The spatial spread of infectious disease is determined by spatial and social processes such as animal space use and family group structure. Yet, the impacts of social processes on spatial spread remain poorly understood and estimates of spatial transmission kernels (STKs) often exclude social structure. Understanding the impacts of social structure on STKs is important for obtaining robust inferences for policy decisions and optimizing response plans. We fit spatially explicit transmission models with different assumptions about contact structure to African swine fever virus surveillance data from eastern Poland from 2014 to 2015 and evaluated how social structure affected inference of STKs and spatial spread. The model with social structure provided better inference of spatial spread, predicted that approximately 80% of transmission events occurred within family groups, and that transmission was weakly female-biased (other models predicted weakly male-biased transmission). In all models, most transmission events were within 1.5 km, with some rare events at longer distances. Effective reproductive numbers were between 1.1 and 2.5 (maximum values between 4 and 8). Social structure can modify spatial transmission dynamics. Accounting for this additional contact heterogeneity in spatial transmission models could provide more robust inferences of STKs for policy decisions, identify best control targets and improve transparency in model uncertainty.

Department of Game Management and Wildlife Biology Faculty of Forestry and Wood Sciences Czech University of Life Sciences Kamýcká 129 165 00 Praha 6 Czech Republic

Mammal Research Institute Polish Academy of Sciences Stoczek 1 17 230 Białowieża Poland

National Wildlife Research Center USDA APHIS Wildlife Services 4101 Laporte Avenue Fort Collins CO 80526 USA

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Sah P, Mann J, Bansal S, Farine D. 2018. Disease implications of animal social network structure: a synthesis across social systems. J. Anim. Ecol. 87, 546–558. (10.1111/1365-2656.12786) PubMed DOI

Riley S 2007. Large-scale spatial-transmission models of infectious disease. Science 316, 1298–1301. (10.1126/science.1134695) PubMed DOI

Dougherty ER, Seidel DP, Carlson CJ, Spiegel O, Getz WM, Lafferty K. 2018. Going through the motions: incorporating movement analyses into disease research. Ecol. Lett. 21, 588–604. (10.1111/ele.12917) PubMed DOI

Emch M, Root ED, Giebultowicz S, Ali M, Perez-Heydrich C, Yunus M. et al. 2012. Integration of spatial and social network analysis in disease transmission studies. Ann. Assoc. Am. Geogr. 102, 1004–1015. (10.1080/00045608.2012.671129) PubMed DOI PMC

Arthur RF, Gurley ES, Salje H, Bloomfield LSP, Jones JH. 2017. Contact structure, mobility, environmental impact and behaviour: the importance of social forces to infectious disease dynamics and disease ecology. Phil. Trans. R. Soc. B 372, 20160454 (10.1098/rstb.2016.0454) PubMed DOI PMC

Woodroffe R, et al. 2009. Social group size affects Mycobacterium bovis infection in European badgers (Meles meles). J. Anim. Ecol. 78, 818–827. (10.1111/j.1365-2656.2009.01545.x) PubMed DOI

McClure KM, Gilbert AT, Chipman RB, Rees EE, Pepin KM, Hoye B. 2020. Variation in host home range size decreases rabies vaccination effectiveness by increasing the spatial spread of rabies virus. J. Anim. Ecol. 89, 1375–1386. (10.1111/1365-2656.13176) PubMed DOI PMC

Habib TJ, Merrill EH, Pybus MJ, Coltman DW. 2011. Modelling landscape effects on density–contact rate relationships of deer in eastern Alberta: implications for chronic wasting disease. Ecol. Modell. 222, 2722–2732. (10.1016/j.ecolmodel.2011.05.007) DOI

Nunn CL, Jordán F, McCabe CM, Verdolin JL, Fewell JH. 2015. Infectious disease and group size: more than just a numbers game. Phil. Trans. R. Soc. B 370, 20140111 (10.1098/rstb.2014.0111) PubMed DOI PMC

