Hostname: page-component-54dcc4c588-2bdfx Total loading time: 0 Render date: 2025-09-12T18:40:08.729Z Has data issue: false hasContentIssue false
  • English
  • Français

Bidirectional interactions between host social behaviour and parasites arise through ecological and evolutionary processes

Published online by Cambridge University Press:  23 October 2020

Dana M. Hawley Open the ORCID record for Dana M. Hawley [Opens in a new window] ,
Amanda K. Gibson ,
Andrea K. Townsend ,
Meggan E. Craft  and
Jessica F. Stephenson
Dana M. Hawley*
Affiliation:
Department of Biological Sciences, Virginia Tech, Blacksburg, VA 24061, USA
Amanda K. Gibson
Affiliation:
Department of Biology, University of Virginia, Charlottesville, VA 22903, USA
Andrea K. Townsend
Affiliation:
Department of Biology, Hamilton College, Clinton, NY 13323, USA
Meggan E. Craft
Affiliation:
Department of Veterinary Population Medicine and Department of Ecology, Evolution and Behavior, University of Minnesota, St Paul, MN 55108, USA
Jessica F. Stephenson
Affiliation:
Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, USA
*
Author for correspondence: Dana M. Hawley, E-mail: Hawleyd@vt.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

An animal's social behaviour both influences and changes in response to its parasites. Here we consider these bidirectional links between host social behaviours and parasite infection, both those that occur from ecological vs evolutionary processes. First, we review how social behaviours of individuals and groups influence ecological patterns of parasite transmission. We then discuss how parasite infection, in turn, can alter host social interactions by changing the behaviour of both infected and uninfected individuals. Together, these ecological feedbacks between social behaviour and parasite infection can result in important epidemiological consequences. Next, we consider the ways in which host social behaviours evolve in response to parasites, highlighting constraints that arise from the need for hosts to maintain benefits of sociality while minimizing fitness costs of parasites. Finally, we consider how host social behaviours shape the population genetic structure of parasites and the evolution of key parasite traits, such as virulence. Overall, these bidirectional relationships between host social behaviours and parasites are an important yet often underappreciated component of population-level disease dynamics and host–parasite coevolution.

Keywords

Avoidance behaviourbehavioural ecologydisease ecologyepidemiologyevolutionary parasitologyhost–parasite coevolutionparasite transmissionparasite-induced behavioural plasticitysickness behavioursocial behaviour

Information

Type
Review Article
Information
Parasitology , Volume 148 , Issue 3 , March 2021 , pp. 274 - 288
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Adamo, SA, Gomez-Juliano, A, LeDue, EE, Little, SN and Sullivan, K (2015) Effect of immune challenge on aggressive behaviour: how to fight two battles at once. Animal Behaviour 105, 153–161.CrossRefGoogle Scholar
Adelman, JS, Kirkpatrick, L, Grodio, JL and Hawley, DM (2013) House finch populations differ in early inflammatory signaling and pathogen tolerance at the peak of Mycoplasma gallisepticum infection. The American Naturalist 181, 674–689.CrossRefGoogle ScholarPubMed
Adelman, JS, Mayer, C and Hawley, DM (2017) Infection reduces anti-predator behaviors in house finches. Journal of Avian Biology 48, 519–528.CrossRefGoogle ScholarPubMed
Alexander, RD (1974) The evolution of social behavior. Annual Review of Ecology and Systematics 5, 325–383.CrossRefGoogle Scholar
Alizon, S, de Roode, JC and Michalakis, Y (2013) Multiple infections and the evolution of virulence. Ecology Letters 16, 556–567.CrossRefGoogle ScholarPubMed
Almberg, ES, Cross, PC, Dobson, AP, Smith, DW, Metz, MC, Stahler, DR and Hudson, PJ (2015) Social living mitigates the costs of a chronic illness in a cooperative carnivore. Ecology Letters 18, 660–667.CrossRefGoogle Scholar
Altermatt, F and Ebert, D (2008) Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecology Letters 11, 918–928.CrossRefGoogle ScholarPubMed
Altizer, S, Nunn, CL, Thrall, PH, Gittleman, JL, Antonovics, J, Cunningham, AA, Dobson, A, Ezenwa, V, Jones, KE, Pedersen, AB, Poss, M and Pulliam, JRC (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics 34, 517–547.CrossRefGoogle Scholar
Alzaga, V, Vicente, J, Villanua, D, Acevedo, P, Casas, F and Gortazar, C (2008) Body condition and parasite intensity correlates with escape capacity in Iberian hares (Lepus granatensis). Behavioral Ecology and Sociobiology 62, 769–775.CrossRefGoogle Scholar
Amoroso, CR and Antonovics, J (2020) Evolution of behavioral resistance in host-pathogen systems. Biology Letters 16, 20200508.CrossRefGoogle Scholar
Anderson, JR and Behringer, DC (2013) Spatial dynamics in the social lobster Panulirus argus in response to diseased conspecifics. Marine Ecology Progress Series 474, 191–200.CrossRefGoogle Scholar
Anderson, RM and May, RM (1982). Coevolution of hosts and parasites. Parasitology 85(Pt 2), 411–426.CrossRefGoogle ScholarPubMed
Antonovics, J, Wilson, AJ, Forbes, MR, Hauffe, HC, Kallio, ER, Leggett, HC, Longdon, B, Okamura, B, Sait, SM and Webster, JP (2017) The evolution of transmission mode. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 372, 20160083.CrossRefGoogle ScholarPubMed
