1932

Abstract

Parasite avoidance is a host defense that reduces an individual's contact rate with parasites. We investigate avoidance as a primary driver of variation among individuals in their risk of parasitism and the evolution of host–parasite interactions. To bridge mechanistic and taxonomic divides, we define and categorize avoidance by its function and position in the sequence of host defenses. We also examine the role of avoidance in limiting epidemics and evaluate evidence for the processes that drive its evolution. Throughout, we highlight important directions in which to advance our conceptual and theoretical understanding of the role of avoidance in host–parasite interactions. We emphasize the need to test assumptions and quantify the effect of avoidance independent of other defenses. Importantly, many open questions may be most tractable in host systems that have not been the focus of traditional behavioral avoidance research, such as plants and invertebrates.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-102220-020636
2022-11-02
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/53/1/annurev-ecolsys-102220-020636.html?itemId=/content/journals/10.1146/annurev-ecolsys-102220-020636&mimeType=html&fmt=ahah

Literature Cited

  1. Abbot P, Dill LM. 2001. Sexually transmitted parasites and sexual selection in the milkweed leaf beetle. Labidomera clivicollis. Oikos 92:191–100
    [Google Scholar]
  2. Aiello CM, Nussear KE, Esque TC, Emblidge PG, Sah P et al. 2016. Host contact and shedding patterns clarify variation in pathogen exposure and transmission in threatened tortoise Gopherus agassizii: implications for disease modelling and management. J. Anim. Ecol. 85:3829–42
    [Google Scholar]
  3. Amoroso CR. 2021. Integrating concepts of physiological and behavioral resistance to parasites. Front. Ecol. Evol. 9:635607
    [Google Scholar]
  4. Amoroso CR, Antonovics J. 2020. Evolution of behavioural resistance in host–pathogen systems. Biol. Lett. 16:20200508
    [Google Scholar]
  5. Anderson RM, May RM. 1979. Population biology of infectious diseases: Part I. Nature 280:5721361–67
    [Google Scholar]
  6. Antonovics J, Wilson AJ, Forbes MR, Hauffe HC, Kallio ER et al. 2017. The evolution of transmission mode. Philos. Trans. R. Soc. B 372:171920160083
    [Google Scholar]
  7. Antonovics J, Thrall PH. 1994. The cost of resistance and the maintenance of genetic polymorphism in host–pathogen systems. Proc. R. Soc. B 257:1349105–10
    [Google Scholar]
  8. 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 372:171920160454
    [Google Scholar]
  9. Babin A, Kolly S, Schneider F, Dolivo V, Zini M, Kawecki TJ. 2014. Fruit flies learn to avoid odours associated with virulent infection. Biol. Lett. 10:2014004
    [Google Scholar]
  10. Bacot AW, Martin CJ. 1914. LXVII. Observations on the mechanism of the transmission of plague by fleas. J. Hyg. 13:Suppl.423–39
    [Google Scholar]
  11. Baines CB, Diab S, McCauley SJ. 2020. Parasitism risk and infection alter host dispersal. Am. Nat. 196:2119–31
    [Google Scholar]
  12. Bartlett LJ, Wilfert L, Boots M. 2018. A genotypic trade-off between constitutive resistance to viral infection and host growth rate. Evolution 72:2749–57
    [Google Scholar]
  13. Behringer DC, Butler MJ, Shields JD. 2006. Avoidance of disease by social lobsters. Nature 441:421
    [Google Scholar]
  14. Behringer DC, Karvonen A, Bojko J. 2018. Parasite avoidance behaviours in aquatic environments. Phil. Trans. R. Soc. B 373:20170202
    [Google Scholar]
  15. Ben-Horin T, Allen SK Jr., Small JM, Proestou DA 2018. Genetic variation in anti-parasite behavior in oysters. Mar. Ecol. Progress Ser. 594:107–17