Daviews C, Ayres JM, Dye C, Deane LM. 1991. Malaria infection rate of Amazonian primates increases with body weight and group size. Funct. Ecol. 5, 655–662. (10.2307/2389485) DOI

Ezenwa VO 2004. Host social behavior and parasitic infection: a multifactorial approach. Behav. Ecol. 15, 446–454. (10.1093/beheco/arh028) DOI

Rosengaus RB, Maxmen AB, Coates LE, Traniello JFA. 1998. Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav. Ecol. Sociobiol. 44, 125–134. (10.1007/s002650050523) DOI

Benincà E, Hagenaars T, Boender GJ, van de Kassteele J, van Boven M, Ferrari M. 2020. Trade-off between local transmission and long-range dispersal drives infectious disease outbreak size in spatially structured populations. PLoS Comput. Biol. 16, e1008009 (10.1371/journal.pcbi.1008009) PubMed DOI PMC

Boender GJ, Hagenaars TJ, Bouma A, Nodelijk G, Elbers ARW, de Jong MCM, van Boven M. 2007. Risk maps for the spread of highly pathogenic avian influenza in poultry. PLoS Comput. Biol. 3, e71 (10.1371/journal.pcbi.0030071) PubMed DOI PMC

Boender GJ, van Roermund HJW, de Jong MCM, Hagenaars TJ. 2010. Transmission risks and control of foot-and-mouth disease in The Netherlands: spatial patterns. Epidemics 2, 36–47. (10.1016/j.epidem.2010.03.001) PubMed DOI

Gubbins S, Stegeman A, Klement E, Pite L, Broglia A, Abrahantes JC. 2020. Inferences about the transmission of lumpy skin disease virus between herds from outbreaks in Albania in 2016. Prev. Vet. Med. 181, 104602 (10.1016/j.prevetmed.2018.12.008) PubMed DOI PMC

Craft ME 2015. Infectious disease transmission and contact networks in wildlife and livestock. Phil. Trans. R. Soc. B 370, 20140107 (10.1098/rstb.2014.0107) PubMed DOI PMC

Salje H, Cummings DA, Lessler J. 2016. Estimating infectious disease transmission distances using the overall distribution of cases. Epidemics 17, 10–18. (10.1016/j.epidem.2016.10.001) PubMed DOI PMC

Ferguson NM, Donnelly CA, Anderson RM. 2001. The foot-and-mouth epidemic in Great Britain: pattern of spread and impact of interventions. Science 292, 1155–1160. (10.1126/science.1061020) PubMed DOI

Ferguson NM, Donnelly CA, Anderson RM. 2001. Transmission intensity and impact of control policies on the foot and mouth epidemic in Great Britain. Nature 413, 542–548. (10.1038/35097116) PubMed DOI

Keeling MJ, et al. 2001. Dynamics of the 2001 UK foot and mouth epidemic: stochastic dispersal in a heterogeneous landscape. Science 294, 813–817. (10.1126/science.1065973) PubMed DOI

Woolhouse M 2011. How to make predictions about future infectious disease risks. Phil. Trans. R. Soc. B 366, 2045–2054. (10.1098/rstb.2010.0387) PubMed DOI PMC

Rees EE, Pond BA, Tinline RR, Bélanger D, McCallum H. 2013. Modelling the effect of landscape heterogeneity on the efficacy of vaccination for wildlife infectious disease control. J. Appl. Ecol. 50, 881–891. (10.1111/1365-2664.12101) DOI

Shirley MDF, Rushton SP, Smith GC, South AB, Lurz PWW. 2003. Investigating the spatial dynamics of bovine tuberculosis in badger populations: evaluating an individual-based simulation model. Ecol. Modell. 167, 139–157. (10.1016/S0304-3800(03)00167-4) DOI