Aplin, LM, Farine, DR, Morand-Ferron, J, Cole, EF, Cockburn, A and Sheldon, BC (2013) Individual personalities predict social behaviour in wild networks of great tits (Parus major). Ecology Letters 16, 1365–1372.CrossRefGoogle Scholar
Arakawa, H, Arakawa, K and Deak, T (2009) Acute illness induces the release of aversive odor cues from adult, but not prepubertal, male rats and suppresses social investigation by conspecifics. Behavioral Neuroscience 123, 964–978.CrossRefGoogle Scholar
Archie, EA, Moss, CJ and Alberts, SC (2006) The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proceedings of the Royal Society of London. Series B: Biological Sciences 273, 513–522.Google ScholarPubMed
Baer, B and Schmid-Hempel, P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397, 151–154.CrossRefGoogle Scholar
Baracchi, D, Fadda, A and Turillazzi, S (2012) Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. Journal of Insect Physiology 58, 1589–1596.CrossRefGoogle ScholarPubMed
Barber, I and Dingemanse, NJ (2010) Parasitism and the evolutionary ecology of animal personality. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 365, 4077–4088.CrossRefGoogle ScholarPubMed
Barrett, LG, Thrall, PH, Burdon, JJ and Linde, CC (2008) Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends in Ecology & Evolution 23, 678–685.CrossRefGoogle ScholarPubMed
Baudouin, A, Gatti, S, Levréro, F, Genton, C, Cristescu, RH, Billy, V, Motsch, P, Pierre, JS, Le Gouar, P and Ménard, N (2019) Disease avoidance, and breeding group age and size condition the dispersal patterns of western lowland gorilla females. Ecology 100, e02786–29.CrossRefGoogle ScholarPubMed
Begon, M, Bennett, M, Bowers, RG, French, NP, Hazel, SM and Turner, J (2002) A clarification of transmission terms in host-microparasite models: numbers, densities and areas. Epidemiology and Infection 129, 147–153.CrossRefGoogle ScholarPubMed
Behringer, DC, Butler, MJD and Shields, J (2006) Avoidance of disease by social lobsters. Nature 441, 421.CrossRefGoogle ScholarPubMed
Berngruber, TW, Lion, S and Gandon, S (2015) Spatial structure, transmission modes and the evolution of viral exploitation strategies. PLoS Pathogens 11, e1004810.CrossRefGoogle ScholarPubMed
Best, A, Webb, S, White, A and Boots, M (2011) Host resistance and coevolution in spatially structured populations. Proceedings of the Royal Society of London. Series B: Biological Sciences 278, 2216–2222.Google ScholarPubMed
Biganski, S, Kurze, C, Müller, MY and Moritz, RFA (2018) Social response of healthy honeybees towards Nosema ceranae-infected workers: care or kill? Apidologie 49, 325–334.CrossRefGoogle Scholar
Block, P, Hoffman, M, Raabe, IJ, Dowd, JB, Rahal, C, Kashyap, R and Mills, MC (2020) Social network-based distancing strategies to flatten the COVID-19 curve in a post-lockdown world. Nature Human Behaviour 4, 588–596.CrossRefGoogle Scholar
Blumstein, DT, Ebensperger, L and Hayes, L (2010) Towards an integrative understanding of social behavior: new models and new opportunities. Frontiers in Behavioral Neuroscience 4, 34.Google Scholar
Bolker, BM, Nanda, A and Shah, D (2010) Transient virulence of emerging pathogens. Journal of the Royal Society Interface/the Royal Society 7, 811–822.CrossRefGoogle ScholarPubMed
Bonds, MH, Keenan, DC, Leidner, AJ and Rohani, P (2005) Higher disease prevalence can induce greater sociality: a game theoretic coevolutionary model. Evolution 59, 1859–1866.CrossRefGoogle ScholarPubMed
Bono, LM, Smith, LB Jr, Pfennig, DW and Burch, CL (2017) The emergence of performance trade-offs during local adaptation: insights from experimental evolution. Molecular Ecology 26, 1720–1733.CrossRefGoogle ScholarPubMed
Boots, M and Mealor, M (2007) Local interactions select for lower pathogen infectivity. Science (New York, N.Y.) 315, 1284–1286.CrossRefGoogle ScholarPubMed
Boots, M and Sasaki, A (1999) ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance. Proceedings of the Royal Society of London. Series B: Biological Sciences 266, 1933–1938.CrossRefGoogle ScholarPubMed
Bordes, F, Blumstein, DT and Morand, S (2007) Rodent sociality and parasite diversity. Biology Letters 3, 692–694.CrossRefGoogle ScholarPubMed
Bos, N, Lefèvre, T, Jensen, AB and d'Ettorre, P (2012) Sick ants become unsociable. Journal of Evolutionary Biology 25, 342–351.CrossRefGoogle ScholarPubMed
Bouwman, KM and Hawley, DM (2010) Sickness behaviour acting as an evolutionary trap? Male house finches preferentially feed near diseased conspecifics. Biology Letters 6, 462–465.CrossRefGoogle ScholarPubMed
Bremermann, HJ and Pickering, J (1983) A game-theoretical model of parasite virulence. Journal of Theoretical Biology 100, 411–426.CrossRefGoogle ScholarPubMed
Brown, SP, Hochberg, ME and Grenfell, BT (2002) Does multiple infection select for raised virulence? Trends in Microbiology 10, 401–405.CrossRefGoogle ScholarPubMed
Buck, JC, Weinstein, SB and Young, HS (2018) Ecological and evolutionary consequences of parasite avoidance. Trends in Ecology & Evolution 33, 619–632.CrossRefGoogle ScholarPubMed
Bull, JJ, Molineux, IJ and Rice, WR (1991) Selection of benevolence in a host-parasite system. Evolution 45, 875–882.CrossRefGoogle Scholar
Bull, CM, Godfrey, SS and Gordon, DM (2012) Social networks and the spread of Salmonella in a sleepy lizard population. Molecular Ecology 21, 4386–4392.CrossRefGoogle Scholar
Butler, JM and Roper, TJ (1996) Ectoparasites and sett use in European badgers. Animal Behaviour 52, 621–629.CrossRefGoogle Scholar