    [Google Scholar]
  16. Biere A, Antonovics J. 1996. Sex-specific costs of resistance to the fungal pathogen Ustilago violacea (Microbotryum violaceum) in Silene alba. Evolution 50:31098–110
    [Google Scholar]
  17. Boillat M, Challet L, Rossier D, Kan C, Carleton A, Rodriguez I. 2015. The vomeronasal system mediates sick conspecific avoidance. Curr. Biol. 25:2251–55
    [Google Scholar]
  18. Boots M, Best A, Miller MR, White A. 2009. The role of ecological feedbacks in the evolution of host defence: What does theory tell us?. Philos. Trans. R. Soc. B 364:151327–36
    [Google Scholar]
  19. Boots M, Bowers RG. 1999. Three mechanisms of host resistance to microparasites—avoidance, recovery and tolerance—show different evolutionary dynamics. J. Theor. Biol. 201:113–23
    [Google Scholar]
  20. Bowers RG, Boots M, Begon M. 1994. Life-history trade-offs and the evolution of pathogen resistance: competition between host strains. Proc. R. Soc. B 257:1350247–53
    [Google Scholar]
  21. Boyer N, Réale D, Marmet J, Pisanu B, Chapuis JL. 2010. Personality, space use and tick load in an introduced population of Siberian chipmunks, Tamias sibiricus. . J. Anim. Ecol. 79:3538–47
    [Google Scholar]
  22. Buck JC, Weinstein SB, Young HS. 2018. Ecological and evolutionary consequences of parasite avoidance. Trends Ecol. Evol. 33:8619–32
    [Google Scholar]
  23. Buckling A, Rainey PB. 2002. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. B 269:1494931–36
    [Google Scholar]
  24. Bunke M, Alexander ME, Dick JTA, Hatcher MJ, Paterson R, Dunn AM. 2015. Eaten alive: cannibalism is enhanced by parasites. R. Soc. Open Sci. 2:3140369
    [Google Scholar]
  25. Butler MJ, Behringer DC, Dolan TW, Moss J, Shields JD. 2015. Behavioral immunity suppresses an epizootic in Caribbean spiny lobsters. PLOS ONE 10:6e0126374
    [Google Scholar]
  26. Candia-Zulbarán RI, Briones-Fourzán P, Lozano-Álvarez E, Barradas-Ortiz C, Negrete-Soto F. 2015. Caribbean spiny lobsters equally avoid dead and clinically PaV1-infected conspecifics. ICES J. Mar. Sci. 72:Suppl. 1i164–69
    [Google Scholar]
  27. Capinera JL, Kirouac SP, Barbosa P. 1976. Phagodeterrency of cadaver components to gypsy moth larvae, Lymantria dispar. . J. Invertebr. Pathol. 28:2277–79
    [Google Scholar]
  28. Carney WP. 1969. Behavioral and morphological changes in carpenter ants harboring Dicrocoeliid metacercariae. . Am. Midl. Nat. 82:2605–11
    [Google Scholar]
  29. Chaisson KE, Hallem EA. 2012. Chemosensory behaviors of parasites. Trends Parasitol. 28:10427–36
    [Google Scholar]
  30. Chang HC, Paek J, Kim DH. 2012. Natural polymorphisms in C. elegans HECW-1 E3 ligase affect pathogen avoidance behaviour. Nature 480:7378525–29
    [Google Scholar]
  31. Combes C. 2001. Parasitism: The Ecology and Evolution of Intimate Interactions Chicago: Univ. Chicago Press
  32. Curtis V, de Barra M, Aunger R. 2011. Disgust as an adaptive system for disease avoidance behaviour. Philos. Trans. R. Soc. B 366:1563389–401
    [Google Scholar]
  33. Curtis VA. 2014. Infection-avoidance behaviour in humans and other animals. Trends Immunol 35:10457–64
    [Google Scholar]
  34. Daly EW, Johnson PTJ. 2011. Beyond immunity: quantifying the effects of host anti-parasite behavior on parasite transmission. Oecologia 165:41043–50
    [Google Scholar]
  35. Daversa DR, Hechinger RF, Madin E, Fenton A, Dell AI et al. 2021. Broadening the ecology of fear: non-lethal effects arise from diverse responses to predation and parasitism. Proc. R. Soc. B 2881945:20202966
    [Google Scholar]
  36. de Roode JC, Lefèvre T. 2012. Behavioral immunity in insects. Insects 3:3789–820
