Advances from the nexus of animal behaviour and pathogen transmission: new directions and opportunities using contact networks

In: Behaviour

Abstract

Contact network models have enabled significant advances in understanding the influence of behaviour on parasite and pathogen transmission. They are an important tool that links variation in individual behaviour, to epidemiological consequences at the population level. Here, in our introduction to this special issue, we highlight the importance of applying network approaches to disease ecological and epidemiological questions, and how this has provided a much deeper understanding of these research areas. Recent advances in tracking host behaviour (bio-logging: e.g., GPS tracking, barcoding) and tracking pathogens (high-resolution sequencing), as well as methodological advances (multi-layer networks, computational techniques) started producing exciting new insights into disease transmission through contact networks. We discuss some of the exciting directions that the field is taking, some of the challenges, and importantly the opportunities that lie ahead. For instance, we suggest to integrate multiple transmission pathways, multiple pathogens, and in some systems, multiple host species, into the next generation of network models. Corresponding opportunities exist in utilising molecular techniques, such as high-resolution sequencing, to establish causality in network connectivity and disease outcomes. Such novel developments and the continued integration of network tools offers a more complete understanding of pathogen transmission processes, their underlying mechanisms and their evolutionary consequences.

  • AdelmanJ.S.MoyersS.C.FarineD.R. & HawleyD.M. (2015). Feeder use predicts both acquisition and transmission of a contagious pathogen in a North American songbird. — Proc. Roy. Soc. Lond. B: Biol. Sci. 282: 20151429.

    • Search Google Scholar
    • Export Citation
  • AielloC.M.EsqueT.C.NussearK.E.EmblidgeP.G. & HudsonP.J. (2018). Associating sex-biased and seasonal behaviour with contact patterns and transmission risk in Gopherus agassizii. — Behaviour 155: 585-619.

    • Search Google Scholar
    • Export Citation
  • AielloC.M.NussearK.E.WaldeA.D.EsqueT.C.EmblidgeP.G.SahP.BansalS. & HudsonP.J. (2014). Disease dynamics during wildlife translocations: disruptions to the host population and potential consequences for transmission in desert tortoise contact networks. — Anim. Cons. 17: 27-39.

    • Search Google Scholar
    • Export Citation
  • Alarcón-NietoG.GravingJ.M.Klarevas-IrbyJ.A.Maldonado-ChaparroA.A.MuellerI. & FarineD.R. (2018). An automated barcode tracking system for behavioural studies in birds. — Methods Ecol. Evol. 9: 1536-1547.

    • Search Google Scholar
    • Export Citation
  • Azimi-TafreshiN. (2016). Cooperative epidemics on multiplex networks. — Phys. Rev. E 93: 042303.

  • BansalS.GrenfellB.T. & MeyersL.A. (2007). When individual behaviour matters: homogeneous and network models in epidemiology. — J. R. Soc. Interface 4: 879-891.

    • Search Google Scholar
    • Export Citation
  • BansalS.ReadJ.PourbohloulB. & MeyersL.A. (2010). The dynamic nature of contact networks in infectious disease epidemiology. — J. Biol. Dyn. 4: 478-489.

    • Search Google Scholar
    • Export Citation
  • BlytonM.D.J.BanksS.C.PeakallR.LindenmayerD.B. & GordonD.M. (2014). Not all types of host contacts are equal when it comes to E. coli transmission. — Ecol. Lett. 17: 970-978.

    • Search Google Scholar
    • Export Citation
  • BöhmM.HutchingsM.R. & WhiteP.C. (2009). Contact networks in a wildlife-livestock host community: identifying high-risk individuals in the transmission of bovine TB among badgers and cattle. — PLoS One 4: e5016.

    • Search Google Scholar
    • Export Citation
  • BrearleyG.RhodesJ.BradleyA.BaxterG.SeabrookL.LunneyD.LiuY. & McAlpineC. (2013). Wildlife disease prevalence in human-modified landscapes. — Biol. Rev. 88: 427-442.

    • Search Google Scholar
    • Export Citation
  • BrentL.N.MacLarnonA.PlattM. & SempleS. (2013). Seasonal changes in the structure of rhesus macaque social networks. — Behav. Ecol. Sociobiol. 67: 349-359.