Campbell, EO and Luong, LT (2016) Mite choice generates sex- and size-biased infection in Drosophila hydei. Parasitology 143, 787–793.CrossRefGoogle ScholarPubMed
Carney, WP (1969) Behavioral and morphological changes in carpenter ants harboring dicrocoeliid metacercariae. The American Midland Naturalist 82, 605–611.CrossRefGoogle Scholar
Chao, L, Hanley, KA, Burch, CL, Dahlberg, C and Turner, PE (2000) Kin selection and parasite evolution: higher and lower virulence with hard and soft selection. The Quarterly Review of Biology 75, 261–275.CrossRefGoogle ScholarPubMed
Chapman, CA, Friant, S, Godfrey, K, Liu, C, Sakar, D, Schoof, VAM, Sengupta, R, Twinomugisha, D, Valenta, K and Goldberg, TL (2016) Social behaviours and networks of vervet monkeys are influenced by gastrointestinal parasites. PLoS ONE 11, e0161113.CrossRefGoogle ScholarPubMed
Cheesman, CL and Mallinson, PJ (1981) Behavior of badgers (Meles-meles) infected with bovine TB. Journal of Zoology 194, 284–289.CrossRefGoogle Scholar
Childress, MJ, Heldt, KA and Miller, SD (2015) Are juvenile Caribbean spiny lobsters (Panulirus argus) becoming less social? ICES Journal of Marine Science 72, i170–i176.CrossRefGoogle Scholar
Christe, P, Glaizot, O, Evanno, G, Bruyndonckx, N, Devevey, G, Yannic, G, Patthey, P, Maeder, A, Vogel, P and Arlettaz, R (2007) Host sex and ectoparasites choice: preference for, and higher survival on female hosts. Journal of Animal Ecology 76, 703–710.CrossRefGoogle ScholarPubMed
Claessen, D and de Roos, AM (1995) Evolution of virulence in a host-pathogen system with local pathogen transmission. Oikos 74, 401–413.CrossRefGoogle Scholar
Côté, IM and Poulin, R (1995) Parasitism and group size in social animals: a meta-analysis. Behavioral Ecology 6, 159.CrossRefGoogle Scholar
Cremer, S, Pull, CD and Fürst, MA (2018) Social immunity: emergence and evolution of colony-level disease protection. Annual Review of Entomology 63, 105–123.CrossRefGoogle ScholarPubMed
Croft, DP, Edenbrow, M, Darden, SK, Ramnarine, IW, van Oosterhout, C and Cable, J (2011) Effect of gyrodactylid ectoparasites on host behaviour and social network structure in guppies, Poecilia reticulata. Behavioral Ecology and Sociobiology 65, 2219–2227.CrossRefGoogle Scholar
Cross, PC, Lloyd-Smith, JO, Johnson, PLF and Getz, WM (2005) Duelling timescales of host movement and disease recovery determine invasion of disease in structured populations. Ecology Letters 8, 587–595.CrossRefGoogle Scholar
Daversa, DR, Hechinger, RF, Madin, E, Fenton, A, Dell, AI, Ritchie, E, Rohr, J and Rudolf, VHW (2019) Beyond the ecology of fear: non-lethal effects of predators are strong whereas those of parasites are diverse. bioRxiv 766477. doi: 10.1101/766477.Google Scholar
Davis, AR (2012) Kin presence drives philopatry and social aggregation in juvenile Desert Night Lizards (Xantusia vigilis). Behavioral Ecology 23, 18–24.CrossRefGoogle Scholar
de Brooke, ML (1985) The effect of allopreening on tick burdens of moulting eudyptid penguins. The Auk 102, 893–895.Google Scholar
Dennehy, JJ, Abedon, ST and Turner, PE (2007) Host density impacts relative fitness of bacteriophage φ6 genotypes in structured habitats. Evolution 61, 2516–2527.CrossRefGoogle ScholarPubMed
de Roode, JC, Pansini, R, Cheesman, SJ, Helinski, MEH, Huijben, S, Wargo, AR, Bell, AS, Chan, BHK, Walliker, D and Read, AF (2005) Virulence and competitive ability in genetically diverse malaria infections. Proceedings of the National Academy of Sciences 102, 7624–7628.CrossRefGoogle ScholarPubMed
Dizney, L and Dearing, MD (2013) The role of behavioural heterogeneity on infection patterns: implications for pathogen transmission. Animal Behaviour 86, 911–916.CrossRefGoogle ScholarPubMed
Drewe, JA (2010) Who infects whom? Social networks and tuberculosis transmission in wild meerkats. Proceedings of the Royal Society London. Series B: Biological Sciences 277, 633–642.Google ScholarPubMed
Duneau, D and Ebert, D (2012) Host sexual dimorphism and parasite adaptation. PLoS Biology 10, e1001217.CrossRefGoogle ScholarPubMed
Duneau, D, Luijckx, P, Ruder, LF and Ebert, D (2012) Sex-specific effects of a parasite evolving in a female-biased host population. BMC Biology 10, 104.CrossRefGoogle Scholar
Ebert, D (1998) Experimental evolution of parasites. Science (New York, N.Y.) 282, 1432–1436.CrossRefGoogle ScholarPubMed
Edwards, JC (1988) The effects of Trichinella spiralis infection on social interactions in mixed groups of infected and uninfected male mice. Animal Behaviour 36, 529–540.CrossRefGoogle Scholar
Ekroth, AKE, Rafaluk-Mohr, C and King, KC (2019) Host genetic diversity limits parasite success beyond agricultural systems: a meta-analysis. Proceedings of the Royal Society of London. Series B: Biological Sciences 286, 20191811.Google ScholarPubMed
Evans, JD, Aronstein, K, Chen, YP, Hetru, C, Imler, J-L, Jiang, H, Kanost, M, Thompson, GJ, Zou, Z and Hultmark, D (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology 15, 645–656.CrossRefGoogle ScholarPubMed
Ezenwa, VO and Worsley-Tonks, KEL (2018) Social living simultaneously increases infection risk and decreases the cost of infection. Proceedings of the Royal Society of London. Series B: Biological Sciences 285, 20182142.Google ScholarPubMed
Ezenwa, VO, Archie, EA, Craft, ME, Hawley, DM, Martin, LB, Moore, J and White, L (2016a) Host behaviour-parasite feedback: an essential link between animal behaviour and disease ecology. Proceedings of the Royal Society of London. Series B: Biological Sciences 283, 20153078.Google Scholar