    [Google Scholar]
  37. Dizney L, Dearing MD. 2013. The role of behavioural heterogeneity on infection patterns: implications for pathogen transmission. Anim. Behav. 86:5911–16
    [Google Scholar]
  38. Dobson A. 1995. The ecology and epidemiology of rinderpest virus in Serengeti and Ngorongoro Conservation Area. Serengeti II: Dynamics, Management, and Conservation of an Ecosystem ARE Sinclair, P Arcese 485–505 Chicago: Univ. Chicago Press
    [Google Scholar]
  39. Eakin L, Wang M, Dwyer G. 2015. The effects of the avoidance of infectious hosts on infection risk in an insect–pathogen interaction. Am. Nat. 185:1100–12
    [Google Scholar]
  40. Fenton A, Antonovics J, Brockhurst MA. 2012. Two-step infection processes can lead to coevolution between functionally independent infection and resistance pathways. Evolution 66:72030–41
    [Google Scholar]
  41. Ferguson NM, Laydon D, Nedjati-Gilani G, Imai N, Ainslie K et al. 2020. Report 9: Impact of non-pharmaceutical interventions (NPIs) to reduce COVID-19 mortality and healthcare demand. Rep., Imperial College COVID-19 Response Team, London. https://www.imperial.ac.uk/media/imperial-college/medicine/sph/ide/gida-fellowships/Imperial-College-COVID19-NPI-modelling-16-03-2020.pdf
  42. Fernández-Aparicio M, Kisugi T, Xie X, Rubiales D, Yoneyama K. 2014. Low strigolactone root exudation: a novel mechanism of broomrape (Orobanche and Phelipanche spp.) resistance available for faba bean breeding. J. Agric. Food Chem. 62:297063–71
    [Google Scholar]
  43. Fill A, Long EY, Finke DL. 2012. Non-consumptive effects of a natural enemy on a non-prey herbivore population. Ecol. Entomol. 37:143–50
    [Google Scholar]
  44. Frank SA. 1993. Coevolutionary genetics of plants and pathogens. Evol. Ecol. 7:145–75
    [Google Scholar]
  45. Freeland WJ. 1976. Pathogens and the evolution of primate sociality. Biotropica 8:112–24
    [Google Scholar]
  46. Fujita N, Koda R. 2015. Capitulum and rosette leaf avoidance from grazing by large herbivores in Taraxacum. Ecol. Res. 30:3517–25
    [Google Scholar]
  47. Gaynor KM, Brown JS, Middleton AD, Power ME, Brashares JS. 2019. Landscapes of fear: spatial patterns of risk perception and response. Trends Ecol. Evol. 34:435568
    [Google Scholar]
  48. Hall MD, Bento G, Ebert D. 2017. The evolutionary consequences of stepwise infection processes. Trends Ecol. Evol. 32:8612–23
    [Google Scholar]
  49. Hart BL. 2011. Behavioural defences in animals against pathogens and parasites: parallels with the pillars of medicine in humans. Philos. Trans. R. Soc. B 366:3406–17
    [Google Scholar]
  50. Hawley DM, Etienne RS, Ezenwa VO, Jolles AE. 2011. Does animal behavior underlie covariation between hosts’ exposure to infectious agents and susceptibility to infection? Implications for disease dynamics. Integr. Comp. Biol. 51:4528–39
    [Google Scholar]
  51. Hawley DM, Gibson AK, Townsend AK, Craft ME, Stephenson JF. 2021. Bidirectional interactions between host social behaviour and parasites arise through ecological and evolutionary processes. Parasitology 148:3274–88
    [Google Scholar]
  52. Hendry TA, Ligon RA, Besler KR, Fay RL, Smee MR. 2018. Visual detection and avoidance of pathogenic bacteria by aphids. Curr. Biol. 28:193158–64.e4
    [Google Scholar]
  53. Hethcote HW, Yorke JA. 1984. Gonorrhea Transmission Dynamics and Control Heidelberg, Ger: Springer
  54. Hewlett BS, Amola RP. 2003. Cultural contexts of Ebola in northern Uganda. Emerg. Infect. Dis. 9:101242–48
    [Google Scholar]
  55. Hoyle A, Bowers RG, White A, Boots M. 2008. The influence of trade-off shape on evolutionary behaviour in classical ecological scenarios. J. Theor. Biol. 250:3498–511
