrate clearly malaria avian on findings Our 2001). al.et Boulinier 1996; Lemel (Boulinier and probability infection can influence dispersal parasitism willhow of critically influence patterns spatiotemporal that been recognised also has However, it parasitism. toavoid hosts allowing location, initial atthe parasitism withincreasing distance should increase dispersal prediction common is that A 2007). al. et effects (Tschirren by maternal controlled and adaptive be this may suggested and have ordistance, dispersal host emigration etal.1999) (Heeb or decreased 1992) and Brown (Brown increased either with associated be may parasitism of levels high shown that systems have bird-ectoparasite of Several studies 2001). etal. (Boulinier This article This protectedis by Allcopyright. rights reserved. still. further dispersal optimal about predictions complicates relative virulence their of consideration in occur patterns the area, with same parasites different spatiotemporal multiple where that illustrates also Thissystem mechanism. avoidance a as disease to function dispersal potential for the theseinfluences parasites clearly of two ecology transmission contrasting the Overall, infection risk. may minimize dispersal minimal distance, P. relictum local adaptation. Several studies have examined the evidence for local adaptation in adaptation localevidence for the examined have studies Several local adaptation. host-parasite for the potential will affect also biology transmission Species-specific is much less obvious. Since infection probability increases with dispersal dispersal with increases probability infection Since obvious. less ismuch P. circumflexum P.

, with high dispersal (or production production (or dispersal high with , Accepted Article This article This protectedis by Allcopyright. rights reserved. on breeding performance in blue et al. performance tits thesedifferences on breeding (Knowles 2010). Whether of effect an finding also work with experimental al. 2011), et (Lachish breed P. circumflexum P. with ways, different in hostfitness affect species two these suggested this population on study capture-mark-recapture arecent Interestingly, et al.2011). (Best resistance host greater for alsopredicted to select are interactions global, host-parasite relictum as such ability dispersal high a with one than lower virulence have to predicted shorter) host movements to transport totransport movements host shorter) (much subsequent for potential limited is there dispersal), event(postnatal dispersal circumflexum a high riskof pose repeatedly the nestboxes same In is unknown. Wytham, ecology spatiotemporal parasites’ it, asthe expect should one clear always not itis yet at a avian haemosporidia genetic et al. (Bonneaud level Loiseau 2006, et al. 2011), dispersal potential and a repeatable spatial distribution like distribution spatial and a repeatable potential dispersal with low parasite A virulence. their in differences may to lead parasites two these of ecology spatiotemporal contrasting the suggests theory evolutionary Finally, theyduringdispersal. postnatal if canbecome infected exposure, in spatial variation any may disrupt whichhost for movements and distribution, spatial for localadaptation expect not would one in P variation spatial ( tit great Wytham the in structure genetic for possible seems adaptation local within-population Thus, prevalence. in variation spatial driven (Kerr et al. 2006, Boots and Mealor 2007, Wild et al. 2009). Local, rather than than Local, rather 2009). et al. 2007, Mealor and Wild 2006, al. et Boots (Kerr P. circumflexum P. infection and since we show that infection occurs after the major major the after occurs infection that show we since and infection reducing survival whereas survival reducing . circumflexum . Indeed, recent work has found that fine-scale spatial spatial fine-scale that found has work recent Indeed, . infection risk infection et(Garroway In 2013). contrast, al P. circumflexum P. Parus major P. relictum P. relictum,

and break up this environment- up this break and ) population is associated with associated is ) population may reduce thepropensity to which shows no consistent no consistent which shows P. circumflexum P. P. relictum is is P. P. P.

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Cyanistes caeruleus Cyanistes Parus major major Journal of Journal . Journal Journal