Ezenwa, VO, Ghai, RR, McKay, AF and Williams, AE (2016b) Group living and pathogen infection revisited. Current Opinion in Behavioral Sciences 12, 66–72.CrossRefGoogle Scholar
Fairbanks, BM, Hawley, DM and Alexander, KA (2014) No evidence for avoidance of visibly diseased conspecifics in the highly social banded mongoose (Mungos mungo). Behavioral Ecology and Sociobiology 69, 371–381.CrossRefGoogle Scholar
Filiano, AJ, Xu, Y, Tustison, NJ, Marsh, RL, Baker, W, Smirnov, I, Overall, CC, Gadani, SP, Turner, SD, Weng, Z, Peerzade, SN, Chen, H, Lee, KS, Scott, MM, Beenhakker, MP, Litvak, V and Kipnis, J (2016) Unexpected role of interferon-γ in regulating neuronal connectivity and social behaviour. Nature 535, 425–429.CrossRefGoogle ScholarPubMed
Fincher, CL and Thornhill, R (2012) Parasite-stress promotes in-group assortative sociality: the cases of strong family ties and heightened religiosity. The Behavioral and Brain Sciences 35, 61–79.CrossRefGoogle ScholarPubMed
Fisher, RM, Henry, LM, Cornwallis, CK, Kiers, ET and West, SA (2017) The evolution of host-symbiont dependence. Nature Communications 8, 15973.CrossRefGoogle ScholarPubMed
Flint, BF, Hawley, DM and Alexander, KA (2016) Do not feed the wildlife: associations between garbage use, aggression, and disease in banded mongooses (Mungos mungo). Ecology and Evolution 6, 5932–5939.CrossRefGoogle Scholar
Forde, SE, Thompson, JN and Bohannan, BJM (2004) Adaptation varies through space and time in a coevolving host-parasitoid interaction. Nature 431, 841–844.CrossRefGoogle Scholar
Frank, SA (1992) A kin selection model for the evolution of virulence. Proceedings of the Royal Society of London. Series B: Biological Sciences 250, 195–197.Google ScholarPubMed
Freeland, WJ (1976) Pathogens and the evolution of primate sociality. Biotropica 8, 12–24.CrossRefGoogle Scholar
Gandon, S (2002) Local adaptation and the geometry of host–parasite coevolution. Ecology Letters 5, 246–256.CrossRefGoogle Scholar
Gandon, S and Michalakis, Y (2002) Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology 15, 451–462.CrossRefGoogle Scholar
Geffre, AC, Gernat, T, Harwood, GP, Jones, BM, Morselli Gysi, D, Hamilton, AR, Bonning, BC, Toth, AL, Robinson, GE and Dolezal, AG (2020) Honey bee virus causes context-dependent changes in host social behavior. Proceedings of the National Academy of Sciences 117, 10406–10413.CrossRefGoogle ScholarPubMed
Gervasi, SS, Opiekun, M, Martin, T, Beauchamp, GK and Kimball, BA (2018) Sharing an environment with sick conspecifics alters odors of healthy animals. Scientific Reports 8, 14255.CrossRefGoogle ScholarPubMed
Gipson, SAY, Jimenez, L and Hall, MD (2019) Host sexual dimorphism affects the outcome of within-host pathogen competition. Evolution 73, 1443–1455.CrossRefGoogle ScholarPubMed
Godfrey, SS, Ansari, TH, Gardner, MG, Farine, DR and Bull, CM (2014) A contact-based social network of lizards is defined by low genetic relatedness among strongly connected individuals. Animal Behaviour 97, 35–43.CrossRefGoogle Scholar
Greischar, MA and Koskella, B (2007) A synthesis of experimental work on parasite local adaptation. Ecology Letters 10, 418–434.CrossRefGoogle ScholarPubMed
Griffin, RH and Nunn, CL (2012) Community structure and the spread of infectious disease in primate social networks. Evolutionary Ecology 26, 779–800.CrossRefGoogle Scholar
Grosberg, RK and Quinn, JF (1986) The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate. Nature 322, 456–459.CrossRefGoogle Scholar
Hamede, RK, McCallum, H and Jones, M (2013) Biting injuries and transmission of Tasmanian devil facial tumour disease. Journal of Animal Ecology 82, 182–190.CrossRefGoogle ScholarPubMed
Harpur, BA and Zayed, A (2013) Accelerated evolution of innate immunity proteins in social insects: adaptive evolution or relaxed constraint? Molecular Biology and Evolution 30, 1665–1674.CrossRefGoogle ScholarPubMed
Harpur, BA, Guarna, MM, Huxter, E, Higo, H, Moon, K-M, Hoover, SE, Ibrahim, A, Melathopoulos, AP, Desai, S, Currie, RW, Pernal, SF, Foster, LJ and Zayed, A (2019) Integrative genomics reveals the genetics and evolution of the honey bee's social immune system. Genome Biology and Evolution 11, 937–948.CrossRefGoogle ScholarPubMed
Hart, BJ (1988) Biological basis of the behavior of sick animals. Neuroscience and Biobehavioral Reviews 12, 123–137.CrossRefGoogle ScholarPubMed
Hart, BL (1990) Behavioral adaptations to pathogens and parasites: 5 strategies. Neuroscience and Biobehavioral Reviews 14, 273–294.CrossRefGoogle Scholar
Hawley, DM, Etienne, RS, Ezenwa, VO and Jolles, AE (2011) Does animal behavior underlie covariation between hosts’ exposure to infectious agents and susceptibility to infection? Implications for disease dynamics. Integrative and Comparative Biology 51, 528–539.CrossRefGoogle ScholarPubMed
Hoeksema, JD and Forde, SE (2008) A meta-analysis of factors affecting local adaptation between interacting species. The American Naturalist 171, 275–290.CrossRefGoogle ScholarPubMed
Hofmann, HA, Beery, AK, Blumstein, DT, Couzin, ID, Earley, RL, Hayes, LD, Hurd, PL, Lacey, EA, Phelps, SM, Solomon, NG, Taborsky, M, Young, LJ and Rubenstein, DR (2014) An evolutionary framework for studying mechanisms of social behavior. Trends in Ecology & Evolution 29, 581–589.CrossRefGoogle ScholarPubMed