    • Search Google Scholar
    • Export Citation
  • BullC.M.GodfreyS.S. & GordonD.M. (2012). Social networks and the spread of Salmonella in a sleepy lizard population. — Mol. Ecol. 21: 4386-4392.

    • Search Google Scholar
    • Export Citation
  • ChenS.WhiteB.J.SandersonM.W.AmrineD.E.IlanyA. & LanzasC. (2014). Highly dynamic animal contact network and implications on disease transmission. — Sci. Rep. 4: 4472.

    • Search Google Scholar
    • Export Citation
  • CornerL.A.L.PfeifferD.U. & MorrisR.S. (2003). Social-network analysis of Mycobacterium bovis transmission among captive brushtail possums (Trichosurus vulpecula). — Prev. Vet. Med. 59: 147-167.

    • Search Google Scholar
    • Export Citation
  • CraftM.E.VolzE.PackerC. & MeyersL.A. (2009). Distinguishing epidemic waves from disease spillover in a wildlife population. — Proc. Roy. Soc. Lond. B: Biol. Sci. DOI:10.1098/rspb.2008.1636.

    • Search Google Scholar
    • Export Citation
  • CraftM.E. (2015). Infectious disease transmission and contact networks in wildlife and livestock. — Philos. Trans. Roy. Soc. B: Biol. Sci. 370: 2014107.

    • Search Google Scholar
    • Export Citation
  • CroftD.P.JamesR.WardA.J.W.BothamM.S.MawdsleyD. & KrauseJ. (2005). Assortative interactions and social networks in fish. — Oecologia 143: 211-219.

    • Search Google Scholar
    • Export Citation
  • CroftD.P.MaddenJ.R.FranksD.W. & JamesR. (2011). Hypothesis testing in animal social networks. — Trends Ecol. Evol. 26: 502-507.

    • Search Google Scholar
    • Export Citation
  • DoughertyE.R.SeidelD.P.CarlsonC.J.SpiegelO.GetzW.M. & LaffertyK. (2018). Going through the motions: incorporating movement analyses into disease research. — Ecol. Lett. 21: 588-604.

    • Search Google Scholar
    • Export Citation
  • EzenwaV.O.ArchieE.A.CraftM.E.HawleyD.M.MartinL.B.MooreJ. & WhiteL. (2016). Host behaviour-parasite feedback: an essential link between animal behaviour and disease ecology. — Proc. Roy. Soc. Lond. B: Biol. Sci. 283: 20153078.

    • Search Google Scholar
    • Export Citation
  • FarineD. (2017a). The dynamics of transmission and the dynamics of networks. — J. Anim. Ecol. 86: 415-418.

  • FarineD.R. (2017b). A guide to null models for animal social network analysis. — Methods Ecol. Evol. 8: 1309-1320.

  • FeffermanN.H. & NgK.L. (2007). How disease models in static networks can fail to approximate disease in dynamic networks. — Phys. Rev. E 76: 031919.

    • Search Google Scholar
    • Export Citation
  • GilbertsonM.L.Fountain-JonesN.M. & CraftM.E. (2018). Incorporating genomic methods into contact networks to reveal new insights into animal behaviour and infectious disease dynamics. — Behaviour 155: 759-791.

    • Search Google Scholar
    • Export Citation
  • GodfreyS.S.BradleyJ.K.SihA. & BullC.M. (2012). Lovers and fighters in sleepy lizard land: where do aggressive males fit in a social network?Anim. Behav. 83: 209-215.

    • Search Google Scholar
    • Export Citation
  • GodfreyS.S. (2013). Networks and the ecology of parasite transmission: a framework for wildlife parasitology. — Int. J. Parasitol. Parasites Wildl. 2: 235-245.

    • Search Google Scholar
    • Export Citation
  • GorsichE.E.EtienneR.S.MedlockJ.BeechlerB.R.SpaanJ.M.SpaanR.S.EzenwaV.O. & JollesA.E. (2018). Opposite outcomes of coinfection at individual and population scales. — Proc. Natl. Acad. Sci. USA 115: 7545-7550.