Willem L, Verelst F, Bilcke J, Hens N, Beutels P. 2017. Lessons from a decade of individual-based models for infectious disease transmission: a systematic review (2006–2015). BMC Infect. Dis. 17, 612 (10.1186/s12879-017-2699-8) PubMed DOI PMC

Pepin KM, Golnar AJ, Abdo Z, Podgórski T. 2020. Ecological drivers of African swine fever virus persistence in wild boar populations: insight for control. Ecol. Evol. 10, 2846–2859. (10.1002/ece3.6100) PubMed DOI PMC

Pepin KM, VerCauteren KC. 2016. Disease-emergence dynamics and control in a socially-structured wildlife species. Sci. Rep. 6, 25150 (10.1038/srep25150) PubMed DOI PMC

Pepin KM, et al. 2016. Contact heterogeneities in feral swine: implications for disease management and future research. Ecosphere 7, e01230 (10.1002/ecs2.1230) DOI

Podgórski T, Apollonio M, Keuling O. 2018. Contact rates in wild boar populations: implications for disease transmission. J. Wildl. Manage. 82, 1210–1218. (10.1002/jwmg.21480) DOI

Arias M, Jurado C, Gallardo C, Fernández-Pinero J, Sánchez-Vizcaíno JM. 2018. Gaps in African swine fever: analysis and priorities. Transbound. Emerg. Dis. 65, 235–247. (10.1111/tbed.12695) PubMed DOI

Pepin KM, Davis AJ, Streicker DG, Fischer JW, VerCauteren KC, Gilbert AT, Recuenco S. 2017. Predicting spatial spread of rabies in skunk populations using surveillance data reported by the public. PLoS Negl. Trop. Dis. 11, e0005822 (10.1371/journal.pntd.0005822) PubMed DOI PMC

Chipperfield JD, Holland EP, Dytham C, Thomas CD, Hovestadt T. 2011. On the approximation of continuous dispersal kernels in discrete-space models. Methods Ecol. Evol. 2, 668–681. (10.1111/j.2041-210X.2011.00117.x) DOI

Ypma RJF, Bataille AMA, Stegeman A, Koch G, Wallinga J, van Ballegooijen WM. 2012. Unravelling transmission trees of infectious diseases by combining genetic and epidemiological data. Proc. R. Soc. B 279, 444–450. (10.1098/rspb.2011.0913) PubMed DOI PMC

Kamath PL, et al. 2016. Genomics reveals historic and contemporary transmission dynamics of a bacterial disease among wildlife and livestock. Nat. Commun. 7, 11448 (10.1038/ncomms11448) PubMed DOI PMC

Price SJ, Garner TWJ, Cunningham AA, Langton TES, Nichols RA. 2016. Reconstructing the emergence of a lethal infectious disease of wildlife supports a key role for spread through translocations by humans. Proc. R. Soc. B 283, 20160952 (10.1098/rspb.2016.0952) PubMed DOI PMC

Frant M, Lyjak M, Bocian L, Barszcz A, Niemczuk K, Wozniakowski G. 2020. African swine fever virus (ASFV) in Poland: prevalence in a wild boar population (2017–2018). Vet. Med. 65, 143–158. (10.17221/105/2019-VETMED) DOI

Mazur-Panasiuk N, Woźniakowski G. 2019. The unique genetic variation within the O174 L gene of Polish strains of African swine fever virus facilitates tracking virus origin. Arch. Virol. 164, 1667–1672. (10.1007/s00705-019-04224-x) PubMed DOI PMC

Chapman DAG, Darby AC, Da Silva M, Upton C, Radford AD, Dixon LK. 2011. Genomic analysis of highly virulent Georgia 2007/1 isolate of African swine fever virus. Emerg. Infect. Dis. 17, 599–605. (10.3201/eid1704.101283) PubMed DOI PMC

European Food Safety Authority et al. 2020. Epidemiological analyses of African swine fever in the European Union (November 2018 to October 2019). EFSA J. 18, e05996. PubMed PMC