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Accepted Article Naef Daenzer, L., Naef Naef Daenzer, L., & Daenzer, B. Nager, Naef R. G.(2000) and foraging Prey selection Mitchell, S. E., & Read, A. F. (2005) Poor maternal environment enhances offspring offspring enhances environment maternal (2005) Poor F. A. &Read, E., Mitchell, S. Minot, E. O., & Perrins, C. M. (1986) Interspecific interference competition: nest sites nest competition: interference Interspecific C.M. (1986) Perrins, O., & E. Minot, Matthysen E., Van de Casteele, T. , & Adriaensen, F. (2005) Do sibling tits ( tits sibling Do (2005) F. Adriaensen, & , T. Casteele, de Van E., Matthysen This article This protectedis by Allcopyright. rights reserved. Marzal, A., Ricklefs, Ricklefs, Marzal, A., R. Valki E., (2005) N. T. & Marsh, K. Williams, Snow, R. W., M. Mwangi, T. J., W., Mackinnon, (2011) G. Sorci, Julliard,& O. R. Chastel, A., Robert, R., Zoorob, C., Loiseau, L. (2010) The A. Graham, & T Day, N., M., Colegrave, D. Shuker, J., T. Little, performance of breeding greattits performance 2601–2607. disease resistance in an invertebrate. resistancein disease an invertebrate. for blue and great tits. tits. great blueand for Oecologia major gain of malaria parasites in a globally invasive bird. invasive ina globally parasites malaria gain of Szöll A. P., Palinauskas, V., Pap, P. L., Perez-Tris, Sehgal,J., M., R. N. Soler,M., A., Lima, M. Krizanauskiene, Møller,R., deMartin, L. B., Magnussen, E., Lope, F., Czirják, G. A., Ewen, J., Hellgren, O., Ho Hellgren, O., J., Ewen, A., G. Czirják, Africa. in malaria of Heritability domesticus Plasmodium relictum perspective. in tolerance virulence: of coevolution and Evolution Ecology diagnostic tests. imperfect from prevalence wildlife disease estimating ő , si, E., Westerdahl, H., Zetindjiev, P. & Bensch, S. (2011) Diversity, loss, and loss, Diversity, (2011) S. Bensch, & P. Zetindjiev, H., E., Westerdahl, si, P. caeruleus P. 143, 301–307. 301–307. 143, ). Proceedings of the Royal Society oftheB Society Royal Proceedings ) disperse over similar distances and in similar directions? directions? insimilar and distances similar over disperse ) infection and MHC diversity in the house sparrow and MHCdiversity thehousesparrow ( in infection 3, 339-348. 3,339-348. Journal of Animal Ecology Ecology ofAnimal Journal ū nas, G., Albayrak, T., Arriero, E., Bonneaud, C., C., Bonneaud, E., Arriero, T., Albayrak, nas, G., PLoS Medicine PLoS Parus major

Proceedings of the Royal Society B Society Royal ofthe Proceedings ř áková, D., Iezhova, T. A., Jensen, H., H., Jensen, A., T. Iezhova, D., áková, 2, e340 2,e340

in relation to food availability. food availability. to relation in 278, 1264–1272. 278,1264–1272. 55, 331–350. 55, 331–350. PLoS Pathogens PLoS PLoS One PLoS 6,e21905. 6, e1001006. Methods in Methods in Parus Passer 272, Accepted Article Sepil I., Lachish, S., Hinks, A. E., & Sheldon, B. C. (2013) C. B. Sheldon, & E., Hinks, A. S., Lachish, Sepil I., Sehgal, R. N. M., Buermann, W., Harrigan, R. J., Bonneaud, C., Loiseau, C., Chasar, Chasar, C., Loiseau, C., Bonneaud, J., R. Harrigan, M.,Buermann, W., R.N. Sehgal, avian of vectors Dipteran H.M. (2012) Schaefer, G., Valkiunas, D., Santiago-Alarcon, Sadd, B. M., & Schmid-Hempel, P. (2009) A distinct infection cost associated with associated cost distinct infection A (2009) P. Schmid-Hempel, M., & B. Sadd, This article This protectedis by Allcopyright. rights reserved. Stauss, M. J., Burkhardt, J. F. & Tomiuk, J. (2005) Foraging flight distances as aas distances flight J. (2005) Foraging Tomiuk, & J. F. Burkhardt, M. J., Stauss, host and R., relationships, Ricklefs, Fallon, (2004)cospeciation, & S. Evolutionary forstatistical environment language and R:A 2011. Team, Core R Development Palinauskas, Kosarev, V., Shapoval, V., Bensch, A., ValkiS. & qualitative and quantitative resistance to avian malaria infections in a wilda in infections malaria toavian resistance quantitative and qualitative Proceedings of the Royal Society B Society Royal ofthe Proceedings a in bloodparasites of predictions explicit Valki Sepil, I., A., Biological Reviews taxonomy. their and cycles life parasite untangling parasites: Haemosporidian Letters bumble-bees. in immunity antibacterial of priming trans-generational switching in avian malaria parasites. parasites. malaria in avian switching URL http://www.R-project.org/. 900051-07-0, 3- ISBN Austria. Vienna, Statistical Computing, for RFoundation computing. Plasmodiidae). (Haemosporida: and Giovannolaia the of subgenera parasites Haemamoeba avian malaria two of and morphospecies blineages cytochrome mitochondrial of Comparison Biology of Avian Journal doi:10.1098/rspb.2013.0134 doi:10.1098/rspb.2013.0134 population 5, 798–801. 5,798–801. . Proceedings of the Royal Society B of theRoyalSociety Proceedings . ū nas, G., Iezhova, T., Saatchi, S. & Smith, T. B. (2011) Spatially (2011) Spatially B. T. Smith, & S. Saatchi, T., Iezhova, G., nas, 87, 928-964. 928-964. 87, 31, 206–214. 206–214. 31, Zootaxa 278, 1025–1033. 1025–1033. 278, Systematic Biology Systematic 1626, 39–50. 39–50. 1626, widely distributed African rainforest bird. rainforest African widely distributed