Houde, A and Torio, AJ (1992) Effect of parasitic infection on male color pattern and female choice in guppies. Behavioral Ecology 3, 346–351.CrossRefGoogle Scholar
Hubert, J-N, Zerjal, T and Hospital, F (2018) Cancer- and behavior-related genes are targeted by selection in the Tasmanian devil (Sarcophilus harrisii). PLoS ONE 13, e0201838–15.CrossRefGoogle Scholar
Hughes, DP, Pierce, NE and Boomsma, JJ (2008) Social insect symbionts: evolution in homeostatic fortresses. Trends in Ecology & Evolution 23, 672–677.CrossRefGoogle ScholarPubMed
Jacquin, L, Reader, SM, Boniface, A, Mateluna, J, Patalas, I, Pérez-Jvostov, F and Hendry, AP (2016) Parallel and non-parallel behavioural evolution in response to parasitism and predation in Trinidadian guppies. Journal of Evolutionary Biology 29, 1406–1422.CrossRefGoogle Scholar
Kassen, R (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology 15, 173–190.CrossRefGoogle Scholar
Kavaliers, M, Choleris, E and Pfaff, DW (2005) Genes, odours and the recognition of parasitized individuals by rodents. Trends in Ecology & Evolution 21, 423–429.Google ScholarPubMed
Keiser, N, Pinter-Wollman, N, Augustine, DA, Ziemba, MJ, Hao, L, Lawrence, JG and Pruitt, JN (2016) Individual differences in boldness influence patterns of social interactions and the transmission of cuticular bacteria among group-mates. Proceedings of the Royal Society of London. Series B: Biological Sciences 283, 20160457.Google ScholarPubMed
Kerr, B, Neuhauser, C, Bohannan, BJM and Dean, AM (2006) Local migration promotes competitive restraint in a host–pathogen ‘tragedy of the commons’. Nature 442, 75–78.CrossRefGoogle Scholar
Kessler, SE, Bonnell, TR, Byrne, RW and Chapman, CA (2017) Selection to outsmart the germs: the evolution of disease recognition and social cognition. Journal of Human Evolution 108, 92–109.CrossRefGoogle ScholarPubMed
King, KC and Lively, CM (2012) Does genetic diversity limit disease spread in natural host populations? Heredity 109, 199–203.CrossRefGoogle ScholarPubMed
Kirsten, K, Fior, DXB, Kreutz, LC and Barcellos, LJXG (2018) First description of behavior and immune system relationship in fish. Scientific Reports 8, 1–7.CrossRefGoogle ScholarPubMed
Klein, SL (2000) The effects of hormones on sex differences in infection: from genes to behavior. Neuroscience and Biobehavioral Reviews 24, 627–638.CrossRefGoogle Scholar
Klein, SL (2003) Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiology & Behavior 79, 441–449.CrossRefGoogle ScholarPubMed
Klemme, I, Hyvärinen, P and Karvonen, A (2020) Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations. Proceedings of the Royal Society of London. Series B: Biological Sciences 287, 20200388.Google ScholarPubMed
Kocher, SD, Mallarino, R, Rubin, BER, Yu, DW, Hoekstra, HE and Pierce, NE (2018) The genetic basis of a social polymorphism in halictid bees. Nature Communications 9, 4338.CrossRefGoogle ScholarPubMed
Koprivnikar, J and Penalva, L (2015) Lesser of two evils? Foraging choices in response to threats of predation and parasitism. PLoS ONE 10, e0116569.CrossRefGoogle ScholarPubMed
Kotrschal, A, Szorkovszky, A, Herbert-Read, J, Bloch, NI, Romenskyy, M, Buechel, SD, Eslava, AF, Alòs, LS, Zeng, H, Le Foll, A, Braux, G, Pelckmans, K, Mank, JE, Sumpter, D and Kolm, N (2020) Rapid evolution of coordinated and collective movement in response to artificial selection. bioRxiv 2020.01.30.926311. doi: 10.1101/2020.01.30.926311.Google ScholarPubMed
Krause, J and Ruxton, GD (2002) Living in Groups. Oxford: Oxford University Press.Google Scholar
Kulahci, IG, Ghazanfar, AA and Rubenstein, DI (2018) Consistent individual variation across interaction networks indicates social personalities in lemurs. Animal Behaviour 136, 217–226.CrossRefGoogle Scholar
Lefevre, T, Adamo, SA, Biron, DG, Missé, D, Hughes, D and Thomas, F (2009) Invasion of the body snatchers: the diversity and evolution of manipulative strategies in host–parasite interactions. Advances in Parasitology 68, 45–83.Google ScholarPubMed
Lion, S and Boots, M (2010) Are parasites ‘prudent’ in space? Ecology Letters 13, 1245–1255.CrossRefGoogle ScholarPubMed
Lipsitch, M, Herre, EA and Nowak, MA (1995) Host population structure and the evolution of virulence: a ‘Law of Diminishing Returns’. Evolution 49, 743–748.Google Scholar
Lively, CM (1999) Migration, virulence, and the geographic mosaic of adaptation by parasites. The American Naturalist 153, S34–S47.CrossRefGoogle ScholarPubMed
Lively, CM (2016) Coevolutionary epidemiology: disease spread, local adaptation, and sex. The American Naturalist 187, E77–E82.CrossRefGoogle ScholarPubMed
Loehle, C (1995) Social barriers to pathogen transmission in wild animal populations. Ecology 76, 326–335.CrossRefGoogle Scholar
Lopes, PC (2014) When is it socially acceptable to feel sick? Proceedings of the Royal Society B. Series B: Biological Sciences 281, 20140218.Google ScholarPubMed
Lopes, PC, Adelman, J, Wingfield, JC and Bentley, GE (2012) Social context modulates sickness behaviour. Behavioral Ecology and Sociobiology 66, 1421–1428.CrossRefGoogle Scholar
Lopes, PC, Block, P and König, B (2016) Infection-induced behavioural changes reduce connectivity and the potential for disease spread in wild mice contact networks. Scientific Reports 6, 31790.CrossRefGoogle ScholarPubMed
López-Uribe, MM, Sconiers, WB, Frank, SD, Dunn, RR and Tarpy, DR (2016) Reduced cellular immune response in social insect lineages. Biology Letters 12, 20150984.CrossRefGoogle ScholarPubMed