    [Google Scholar]
  56. Hutchings MR, Athanasiadou S, Kyriazakis I, Gordon IJ. 2003. Can animals use foraging behaviour to combat parasites?. Proc. Nutr. Soc. 62:2361–70
    [Google Scholar]
  57. Hutchings MR, Knowler KJ, McAnulty R, McEwan JC. 2007. Genetically resistant sheep avoid parasites to a greater extent than do susceptible sheep. Proc. R. Soc. B 274:16201839–44
    [Google Scholar]
  58. Hutchings MR, Kyriazakis I, Gordon IJ. 2001. Herbivore physiological state affects foraging trade-off decisions between nutrient intake and parasite avoidance. Ecology 82:41138–50
    [Google Scholar]
  59. Jefferies D, Livesey JL, Molyneux DH. 1986. Fluid mechanics of bloodmeal uptake by Leishmania-infected sandflies. Acta Trop 43:143–53
    [Google Scholar]
  60. Jørgensen RJ, Rønne H, Helsted C, Iskander AR. 1982. Spread of infective Dictyocaulus viviparus larvae in pasture and to grazing cattle: experimental evidence of the role of Pilobolus fungi. Vet. Parasitol. 10:4331–39
    [Google Scholar]
  61. Kavaliers M, Choleris E, Colwell DD. 2001. Learning from others to cope with biting flies: social learning of fear-induced conditioned analgesia and active avoidance. Behav. Neurosci. 115:661–74
    [Google Scholar]
  62. Kavaliers M, Choleris E, Pfaff DW. 2005. Genes, odours and the recognition of parasitized individuals by rodents. Trends Parasitol 21:9423–29
    [Google Scholar]
  63. Kavaliers M, Ossenkopp KP, Choleris E. 2019. Social neuroscience of disgust. Genes Brain Behav 18:1e12508
    [Google Scholar]
  64. Kiesecker JM, Skelly DK, Beard KH, Preisser E. 1999. Behavioral reduction of infection risk. PNAS 96:August9165–68
    [Google Scholar]
  65. Klemme I, Hyvärinen P, Karvonen A. 2020. Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations. Proc. R. Soc. B 2871925:20200388
    [Google Scholar]
  66. Klemme I, Karvonen A. 2017. Vertebrate defense against parasites: interactions between avoidance, resistance, and tolerance. Ecol. Evol. 7:2561–71
    [Google Scholar]
  67. Knell RJ. 1999. Sexually transmitted disease and parasite-mediated sexual selection. Evolution 53:4957–61
    [Google Scholar]
  68. Kohler SL, McPeek MA. 1989. Predation risk and the foraging behavior of competing stream insects. Ecology 70:61811–25
    [Google Scholar]
  69. Koprivnikar J, Penalva L. 2015. Lesser of two evils? Foraging choices in response to threats of predation and parasitism. PLOS ONE 10:1e0116569
    [Google Scholar]
  70. Kotler BP, Brown JS, Hasson O. 1991. Factors affecting gerbil foraging behavior and rates of owl predation. Ecology 72:62249–60
    [Google Scholar]
  71. Kraaijeveld AR, Godfray HCJ. 1997. Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. . Nature 389:6648278–80
    [Google Scholar]
  72. Lafferty KD, Kuris AM. 2002. Trophic strategies, animal diversity and body size. Trends Ecol. Evol. 17:11507–13
    [Google Scholar]
  73. Lefèvre T, De Roode JC, Kacsoh BZ, Schlenke TA. 2012. Defence strategies against a parasitoid wasp in Drosophila: fight or flight?. Biol. Lett. 8:2230–33
    [Google Scholar]
  74. Lello J, Fenton A. 2017. Lost in transmission…?. Philos. Trans. R. Soc. B 372:171920160082
    [Google Scholar]
  75. Lev-Yadun S. 2021. Avoiding rather than resisting herbivore attacks is often the first line of plant defence. Biol. J. Linn. Soc. Lond. 134:4775–802
    [Google Scholar]
  76. Lewkiewicz DA, Zuk M. 2004. Latency to resume calling after disturbance in the field cricket, Teleogryllus oceanicus, corresponds to population-level differences in parasitism risk. Behav. Ecol. Sociobiol. 55:6569–73
    [Google Scholar]