Guinat C, Gogin A, Blome S, Keil G, Pollin R, Pfeiffer DU, Dixon L. 2016. Transmission routes of African swine fever virus to domestic pigs: current knowledge and future research directions. Vet. Rec. 178, 262 (10.1136/vr.103593) PubMed DOI PMC

Śmietanka K, Woźniakowski G, Kozak E, Niemczuk K, Frączyk M, Bocian Ł, Kowalczyk A, Pejsak Z. 2016. African swine fever epidemic, Poland, 2014–2015. Emerg. Infect. Dis. 22, 1201–1207. (10.3201/eid2207.151708) PubMed DOI PMC

Woźniakowski G, Kozak E, Kowalczyk A, Łyjak M, Pomorska-Mól M, Niemczuk K, Pejsak Z. 2016. Current status of African swine fever virus in a population of wild boar in eastern Poland (2014–2015). Arch. Virol. 161, 189–195. (10.1007/s00705-015-2650-5) PubMed DOI PMC

Borowik T, Cornulier T, Jędrzejewska B. 2013. Environmental factors shaping ungulate abundances in Poland. Acta Theriol. 58, 403–413. (10.1007/s13364-013-0153-x) PubMed DOI PMC

Śmietanka K, Woźniakowski G, Kozak E, Niemczuk K, Frączyk M, Bocian L, Kowalczyk A, Pejsak Z. 2016. African swine fever epidemic, Poland, 2014–2015. Emerg. Infect. Dis. 22, 1201–1207. (10.3201/eid2207.151708) PubMed DOI PMC

Rosell C, Navas F, Romero S. 2012. Reproduction of wild boar in a cropland and coastal wetland area: implications for management. Anim. Biodivers. Conserv. 35, 209–217. (10.32800/abc.2012.35.0209) DOI

Selva N, Jędrzejewska B, Jędrzejewski W, Wajrak A. 2005. Factors affecting carcass use by a guild of scavengers in European temperate woodland. Can. J. Zool. 83, 1590–1601. (10.1139/z05-158) DOI

Ježek M, Štípek K, Kušta T, Červený J, Vícha J. 2011. Reproductive and morphometric characteristics of wild boar (Sus scrofa) in the Czech Republic. J. Forest Sci. 57, 285–292. (10.17221/102/2010-JFS) DOI

Bieber C, Ruf T. 2005. Population dynamics in wild boar Sus scrofa: ecology, elasticity of growth rate and implications for the management of pulsed resource consumers. J. Appl. Ecol. 42, 1203–1213. (10.1111/j.1365-2664.2005.01094.x) DOI

Keeling MJ, Rohani P. 2008. Modeling infectious diseases in humans and animals. Princeton, NJ: Princeton University Press.

Sjöberg M, Albrectsen B, Hjältén J. 2000. Truncated power laws: a tool for understanding aggregation patterns in animals? Ecol. Lett. 3, 90–94. (10.1046/j.1461-0248.2000.00113.x) DOI

Massei G, et al. 2015. Wild boar populations up, numbers of hunters down? A review of trends and implications for Europe. Pest Manag. Sci. 71, 492–500. (10.1002/ps.3965) PubMed DOI

Matuszewski S, Konwerski S, Frątczak K, Szafałowicz M. 2014. Effect of body mass and clothing on decomposition of pig carcasses. Int. J. Legal Med. 128, 1039–1048. (10.1007/s00414-014-0965-5) PubMed DOI PMC

Podgórski T, Baś G, Jędrzejewska B, Sönnichsen L, Śnieżko S, Jędrzejewski W, Okarma H. 2013. Spatiotemporal behavioral plasticity of wild boar (Sus scrofa) under contrasting conditions of human pressure: primeval forest and metropolitan area. J. Mammal. 94, 109–119. (10.1644/12-MAMM-A-038.1) DOI

Kay SL, et al. 2017. Quantifying drivers of wild pig movement across multiple spatial and temporal scales. Mov. Ecol. 5, 14 (10.1186/s40462-017-0105-1) PubMed DOI PMC