McCabe, CM, Reader, SM and Nunn, CL (2015) Infectious disease, behavioural flexibility and the evolution of culture in primates. Proceedings of the Royal Society of London. Series B: Biological Sciences 282, 20140862.Google ScholarPubMed
Messenger, AL, Molineux, IJ and Bull, JJ (1999) Virulence evolution in a virus obeys a trade-off. Proceedings of the Royal Society of London. Series B: Biological Sciences 266, 397–404.CrossRefGoogle Scholar
Mikheev, VN, Pasternak, AF, Morozov, AY and Taskinen, J (2019) Innate antipredator behavior can promote infection in fish even in the absence of predators. Behavioral Ecology 31, 267–276.CrossRefGoogle Scholar
Moore, J (2002) Parasites and the Behavior of Animals. Oxford, UK: Oxford University Press.Google Scholar
Mooring, MS and Hart, BL (1992) Animal grouping for protection from parasites: selfish herd and encounter-dilution effects. Behaviour 123, 173–193.CrossRefGoogle Scholar
Mooring, MS, Hart, BL and Fitzpatrick, TA (2006) Grooming in desert bighorn sheep (Ovis canadensis mexicana) and the ghost of parasites past. Behavioral Ecology 17, 364–371.CrossRefGoogle Scholar
Morgan, AD, Gandon, S and Buckling, A (2005) The effect of migration on local adaptation in a coevolving host–parasite system. Nature 437, 253.CrossRefGoogle Scholar
Müller-Klein, N, Heistermann, M, Strube, C, Franz, M, Schülke, O and Ostner, J (2019) Exposure and susceptibility drive reinfection with gastrointestinal parasites in a social primate. Functional Ecology 43, 67.Google Scholar
Nadler, SA (1995) Microevolution and the genetic structure of parasite populations. The Journal of Parasitology 81, 395–403.CrossRefGoogle ScholarPubMed
Nadler, SE, Hafner, MS, Hafner, JC and Hafner, DJ (1990) Genetic differentiation among chewing louse populations (Mallophaga: Trichodectidae) in a pocket gopher contact zone (Rodentia: Geomyidae). Evolution 44, 942–951.CrossRefGoogle Scholar
Natoli, E, Say, L, Cafazzo, S, Bonanni, R, Schmid, M and Pontier, D (2005) Bold attitude makes male urban feral domestic cats more vulnerable to Feline Immunodeficiency Virus. Neuroscience and Biobehavioral Reviews 29, 151–157.CrossRefGoogle ScholarPubMed
Nunn, CL and Altizer, S (2006) Host–parasite dynamics and epidemiological principles. In Nunn, C and Altizer, S (eds), Infectious Diseases in Primates: Behavior, Ecology and Evolution. New York, NY : Oxford University Press, pp. 98–133. doi: 10.1093/acprof:oso/9780198565857.003.0004.CrossRefGoogle Scholar
Nunn, CL, Jordan, F, McCabe, CM, Verdolin, JL and Fewell, JH (2015) Infectious disease and group size: more than just a numbers game. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 370, 20140111.CrossRefGoogle ScholarPubMed
O'Donnell, S (1997) How parasites can promote the expression of social behaviour in their hosts. Proceedings of the Royal Society of London. Series B: Biological Sciences 264, 689–694.CrossRefGoogle Scholar
Owen-Ashley, NT and Wingfield, JC (2006) Seasonal modulation of sickness behavior in free-living northwestern song sparrows (Melospiza melodia morphna). Journal of Experimental Biology 209, 3062–3070.CrossRefGoogle Scholar
Parker, BJ, Barribeau, SM, Laughton, AM, de Roode, JC and Gerardo, NM (2011) Non-immunological defence in an evolutionary framework. Trends in Ecology & Evolution 26, 242–248.CrossRefGoogle Scholar
Patterson, JEH and Ruckstuhl, KE (2013) Parasite infection and host group size: a meta-analytical review. Parasitology 140, 803–813.CrossRefGoogle ScholarPubMed
Petkova, I, Abbey-Lee, RN and Løvlie, H (2018) Parasite infection and host personality: Glugea-infected three-spined sticklebacks are more social. Behavioral Ecology and Sociobiology 72, 1–9.CrossRefGoogle ScholarPubMed
Pharaon, J and Bauch, CT (2018) The influence of social behaviour on competition between virulent pathogen strains. Journal of Theoretical Biology 455, 47–53.CrossRefGoogle ScholarPubMed
Poirotte, C and Charpentier, MJE (2020) Unconditional care from close maternal kin in the face of parasites. Biology Letters 16, 20190869.CrossRefGoogle ScholarPubMed
Poirotte, C, Massot, F, Herbert, A, Willaume, E, Bomo, PM, Kappeler, PM and Charpentier, MJE (2017) Mandrills use olfaction to socially avoid parasitized conspecifics. Science Advances 3, e1601721.CrossRefGoogle ScholarPubMed
Poulin, R (2007) Evolutionary Ecology of Parasites, 2nd Edn Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Poulin, R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Advances in the Study of Behavior 41, 151–186.CrossRefGoogle Scholar
Poulin, R (2019) Modification of host social networks by manipulative parasites. Behaviour 155, 671–688.CrossRefGoogle Scholar
Powell, SN, Wallen, MM, Miketa, ML, Krzyszczyk, E, Foroughirad, V, Bansal, S and Mann, J (2020) Sociality and tattoo skin disease among bottlenose dolphins in Shark Bay, Australia. Behavioral Ecology 31, 459–466.CrossRefGoogle Scholar
Prado, F, Sheih, A, West, JD and Kerr, B (2009) Coevolutionary cycling of host sociality and pathogen virulence in contact networks. Journal of Theoretical Biology 261, 561–569.CrossRefGoogle ScholarPubMed
Rand, DA, Keeling, M and Wilson, HB (1995) Invasion, stability and evolution to criticality in spatially extended, artificial host–pathogen ecologies. Proceedings of the Royal Society of London. Series B: Biological Sciences 259, 55–63.Google Scholar
Ranta, E (1992) Gregariousness versus solitude: another look at parasite faunal richness in Canadian freshwater fishes. Oecologia 89, 150–152.CrossRefGoogle Scholar