  77. Lima SL, Dill LM. 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68:4619–40
    [Google Scholar]
  78. Lloyd-Smith JO, Schreiber SJ, Getz WM 2006. Moving beyond averages: Individual-level variation in disease transmission. Mathematical Studies on Human Disease Dynamics: Emerging Paradigms and Challenges AB Gumel, C Castillo-Chavez, RE Mickens, DP Clemence, pp. 235–58. Contemp. Math. 410 Providence, RI: AMS Books
    [Google Scholar]
  79. Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM. 2005. Superspreading and the effect of individual variation on disease emergence. Nature 438:7066355–59
    [Google Scholar]
  80. Loehle C. 1995. Social barriers to pathogen transmission in wild animal populations. Ecology 76:2326–35
    [Google Scholar]
  81. Lopes PC. 2017. Why are behavioral and immune traits linked?. Horm. Behav. 88:52–59
    [Google Scholar]
  82. Luong LT, Horn CJ, Brophy T. 2017. Mitey costly: energetic costs of parasite avoidance and infection. Physiol. Biochem. Zool. 90:4471–77
    [Google Scholar]
  83. Luong LT, Kaya HK. 2005. Sexually transmitted parasites and host mating behavior in the decorated cricket. Behav. Ecol. 16:4794–99
    [Google Scholar]
  84. Lynch ZR, Schlenke TA, de Roode JC. 2016. Evolution of behavioural and cellular defences against parasitoid wasps in the Drosophila melanogaster subgroup. J. Evol. Biol. 29:51016–29
    [Google Scholar]
  85. Marino JA Jr., Werner EE. 2013. Synergistic effects of predators and trematode parasites on larval green frog (Rana clamitans) survival. Ecology 94:122697–708
    [Google Scholar]
  86. Meaden S, Paszkiewicz K, Koskella B. 2015. The cost of phage resistance in a plant pathogenic bacterium is context-dependent. Evolution 69:51321–28
    [Google Scholar]
  87. Meisel JD, Kim DH. 2014. Behavioral avoidance of pathogenic bacteria by Caenorhabditis elegans. . Trends Immunol 35:10465–70
    [Google Scholar]
  88. Mikheev VN, Pasternak AF, Valtonen ET. 2015. Behavioural adaptations of argulid parasites (Crustacea: Branchiura) to major challenges in their life cycle. Parasit. Vectors. 8:394
    [Google Scholar]
  89. Nakad R, Snoek LB, Yang W, Ellendt S, Schneider F et al. 2016. Contrasting invertebrate immune defense behaviors caused by a single gene, the Caenorhabditis elegans neuropeptide receptor gene npr-1. BMC Genom. 17:1280
    [Google Scholar]
  90. Paciência F, Rushmore J, Chuma IS, Lipende IF, Caillaud D et al. 2019. Mating avoidance in female olive baboons (Papio anubis) infected by Treponema pallidum. Sci. Adv. 5:12eaaw9724
    [Google Scholar]
  91. Parker BJ, Elderd BD, Dwyer G. 2010. Host behaviour and exposure risk in an insect–pathogen interaction. J. Anim. Ecol. 79:4863–70
    [Google Scholar]
  92. Pascoal S, Cezard T, Eik-Nes A, Gharbi K, Majewska J et al. 2014. Rapid convergent evolution in wild crickets. Curr. Biol. 24:121369–74
    [Google Scholar]
  93. Penley MJ, Greenberg AB, Khalid A, Namburar SR, Morran LT. 2018. No measurable fitness cost to experimentally evolved host defence in the Caenorhabditis elegansSerratia marcescens host–parasite system. J. Evol. Biol. 31:121976–81
    [Google Scholar]
  94. Penley MJ, Ha GT, Morran LT. 2017. Evolution of Caenorhabditis elegans host defense under selection by the bacterial parasite Serratia marcescens. . PLOS ONE 12:8e0181913
    [Google Scholar]
  95. Penley MJ, Morran LT. 2018. Host mating system and coevolutionary dynamics shape the evolution of parasite avoidance in Caenorhabditis elegans host populations. Parasitology 145:724–30
    [Google Scholar]
  96. Poirotte C, Massol F, Herbert A, Willaume E, Bomo PM et al. 2017. Mandrills use olfaction to socially avoid parasitized conspecifics. Sci. Adv. 3:4e1601721