Shea K, Tildesley MJ, Runge MC, Fonnesbeck CJ, Ferrari MJ, Dobson AP. 2014. Adaptive management and the value of information: learning via intervention in epidemiology. PLoS Biol. 12, e1001970 (10.1371/journal.pbio.1001970) PubMed DOI PMC

Gudelj I, White KAJ. 2004. Spatial heterogeneity, social structure and disease dynamics of animal populations. Theor. Popul. Biol. 66, 139–149. (10.1016/j.tpb.2004.04.003) PubMed DOI

Craft ME, Volz E, Packer C, Meyers LA. 2011. Disease transmission in territorial populations: the small-world network of Serengeti lions. J. R. Soc. Interface 8, 776–786. (10.1098/rsif.2010.0511) PubMed DOI PMC

Donnelly CA, et al. 2006. Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature 439, 843–846. (10.1038/nature04454) PubMed DOI

McDonald JL, Robertson A, Silk MJ. 2018. Wildlife disease ecology from the individual to the population: insights from a long-term study of a naturally infected European badger population. J. Anim. Ecol. 87, 101–112. (10.1111/1365-2656.12743) PubMed DOI

Firestone SM, Christley RM, Ward MP, Dhand NK. 2012. Adding the spatial dimension to the social network analysis of an epidemic: investigation of the 2007 outbreak of equine influenza in Australia. Prev. Vet. Med. 106, 123–135. (10.1016/j.prevetmed.2012.01.020) PubMed DOI PMC

Manlove K, Aiello C, Sah P, Cummins B, Hudson PJ, Cross PC.. 2018. The ecology of movement and behaviour: a saturated tripartite network for describing animal contacts. Proc. R. Soc. B 285, 20180670 (10.1098/rspb.2018.0670) PubMed DOI PMC

Riley S, Eames K, Isham V, Mollison D, Trapman P. 2015. Five challenges for spatial epidemic models. Epidemics 10, 68–71. (10.1016/j.epidem.2014.07.001) PubMed DOI PMC

Langrock R, et al. 2014. Modelling group dynamic animal movement. Methods Ecol. Evol. 5, 190–199. (10.1111/2041-210X.12155) DOI

Spiegel O, Leu ST, Sih A, Bull CM, Münkemüller T. 2016. Socially interacting or indifferent neighbours? Randomization of movement paths to tease apart social preference and spatial constraints. Methods Ecol. Evol. 7, 971–979. (10.1111/2041-210X.12553) DOI

Belsare AV, Gompper ME, Keller B, Sumners J, Hansen L, Millspaugh JJ. 2020. An agent-based framework for improving wildlife disease surveillance: a case study of chronic wasting disease in Missouri white-tailed deer. Ecol. Modell. 417, 108919 (10.1016/j.ecolmodel.2019.108919) PubMed DOI PMC

Merli E, Grignolio S, Marcon A, Apollonio M. 2017. Wild boar under fire: the effect of spatial behaviour, habitat use and social class on hunting mortality. J. Zool. 303, 155–164. (10.1111/jzo.12471) DOI

Campbell TA, Long DB, Leland BR. 2010. Feral swine behavior relative to aerial gunning in southern Texas. J. Wildl. Manage. 74, 337–341. (10.2193/2009-131) DOI

Sodeikat G, Pohlmeyer K. 2002. Temporary home range modifications of wild boar family groups (Sus scrofa L.) caused by drive hunts in Lower Saxony (Germany). Z. Jagdwiss. 48, 161–166.