    • Search Google Scholar
    • Export Citation
  • Guimarães JrP.R.de MenezesM.A.BairdR.W.LusseauD.GuimarãesP. & Dos ReisS.F. (2007). Vulnerability of a killer whale social network to disease outbreaks. — Phys. Rev. E. 76: 042901.

    • Search Google Scholar
    • Export Citation
  • HartB.L. & HartL.A. (2018). How mammals stay healthy in nature: the evolution of behaviours to avoid parasites and pathogens. — Phil. Trans. Roy. Soc. B: Biol. Sci. 373: 20170205.

    • Search Google Scholar
    • Export Citation
  • HassellJ.M.BegonM.WardM.J. & FèvreE.M. (2017). Urbanization and disease emergence: dynamics at the wildlife–livestock–human interface. — Trends Ecol. Evol. 32: 55-67.

    • Search Google Scholar
    • Export Citation
  • HolmeP. & LiljerosF. (2014). Birth and death of links control disease spreading in empirical contact networks. — Sci. Rep. 4: 4999.

    • Search Google Scholar
    • Export Citation
  • JacobyD.M. & FreemanR. (2016). Emerging network-based tools in movement ecology. — Trends Ecol. Evol. 31: 301-314.

  • JonesK.L.ThompsonR.C.A. & GodfreyS.S. (2018). Social networks: a tool for assessing the impact of perturbations on wildlife behaviour and implications for pathogen transmission. — Behaviour 155: 689-730.

    • Search Google Scholar
    • Export Citation
  • KashimaK.OhtsukiH. & SatakeA. (2013). Fission-fusion bat behavior as a strategy for balancing the conflicting needs of maximizing information accuracy and minimizing infection risk. — J. Theor. Biol. 318: 101-109.

    • Search Google Scholar
    • Export Citation
  • KaysR.CrofootM.C.JetzW. & WikelskiM. (2015). Terrestrial animal tracking as an eye on life and planet. — Science 348: aaa2478.

    • Search Google Scholar
    • Export Citation
  • KeiserC.N.Pinter-WollmanN.AugustineD.A.ZiembaM.J.HaoL.LawrenceJ.G. & PruittJ.N. (2016). Individual differences in boldness influence patterns of social interactions and the transmission of cuticular bacteria among group-mates. — Proc. Roy. Soc. Lond. B: Biol. Sci. 283: 20160457.

    • Search Google Scholar
    • Export Citation
  • KieseckerJ.M.SkellyD.K.BeardK.H. & PreisserE. (1999). Behavioral reduction of infection risk. — Proc. Natl. Acad. Sci. USA 96: 9165-9168.

    • Search Google Scholar
    • Export Citation
  • KrauseJ.KrauseS.ArlinghausR.PsorakisI.RobertsS. & RutzC. (2013). Reality mining of animal social systems. — Trends Ecol. Evol. 28: 541-551.

    • Search Google Scholar
    • Export Citation
  • LeuS.T.KappelerP.M. & BullC.M. (2010). Refuge sharing network predicts ectoparasite load in a lizard. — Behav. Ecol. Sociobiol. 64: 1495-1503.

    • Search Google Scholar
    • Export Citation
  • LeuS.T.FarineD.R.WeyT.W.SihA. & BullC.M. (2016). Environment modulates population social structure: experimental evidence from replicated social networks of wild lizards. — Anim. Behav. 111: 23-31.

    • Search Google Scholar
    • Export Citation
  • Lloyd-SmithJ.O.SchreiberS.J.KoppP.E. & GetzW.M. (2005). Superspreading and the effect of individual variation on disease emergence. — Nature 438: 355-359.

    • Search Google Scholar
    • Export Citation
  • LopesP.C.BlockP. & KönigB. (2016). Infection-induced behavioural changes reduce connectivity and the potential for disease spread in wild mice contact networks. — Sci. Rep. 6: 31790.

    • Search Google Scholar
    • Export Citation
  • MarcoglieseD.J. & PietrockM. (2011). Combined effects of parasites and contaminants on animal health: parasites do matter. — Trends Parasitol. 27: 123-130.