Read, JM and Keeling, MJ (2003) Disease evolution on networks: the role of contact structure. Proceedings of the Royal Society of London. Series B: Biological Sciences 270, 699–708.CrossRefGoogle ScholarPubMed
Reckardt, K and Kerth, G (2009) Does the mode of transmission between hosts affect the host choice strategies of parasites? Implications from a field study on bat fly and wing mite infestation of Bechstein's bats. Oikos 118, 183–190.CrossRefGoogle Scholar
Rékási, J, Rózsa, L and Kiss, BJ (1997) Patterns in the distribution of avian lice (Phthiraptera: Amblycera. Ischnocera). Journal of Avian Biology 28, 150–156.CrossRefGoogle Scholar
Riehl, C (2011) Living with strangers: direct benefits favour non-kin cooperation in a communally nesting bird. Proceedings of the Royal Society of London. Series B: Biological Sciences 278, 1728–1735.Google Scholar
Rifkin, JL, Nunn, CL and Garamszegi, LZ (2012) Do animals living in larger groups experience greater parasitism? A meta-analysis. The American Naturalist 180, 70–82.CrossRefGoogle ScholarPubMed
Ripperger, SP, Stockmaier, S and Carter, GG (2020) Tracking sickness effects on social encounters via proximity-sensing in wild vampire bats. Behavioral Ecology. In Press.CrossRefGoogle Scholar
Rode, NO, Lievens, EJP, Flaven, E, Segard, A, Jabbour-Zahab, R, Sanchez, MI and Lenormand, T (2013) Why join groups? Lessons from parasite-manipulated Artemia. Ecology Letters 16, 493–501.CrossRefGoogle ScholarPubMed
Rogers, ME and Bates, PA (2007) Leishmania manipulation of sand fly feeding behavior results in enhanced transmission. PLoS Pathogens 3, e91.CrossRefGoogle ScholarPubMed
Romano, V, MacIntosh, AJJ and Sueur, C (2020) Stemming the flow: information, infection, and social evolution. Trends in Ecology & Evolution 35, 849–853.CrossRefGoogle ScholarPubMed
Rózsa, L, Rékási, J and Reiczigel, J (1996) Relationship of host coloniality to the population ecology of avian lice (Insecta: Phthiraptera). The Journal of Animal Ecology 65, 242–248.CrossRefGoogle Scholar
Russell, ST, Kelley, JL, Graves, JA and Magurran, AE (2004) Kin structure and shoal composition dynamics in the guppy, Poecilia reticulata. Oikos 106, 520–526.CrossRefGoogle Scholar
Sah, P, Mann, J and Bansal, S (2018) Disease implications of animal social network structure: a synthesis across social systems. Journal of Animal Ecology 87, 546–558.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P (2017) Parasites and their social hosts. Trends in Parasitology 33, 453–462.CrossRefGoogle ScholarPubMed
Seghers, B (1974) Schooling behavior in the guppy (Poecilia reticulata): an evolutionary response to predation. Evolution 28, 486–489.Google ScholarPubMed
Shakhar, K and Shakhar, G (2015) Why do we feel sick when infected – can altruism play a role? PLoS Biology 13, e1002276–15.CrossRefGoogle ScholarPubMed
Shaw, DJ, Grenfell, BT and Dobson, AP (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117(Pt 6), 597–610.CrossRefGoogle ScholarPubMed
Sheldon, BC and Verhulst, S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution 11, 317–321.CrossRefGoogle ScholarPubMed
Sherman, PW, Seeley, TD and Reeve, HK (1988) Parasites, pathogens, and polyandry in social Hymenoptera. The American Naturalist 131, 602–610.CrossRefGoogle Scholar
Shorter, JR and Rueppell, O (2012) A review on self-destructive defence behaviors in social insects. Insectes Sociaux 59, 1–10.CrossRefGoogle Scholar
Silk, MJ, Weber, NL, Steward, LC, Hodgson, DJ, Boots, M, Croft, DP, Delahay, RJ and McDonald, RA (2018) Contact networks structured by sex underpin sex-specific epidemiology of infection. Ecology Letters 21, 309–318.CrossRefGoogle ScholarPubMed
Siva-Jothy, JA and Vale, PF (2019) Viral infection causes sex-specific changes in fruit fly social aggregation behaviour. Biology Letters 15, 20190344.CrossRefGoogle ScholarPubMed
Snyder-Mackler, N, Burger, JR, Gaydosh, L, Belsky, DW, Noppert, GA, Campos, FA, Bartolomucci, A, Yang, YC, Aiello, AE, O'Rand, A, Harris, KM, Shively, CA, Alberts, SC and Tung, J (2020) Social determinants of health and survival in humans and other animals. Science (New York, N.Y.) 368, eaax9553.CrossRefGoogle ScholarPubMed
Spivak, M and Reuter, GS (2001) Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie 32, 555–565.CrossRefGoogle Scholar
Stephenson, JF (2019) Parasite-induced plasticity in host social behaviour depends on sex and susceptibility. Biology Letters 15, 20190557.CrossRefGoogle ScholarPubMed
Stephenson, JF and Reynolds, M (2016) Imprinting can cause a maladaptive preference for infectious conspecifics. Biology Letters 12, 20160020.CrossRefGoogle Scholar
Stephenson, JF, van Oosterhout, C, Mohammed, RS and Cable, J (2015) Parasites of Trinidadian guppies: evidence for sex- and age-specific trait-mediated indirect effects of predators. Ecology 96, 489–498.CrossRefGoogle ScholarPubMed
Stephenson, JF, Kinsella, C, Cable, J and van Oosterhout, C (2016) A further cost for the sicker sex? Evidence for male-biased parasite-induced vulnerability to predation. Ecology and Evolution 6, 2506–2515.CrossRefGoogle ScholarPubMed
Stephenson, JF, Perkins, SE and Cable, J (2018) Transmission risk predicts avoidance of infected conspecifics in Trinidadian guppies. Journal of Animal Ecology 87, 1525–1533.CrossRefGoogle ScholarPubMed
Stewart, AD, Logsdon, JM Jr and Kelley, SE (2005). An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59, 730–739.CrossRefGoogle ScholarPubMed