280, 20130134. 20130134. Mhc 53, 111-119. 111-119. 53, supertypes confer both ū nas, G. (2007) G. nas, Biology

Accepted Article Wood, M. J., Cosgrove, C. L., Wilkin, T. A., Knowles, S. C. L., Day, K. P. & Sheldon, B. Sheldon, B. P. & K. Day, C.L., Knowles, S. A., T. L., C. Wilkin, Cosgrove, M.J., Wood, host-parasite in alter selection can C.(2009)King, Environment K. & J., Wolinska, parasite of evolution the and (2009) Adaptation A. S. & West, A. G.,Gardner, Wild, Wilkin, T. A., Perrins, C. M. & Sheldon, B. C. (2007) The use of GIS in estimating inestimating GIS of use The C.(2007) B. Sheldon, M. Perrins, C. & A., T. Wilkin, onlife- effects Density C.(2006) B. Sheldon, & G. A. Gosler, Garant, D., A., T. Wilkin, disease Quantitative (2012) S. Bensch,& D. M.,Hasselquist, Asghar, H., Westerdahl, nested new A (2004) Ö. Östman, & Hasselquist,D. S., Bensch, J., Waldenström, Valki This article This protectedis by Allcopyright. rights reserved. Tschirren, B., Fitze, P. S. & Richner, H. (2007) Maternal modulation of natal dispersal in natal in dispersal of modulation Maternal Richner,& H.(2007) S. Fitze, P. B., Tschirren, ū C. (2007) Within-population variation in prevalence and lineage distribution of of in distribution and lineage variation prevalence C. (2007) Within-population interactions. world. aconnected in virulence histocompatibility complex. on selection major parasite-mediated to better understand resistance: Haemoproteus detecting in efficient very method reaction chain polymerase CRC Press. major lay of study acase quality: in habitat spatial variation techniques. with GIS data tit the great of population awild in traits history Naturalist with parasitism? cope to strategy anadaptive bird: a passerine conditions. tits inblue effort parental of measure nas, G. 2005. Avian malaria parasites and other haemosporidia. Boca Raton, Raton, Boca haemosporidia. other and parasites 2005. Avian malaria G. nas, . Ibis 169, 87–93. 169, 87–93. 149, 110–118. Journal of Avian Biology of Journal Trends in Parasitology Parasitology in Trends infections from avian blood. blood. avian from infections Journal of Ecology of Animal Journal Proceedings of the Royal Society B Royal Society ofthe Proceedings Nature 36, 47–56. 36, 47–56. 25, 236–244. 25, 236–244. Parus caeruleus 459, 983–986. 983–986. 459, Parasitology

Parus major 75, 604–615. 75,604–615. ‐ date date in thegreat tit differ with environmental 90,191-194. 90,191-194. : analyses of long-term long-term of analyses : Plasmodium 279, 577–584. 577–584. 279, The American American The Parus and Accepted Article This article This protectedis by Allcopyright. rights reserved.

bold. in shown are (p<0.05) effects Significant n=265 broods. recruits from 342 andincluded as afactor, year natal for controlled analyses All recruits. blue tit breeding among status infection Table 1: legends figure and Tables Information.doc”. for this is available “Supporting article Information online: Supporting The following Information Supporting Breeding site only 1 1 1 site) natal for (controlling site Breeding only site Breeding site) breeding for (controlling Natal site Natal site only Local prevalence measure measure prevalence Local avian malaria in blue tits, in avian blue malaria tits, Relative ability of prevalence on natal and breeding territories to explain to explain territories and breeding on natal prevalence of ability Relative df df 1 1 2.59 0.1075 Cyanistes caeruleus 21.65 <0.0001 33.70 <0.0001 14.64 0.0001 χ 2 p P. circumflexum .