Chenais E, Depner K, Guberti V, Dietze K, Viltrop A, Ståhl K. 2019. Epidemiological considerations on African swine fever in Europe 2014–2018. Porcine Health Manage. 5, 1–6. (10.1186/s40813-018-0109-2) PubMed DOI PMC

European Food Safety Authority et al. 2017. Epidemiological analyses of African swine fever in the Baltic States and Poland (update September 2016–September 2017). EFSA J. 15, e05068. PubMed PMC

Pautienius A, et al. 2018. Prevalence and spatiotemporal distribution of African swine fever in Lithuania, 2014–2017. Virol. J. 15, 177 (10.1186/s12985-018-1090-8) PubMed DOI PMC

Pejsak Z, et al. 2018. Four years of African swine fever in Poland. New insights into epidemiology and prognosis of future disease spread. Pol. J. Vet. Sci. 21, 835–841. PubMed

Ståhl K, Sternberg-Lewerin S, Blome S, Viltrop A, Penrith M-L, Chenais E. 2019. Lack of evidence for long term carriers of African swine fever virus—a systematic review. Virus Res. 272, 197725 (10.1016/j.virusres.2019.197725) PubMed DOI

O'Neill X, White A, Ruiz-Fons F, Gortázar C. 2020. Modelling the transmission and persistence of African swine fever in wild boar in contrasting European scenarios. Sci. Rep. 10, 5895 (10.1038/s41598-020-62736-y) PubMed DOI PMC

Probst C, Gethmann J, Amler S, Globig A, Knoll B, Conraths FJ. 2019. The potential role of scavengers in spreading African swine fever among wild boar. Sci. Rep. 9, 11450 (10.1038/s41598-019-47623-5) PubMed DOI PMC

Davies K, Goatley LC, Guinat C, Netherton CL, Gubbins S, Dixon LK, Reis AL. 2017. Survival of African swine fever virus in excretions from pigs experimentally infected with the Georgia 2007/1 isolate. Transbound. Emerg. Dis. 64, 425–431. (10.1111/tbed.12381) PubMed DOI PMC

European Food Safety Authority et al. 2018. Epidemiological analyses of African swine fever in the European Union (November 2017 until November 2018). EFSA J. 16, e05494. PubMed PMC

Iglesias I, Muñoz MJ, Montes F, Perez A, Gogin A, Kolbasov D, de la Torre A. 2016. Reproductive ratio for the local spread of African swine fever in wild boars in the Russian Federation. Transbound. Emerg. Dis. 63, e237–e245. (10.1111/tbed.12337) PubMed DOI

Lange M, Guberti V, Thulke HH. 2018. Understanding ASF spread and emergency control concepts in wild boar populations using individual-based modelling and spatio-temporal surveillance data. EFSA Support. Publ. 15, 1521E (10.2903/sp.efsa.2018.EN-1521) DOI

Probst C, Globig A, Knoll B, Conraths FJ, Depner K. 2017. Behaviour of free ranging wild boar towards their dead fellows: potential implications for the transmission of African swine fever. R. Soc. Open Sci. 4, 170054 (10.1098/rsos.170054) PubMed DOI PMC

Eble P, Hagenaars TJ, Weesendorp E, Quak S, Moonen-Leusen HW, Loeffen WLA. 2019. Transmission of African swine fever virus via carrier (survivor) pigs does occur. Vet. Microbiol. 237, 108345 (10.1016/j.vetmic.2019.06.018) PubMed DOI

Podgórski T, Scandura M, Jędrzejewska B. 2014. Next of kin next door—philopatry and socio-genetic population structure in wild boar. J. Zool. 294, 190–197. (10.1111/jzo.12167) DOI

Keeling MJ 1999. The effects of local spatial structure on epidemiological invasions. Proc. R. Soc. Lond. B 266, 859–867. (10.1098/rspb.1999.0716) PubMed DOI PMC

Ames GM, George DB, Hampson CP, Kanarek AR, McBee CD, Lockwood DR, Achter JD, Webb CT. 2011. Using network properties to predict disease dynamics on human contact networks. Proc. R. Soc. B 278, 3544–3550. (10.1098/rspb.2011.0290) PubMed DOI PMC

Risk of African swine fever virus transmission among wild boar and domestic pigs in Poland