Stockmaier, S, Bolnick, DI, Page, RA and Carter, GG (2018) An immune challenge reduces social grooming in vampire bats. Animal Behaviour 140, 141–149.CrossRefGoogle Scholar
Stockmaier, S, Bolnick, DI, Page, RA, Josic, D and Carter, GG (2020 a) Immune-challenged vampire bats produce fewer contact calls. Biology Letters 16, 20200272.CrossRefGoogle ScholarPubMed
Stockmaier, S, Bolnick, DI, Page, RA and Carter, GG (2020 b) Sickness effects on social interactions depend on the type of behaviour and relationship. Journal of Animal Ecology 89, 1387–1394.CrossRefGoogle ScholarPubMed
Stroeymeyt, N, Grasse, AV, Crespi, A, Mersch, DP, Cremer, S and Keller, L (2018) Social network plasticity decreases disease transmission in a eusocial insect. Science (New York, N.Y.) 362, 941–945.CrossRefGoogle Scholar
Thompson, JN (2005) The Geographic Mosaic of Coevolution. Chicago, IL, USA: University of Chicago Press.CrossRefGoogle Scholar
Townsend, AK, Taff, CC, Wheeler, SS, Weis, AM, Hinton, MG, Jones, ML, Logsdon, RM, Reisen, WK, Freund, D, Sehgal, RNM, Saberi, M, Suh, YH, Hurd, J and Boyce, WM (2018) Low heterozygosity is associated with vector-borne disease in crows. Ecosphere (Washington, DC) 9, e02407.Google Scholar
Townsend, AK, Hawley, DM, Stephenson, JF and Williams, KEG (2020) Emerging infectious disease and the challenges of social distancing in human and non-human animals. Proceedings of the Royal Society of London. Series B: Biological Sciences 287, 20201039.Google ScholarPubMed
Turner, PE and Chao, L (1999) Prisoner's dilemma in an RNA virus. Nature 398, 441–443.CrossRefGoogle Scholar
Turner, PE, Cooper, VS and Lenski, RE (1998) Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Evolution 52, 315–329.CrossRefGoogle ScholarPubMed
Udiani, O and Fefferman, NH (2020) How disease constrains the evolution of social systems. Proceedings of the Royal Society of London. Series B: Biological Sciences 287, 20201284.Google ScholarPubMed
Van Baalen, M (2002) Contact networks and the evolution of virulence. In Diekmann, U, Metz, JAJ, Sabelis, MW and Sigmund, K (eds). Adaptive Dynamics of Infectious Diseases: In Pursuit of Virulence Management. Cambridge, UK: Cambridge University Press, pp. 85–103.CrossRefGoogle Scholar
VanderWaal, KL and Ezenwa, V (2016) Heterogeneity in pathogen transmission: mechanisms and methodology. Functional Ecology 30, 1606–1622.CrossRefGoogle Scholar
VanderWaal, KL, Obanda, V, Omondi, GP, McCowan, B, Wang, H, Fushing, H and Isbell, LA (2016) The ‘strength of weak ties’ and helminth parasitism in giraffe social networks. Behavioral Ecology 27, 1190–1197.CrossRefGoogle Scholar
van Schaik, J, Kerth, G, Bruyndonckx, N and Christe, P (2014) The effect of host social system on parasite population genetic structure: comparative population genetics of two ectoparasitic mites and their bat hosts. BMC Evolutionary Biology 14, 18.CrossRefGoogle ScholarPubMed
van Schaik, J, Dekeukeleire, D and Kerth, G (2015) Host and parasite life history interplay to yield divergent population genetic structures in two ectoparasites living on the same bat species. Molecular Ecology 24, 2324–2335.CrossRefGoogle ScholarPubMed
Viljakainen, L, Evans, JD, Hasselmann, M, Rueppell, O, Tingek, S and Pamilo, P (2009) Rapid evolution of immune proteins in social insects. Molecular Biology and Evolution 26, 1791–1801.CrossRefGoogle ScholarPubMed
Walker, TN and Hughes, WOH (2009) Adaptive social immunity in leaf-cutting ants. Biology Letters 5, 446–448.CrossRefGoogle ScholarPubMed
Weber, N, Bearhop, S, Dall, SRX, Delahay, RJ, McDonald, RA and Carter, SP (2013) Denning behaviour of the European badger (Meles meles) correlates with bovine tuberculosis infection status. Behavioral Ecology and Sociobiology 67, 471–479.CrossRefGoogle ScholarPubMed
Weinstein, SB, Buck, JC and Young, HS (2018) A landscape of disgust. Science (New York, N.Y.) 359, 1213–1214.CrossRefGoogle ScholarPubMed
White, LA, Forester, JD and Craft, ME (2018) Covariation between the physiological and behavioral components of pathogen transmission: host heterogeneity determines epidemic outcomes. Oikos 127, 538–552.CrossRefGoogle Scholar
Whiteman, NK and Parker, PG (2004) Effects of host sociality on ectoparasite population biology. The Journal of Parasitology 90, 939–947.CrossRefGoogle ScholarPubMed
Whitlock, MC and Barton, NH (1997) The effective size of a subdivided population. Genetics 146, 427–441.CrossRefGoogle ScholarPubMed
Wild, G, Gardner, A and West, SA (2009) Adaptation and the evolution of parasite virulence in a connected world. Nature 459, 983–986.CrossRefGoogle Scholar
Willette, AA, Lubach, GR and Coe, CL (2007) Environmental context differentially affects behavioral, leukocyte, cortisol, and interleukin-6 responses to low doses of endotoxin in the rhesus monkey. Brain, Behavior, and Immunity 21, 807–815.CrossRefGoogle ScholarPubMed
Woodroffe, R, Donnelly, CA, Wei, G, Cox, DR, Bourne, FJ, Burke, T, Butlin, RK, Cheeseman, CL, Gettinby, G, Gilks, P, Hedges, S, Jenkins, HE, Johnston, WT, McInerney, JP, Morrison, WI and Pope, LC (2009) Social group size affects Mycobacterium bovis infection in European badgers (Meles meles). Journal of Animal Ecology 78, 818–827.CrossRefGoogle Scholar
Zylberberg, M, Klasing, KC and Hahn, TP (2012) House finches (Carpodacus mexicanus) balance investment in behavioural and immunological defences against pathogens. Biology Letters 9, 20120856.CrossRefGoogle ScholarPubMed