    [Google Scholar]
  97. Pradel E, Zhang Y, Pujol N, Matsuyama T, Bargmann CI, Ewbank JJ. 2007. Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. PNAS 104:72295–300
    [Google Scholar]
  98. Råberg L, Graham AL, Read AF. 2009. Decomposing health: tolerance and resistance to parasites in animals. Philos. Trans. R. Soc. B 364:151337–49
    [Google Scholar]
  99. Rigby MC, Hechinger RF, Stevens L. 2002. Why should parasite resistance be costly?. Trends Parasitol 18:3116–20
    [Google Scholar]
  100. Robert C, Garin G, Abichou M, Houlès V, Pradal C, Fournier C. 2018. Plant architecture and foliar senescence impact the race between wheat growth and Zymoseptoria tritici epidemics. Ann. Bot. 121:5975–89
    [Google Scholar]
  101. Robinson J. 1962. Pilobolus spp. and the translation of the infective larvae of Dictyocaulusviviparus from faeces to pastures. Nature 193:4813353–54
    [Google Scholar]
  102. Rotundo JL, Aguiar MR. 2007. Herbivory resistance traits in populations of Poa ligularis subjected to historically different sheep grazing pressure in Patagonia. Plant Ecol 194:1121–33
    [Google Scholar]
  103. Rozin P, Fallon AE. 1987. A perspective on disgust. Psychol. Rev. 94:123–41
    [Google Scholar]
  104. Sauge MH, Mus F, Lacroze JP, Pascal T, Kervella J, Poëssel JL. 2006. Genotypic variation in induced resistance and induced susceptibility in the peach–Myzus persicae aphid system. Oikos 113:2305–313
    [Google Scholar]
  105. Sarabian C, Curtis V, McMullan R. 2018. Evolution of pathogen and parasite avoidance behaviours. Philos. Trans. R. Soc. B 373:175120170256
    [Google Scholar]
  106. Sarabian C, MacIntosh AJJ. 2015. Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques. Biol. Lett. 11:20150757
    [Google Scholar]
  107. Sarabian C, Ngoubangoye B, MacIntosh AJJ. 2017. Avoidance of biological contaminants through sight, smell and touch in chimpanzees. R. Soc. Open Sci. 4:170968
    [Google Scholar]
  108. Schmid-Hempel P. 2011. Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics Oxford, UK: Oxford Univ. Press
  109. Sercu BK, Moeneclaey I, Bonte D, Baeten L. 2020. Induced phenological avoidance: a neglected defense mechanism against seed predation in plants. J. Ecol. 108:31115–24
    [Google Scholar]
  110. Shook NJ, Thomas R, Ford CG 2019. Testing the relation between disgust and general avoidance behavior. Pers. Individ. Differ. 150:July109457
    [Google Scholar]
  111. Sillero JC, Moreno MT, Rubiales D. 2005. Sources of resistance to crenate broomrape among species of Vicia. . Plant Dis 89:123–27
    [Google Scholar]
  112. Stephenson JF, Perkins SE, Cable J. 2018. Transmission risk predicts avoidance of infected conspecifics in Trinidadian guppies. J. Anim. Ecol. 87:61525–33
    [Google Scholar]
  113. Stockmaier S, Bolnick DI, Page RA, Carter GG. 2020. Sickness effects on social interactions depend on the type of behaviour and relationship. J. Anim. Ecol. 89:61387–94
    [Google Scholar]
  114. Stockmaier S, Stroeymeyt N, Shattuck EC, Hawley DM, Meyers LA, Bolnick DI. 2021. Infectious diseases and social distancing in nature. Science 371:6533eabc8881
    [Google Scholar]
  115. Strauss AT, Hite JL, Civitello DJ, Shocket MS, Cáceres CE, Hall SR. 2019. Genotypic variation in parasite avoidance behaviour and other mechanistic, nonlinear components of transmission. Proc. R. Soc. B 2861915:20192164
    [Google Scholar]
  116. Stroeymeyt N, Grasse AV, Crespi A, Mersch DP, Cremer S, Keller L. 2018. Social network plasticity decreases disease transmission in a eusocial insect. Science 362:6417941–45
    [Google Scholar]