    • Search Google Scholar
    • Export Citation
  • NunnC.L.JordánF.McCabeC.M.VerdolinJ.L. & FewellJ.H. (2015). Infectious disease and group size: more than just a numbers game. — Philos. Trans. Roy. Soc. Lond. B: Biol. Sci. 370: 20140111.

    • Search Google Scholar
    • Export Citation
  • OhK.P. & BadyaevA.V. (2010). Structure of social networks in a passerine bird: consequences for sexual selection and the evolution of mating strategies. — Am. Nat. 176: E80-E89.

    • Search Google Scholar
    • Export Citation
  • OtterstatterM.C. & ThomsonJ.D. (2007). Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies. — Oecologia. 154: 411-421.

    • Search Google Scholar
    • Export Citation
  • PilosofS.PorterM.A.PascualM. & KefiS. (2017). The multilayer nature of ecological networks. — Nat. Ecol. Evol. 1: 0101.

  • PoulinR. (1994). Meta-analysis of parasite-induced behavioural changes. — Anim. Behav. 48: 137-146.

  • PoulinR. (2013). Parasite manipulation of host personality and behavioural syndromes. — J. Exp. Biol. 216: 18-26.

  • PoulinR. (2018). Modification of host social networks by manipulative parasites. — Behaviour 155: 671-688.

  • ReynoldsJ.J.HirschB.T.GehrtS.D. & CraftM.E. (2015). Raccoon contact networks predict seasonal susceptibility to rabies outbreaks and limitations of vaccination. — J. Anim. Ecol. 84: 1720-1731.

    • Search Google Scholar
    • Export Citation
  • RichardF.J.AubertA. & GrozingerC.M. (2008). Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. — BMC Biol. 6: 50.

    • Search Google Scholar
    • Export Citation
  • RimbachR.BisanzioD.GalvisN.LinkA.Di FioreA. & GillespieT.R. (2015). Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics. — Philos. Trans. R. Soc. Lond. B: Biol. Sci. 370: 20140110.

    • Search Google Scholar
    • Export Citation
  • RoucoC.JewellC.RichardsonK.S.FrenchN.P.BuddleB.M. & TompkinsD.M. (2018). Brushtail possum (Trichosurus vulpecula) social interactions and their implications for bovine tuberculosis epidemiology. — Behaviour 155: 621-637.

    • Search Google Scholar
    • Export Citation
  • RuchJ.DumkeM. & SchneiderJ.M. (2015). Social network structure in group-feeding spiders. — Behav. Ecol. Sociobiol 69: 1429-1436.

    • Search Google Scholar
    • Export Citation
  • RynkiewiczE.C.PedersenA.B. & FentonA. (2015). An ecosystem approach to understanding and managing within-host parasite community dynamics. — Trends Parasitol. 31: 212-221.

    • Search Google Scholar
    • Export Citation
  • SahP.LeuS.T.CrossP.C.HudsonP.J. & BansalS. (2017). Unraveling the disease consequences and mechanisms of modular structure in animal social networks. — Proc. Natl. Acad. Sci. USA 114: 4165-4170.

    • Search Google Scholar
    • Export Citation
  • ShizukaD.ChaineA.S.AndersonJ.JohnsonO.LaursenI.M. & LyonB.E. (2014). Across-year social stability shapes network structure in wintering migrant sparrows. — Ecol. Lett. 17: 998-1007.

    • Search Google Scholar
    • Export Citation
  • SihA.SpiegelO.GodfreyS.LeuS. & BullC.M. (2018). Integrating social networks, animal personalities, movement ecology and parasites: a framework with examples from a lizard. — Anim. Behav. 136: 195-205.

    • Search Google Scholar
    • Export Citation
  • SilkM.J.DreweJ.A.DelahayR.J.WeberN.StewardL.C.Wilson-AggarwalJ.BootsM.HodgsonD.J.CroftD.P. & McDonaldR.A. (2018). Quantifying direct and indirect contacts for the potential transmission of infection between species using a multilayer contact network. — Behaviour 155: 731-757.

    • Search Google Scholar
    • Export Citation
  • SilkM.J.CroftD.P.DelahayR.J.HodgsonD.J.BootsM.WeberN. & McDonaldR.A. (2017). Using social network measures in wildlife disease ecology, epidemiology, and management. — Bioscience 67: 245-257.