Molecular Ecology Molecular Parameter Parameter estimate (0.813) (0.813) (0.754) (0.813) (0.735) (SE) 1.33 3.67 3.67 4.18 2.79

0.11 0.7361 0.09 0.7610 0.05 0.8260 0.03 0.8689 χ 2 p 16, 3263–3273. P. relictum Parameter Parameter estimate (1.013) (1.013) (0.998) (1.132) (1.132) (1.11) (1.11) -0.25 -0.18 (SE) 0.34 0.30

Accepted Article aa rvlne - 03 0.5582 0.34 - - - - 4 1 1 1 Natal prevalence*Dispersal distance distance Dispersal Natal prevalence year Natal df Predictor This article This protectedis by Allcopyright. rights reserved. and recruit as effect, for control age andnatal year. a include brood random analyses All attempt. breeding monitored first isintheir status offspring and born, was offspring year the the isfrom status infection Parental tits. blue breeding among 3: Table 342 broods. from recruits 442 include analyses Both the model. left factor point that the at arereported terms removed for statistics the Terms model in are inbold, minimal while shown probability. malaria infection 2: Table N parents infected infected N parents status Paternal Maternal status Parental variable Df Df variable Parental The relationship between parental and offspring malaria infection status malaria infection offspring and parental between relationship The The effect of The effect natal prevalence and postnatal dispersalterritory distance on

1 1 1 266 266 309 0.092 2.84 305 n 11.59 0.001 0.001 11.59 7.14 0.008 0.008 7.14 χ .crufeu P. relictum P. circumflexum 2 p 8.93 0.0628 0.0628 <0.0001 8.93 29.87 6.52 0.0107 0.0107 6.52 χ P. circumflexum 2 p Parameter Parameter

estimate (0.268) (0.268) (0.337) (0.393) (0.393) (SE) 0.92 0.92 0.69 0.69

266 0.390.533 309 0.000.987 305 1.510.220 n 6.18 0.0129 1.26 0.2614 χ 2 p χ P. relictum relictum P. 2 p Parameter Parameter estimate estimate (0.271) (0.271) (0.417) (0.366) (0.366) -0.17 -0.01 -0.44 (SE)

Accepted Article prevalence). (high tored prevalence) blue(low from increasing dataset), in the recruits all (excluding year that adults in breeding from derived prevalence interpolated the shows colours andheat polygons, by Thiessen indicated are territories nestboxes, dotsrepresent figure, the In assessed. also was site prevalence whether it altered natalpredictive and on infectiondistance thepower probability, of dispersal postnatal of effect The occurs. infection stage life-history which at assess to wasused status infection recruit topredict two measures these of ability relative The (B). attempt breeding first their during territory breeding ontheir prevalence interpolated (A), phase and nestling during their on territory natal their prevalence interpolated the were derived: risk localinfection of proxies two each recruit, For species. parasite malaria avian sympatric two for occurs likely most infection 1: Fig.

This article This protectedis by Allcopyright. rights reserved. Illustration of the analytical approach used to examine where and when andwhere used toexamine approach theanalytical of Illustration Photo credit for adult blue tit: JoeTobias tit: adult blue for credit Photo

Accepted Article

This article This protectedis by Allcopyright. rights reserved. P. relictumP. circumflexum P. was Thisfor distance. interaction significant andpostnatal dispersal the natal territory on prevalence local between term interaction the aGLMMincluding from estimates parameter using weregenerated surfaces Heat probability). red (high to probability) blue(low infection from of probability the Colourindicates tit recruits blue breeding A) for probability of infection Fig. 2: The effect of natal territory prevalence and postnatal dispersal distance on distance dispersal and postnatal effect of natal prevalence The territory (see Table 3). 3). Table (see , whereas only a main effect of dispersal distance was supported for for was supported distance dispersal of effect amain only whereas , Plasmodium circumflexum

and B) and B) P. relictumP. , among , among

Accepted Article

This article This protectedis by Allcopyright. rights reserved. postnatal dispersal distance. distance. dispersal postnatal and parentsinfected of the number between term interaction the including GLMM a from values predicted using generated were Heat surfaces probability). (high red to probability) (low blue infection from of probability the indicates Colour recruits. tit A) for probability Fig. 3: The effect of parental infection and postnatal dispersal distance on infection oninfection of distance dispersal and postnatal of parental infection effect The Plasmodium circumflexum Plasmodium and B)

P. relictum , among breeding blue blue breeding among ,