  117. Suárez-Rodríguez M, Garcia CM. 2017. An experimental demonstration that house finches add cigarette butts in response to ectoparasites. J. Avian Biol. 48:101316–21
    [Google Scholar]
  118. Suárez-Rodríguez M, López-Rull I, Garcia CM. 2013. Incorporation of cigarette butts into nests reduces nest ectoparasite load in urban birds: new ingredients for an old recipe?. Biol. Lett. 9:120120931
    [Google Scholar]
  119. Suffert F, Sache I, Lannou C. 2011. Early stages of septoria tritici blotch epidemics of winter wheat: build-up, overseasoning, and release of primary inoculum. Plant Pathol 60:2166–77
    [Google Scholar]
  120. Tavella CM. 1978. Date of heading and plant height of wheat varieties, as related to septoria leaf blotch damage. Euphytica 27:2577–80
    [Google Scholar]
  121. Taylor CN, Oseen KL, Wassersug RJ. 2004. On the behavioural response of Rana and Bufo tadpoles to echinostomatoid cercariae: implications to synergistic factors influencing trematode infections in anurans. Can. J. Zool. 82:5701–6
    [Google Scholar]
  122. Taylor EL. 1954. Grazing behaviour and helminthic disease. Br. J. Anim. Behav. 2:261–62
    [Google Scholar]
  123. Thomas F, Poulin R. 1998. Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance?. Parasitology 116:Part 5431–36
    [Google Scholar]
  124. Tiffin P. 2000. Mechanisms of tolerance to herbivore damage: What do we know?. Evol. Ecol. 14:4–6523–36
    [Google Scholar]
  125. Tybur JM, Lieberman D, Kurzban R, DeScioli P. 2013. Disgust: evolved function and structure. Psychol. Rev. 120:165–84
    [Google Scholar]
  126. van der Wal R, Irvine J, Stien A, Shepherd N, Albon SD. 2000. Faecal avoidance and the risk of infection by nematodes in a natural population of reindeer. Oecologia 124:19–25
    [Google Scholar]
  127. van Schaik J, Kerth G, Bruyndonckx N, 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 Evol. Biol. 14:18
    [Google Scholar]
  128. Velagapudi P, Ghoubrial R, Shah R, Ghali H, Haas M et al. 2020. A potential tradeoff between feeding rate and aversive learning determines intoxication in a Caenorhabditis elegans host-pathogen system. Microbes Infect 22:8340–48
    [Google Scholar]
  129. Walsh PT, McCreless E, Pedersen AB. 2013. Faecal avoidance and selective foraging: Do wild mice have the luxury to avoid faeces ?. Anim. Behav. 86:559–66
    [Google Scholar]
  130. White PS, Penley MJ, Tierney ARP, Soper DM, Morran LT. 2019. Dauer life stage of Caenorhabditis elegans induces elevated levels of defense against the parasite Serratia marcescens. Sci. Rep. 9:11575
    [Google Scholar]
  131. Wilson DS, Coleman K, Clark AB, Biederman L. 1993. Shy-bold continuum in pumpkinseed sunfish (Lepomis gibbosus): an ecological study of a psychological trait. J. Comp. Psychol. 107:3250–60
    [Google Scholar]
  132. Yousefi B, Fouks B. 2019. The presence of a larval honey bee parasite, Ascosphaera apis, on flowers reduces pollinator visitation to several plant species. Acta Oecol 96:49–55
    [Google Scholar]
  133. Zhang Y, Lu H, Bargmann CI. 2005. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. . Nature 438:7065179–84
    [Google Scholar]
  134. Zuk M, Rotenberry JT, Tinghitella RM. 2006. Silent night: adaptive disappearance of a sexual signal in a parasitized population of field crickets. Biol. Lett. 2:4521–24
    [Google Scholar]
  135. Zylberberg M, Klasing KC, Hahn TP. 2013. House finches (Carpodacus mexicanus) balance investment in behavioural and immunological defences against pathogens. Biol. Lett. 9:120120856
    [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-102220-020636
Loading
/content/journals/10.1146/annurev-ecolsys-102220-020636
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error