    • Search Google Scholar
    • Export Citation
  • SnijdersL.van RooijE.P.BurtJ.M.HindeC.A.van OersK. & NaguibM. (2014). Social networking in territorial great tits: slow explorers have the least central social network positions. — Anim. Behav. 98: 95-102.

    • Search Google Scholar
    • Export Citation
  • SpiegelO.LeuS.T.SihA. & BullC.M. (2016). Socially-interacting or indifferent neighbors? Randomization of movement paths to tease apart social preference and spatial constraints. — Methods Ecol. Evol. 7: 971-979.

    • Search Google Scholar
    • Export Citation
  • SpiegelO.LeuS.T.BullC.M. & SihA. (2017a). What’s your move? Movement as a link between personality and spatial dynamics in animal populations. — Ecol. Lett. 20: 3-18.

    • Search Google Scholar
    • Export Citation
  • SpringerA.KappelerP.M. & NunnC.L. (2017). Dynamic vs. static social networks in models of parasite transmission: predicting Cryptosporidium spread in wild lemurs. — J. Anim. Ecol. 86: 419-433.

    • Search Google Scholar
    • Export Citation
  • SpringerA.MellmannA.FichtelC. & KappelerP.M. (2016). Social structure and Escherichia coli sharing in a group-living wild primate, Verreaux’s sifaka. — BMC Ecol. 16: 1-12.

    • Search Google Scholar
    • Export Citation
  • StellaM.AndreazziC.S.SelakovicS.GoudarziA. & AntonioniA. (2017). Parasite spreading in spatial ecological multiplex networks. — J. Complex Netw. 5: 486-511.

    • Search Google Scholar
    • Export Citation
  • SumnerK.M.McCabeC.M. & NunnC.L. (2018). Network size, structure, and pathogen transmission: a simulation study comparing different community detection algorithms. — Behaviour 155: 639-670.

    • Search Google Scholar
    • Export Citation
  • VanderWaalK.L.AtwillE.R.IsbellL.A. & McCowanB. (2014). Linking social and pathogen transmission networks using microbial genetics in giraffe (Giraffa camelopardalis). — J. Anim. Ecol. 83: 406-414.

    • Search Google Scholar
    • Export Citation
  • VanderWaalK.EnnsE.A.PicassoC.PackerC. & CraftM.E. (2016a). Evaluating empirical contact networks as potential transmission pathways for infectious diseases. — J. R. Soc. Interface 13: 20160166.

    • Search Google Scholar
    • Export Citation
  • VanderWaalK.L.ObandaV.OmondiG.P.McCowanB.WangH.FushingH. & IsbellL.A. (2016b). The “strength of weak ties” and helminth parasitism in giraffe social networks. — Behav. Ecol. 27: 1190-1197.

    • Search Google Scholar
    • Export Citation
  • WebsterJ.P. (1994). The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus. — Parasitology 109: 583-589.

    • Search Google Scholar
    • Export Citation
  • WeyT.BlumsteinD.T.ShenW. & JordánF. (2008). Social network analysis of animal behaviour: a promising tool for the study of sociality. — Anim. Behav. 75: 333-344.

    • Search Google Scholar
    • Export Citation
  • WeyT.W.BurgerJ.R.EbenspergerL.A. & HayesL.D. (2013). Reproductive correlates of social network variation in plurally breeding degus (Octodon degus). — Anim. Behav. 85: 1407-1414.

    • Search Google Scholar
    • Export Citation
  • WhiteL.A.ForesterJ.D. & CraftM.E. (2017). Using contact networks to explore mechanisms of parasite transmission in wildlife. — Biol. Rev. 92: 389-409.

    • Search Google Scholar
    • Export Citation
  • WymantC.HallM.RatmannO.BonsallD.GolubchikT.de CesareM.GallA.CornelissenM.FraserC.STOP-HCV ConsortiumThe Maela Pneumococcal Collaboration & The BEEHIVE Collaboration (2018). PHYLOSCANNER: inferring transmission from within- and between-host pathogen genetic diversity. — Mol. Biol. Evol. 35: 719-733.

    • Search Google Scholar
    • Export Citation

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