Migration and tolerance shape host behaviour and response to parasite infection.

Dongmin Kim, Allison K Shaw
Author Information
  1. Dongmin Kim: Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN, USA. ORCID
  2. Allison K Shaw: Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN, USA. ORCID

Abstract

Numerous theoretical models have demonstrated that migration, a seasonal animal movement behaviour, can minimize the risks and costs of parasite infection. Past work on migration-infection interactions assumes migration is the only strategy available to organisms for dealing with the parasite infection, that is they migrate to a different environment to recover or escape from infection. Thus, migration is similar to the non-spatial strategy of resistance, where hosts prevent infection or kill parasites once infected. However, an alternative defence strategy is to tolerate the infection and experience a lower cost to the infection. To our knowledge, no studies have examined how migration can change based on combining two host strategies (migration and tolerance) for dealing with parasites. In this paper, we aim to understand how both parasite transmission and infection tolerance can influence the host's migratory behaviour. We constructed a model that incorporates two host strategies (migration and tolerance) to understand whether allowing for tolerance affects the proportion of the population that migrates at equilibrium in response to infection. We show that the benefits of tolerance can either decrease or increase the host's migration. Also, if the benefit of migration is great, then individuals are more likely to migrate regardless of the presence of tolerance. Finally, we find that the transmission rate of parasite infection can either decrease or increase the tolerant host's migration, depending on the cost of migration. These findings highlight that adopting two defence strategies is not always beneficial to the hosts. Instead, a single strategy is often better, depending on the costs and benefits of the strategies and infection pressures. Our work further suggests that multiple host-defence strategies as a potential explanation for the evolution of migration to minimize the parasite infection. Moreover, migration can also affect the ecological and evolutionary dynamics of parasite-host interactions.

Keywords

References

  1. Altizer, S., Bartel, R., & Han, B. (2011). Animal migration and infectious disease risk. Science, 331(6015), 296-302. https://doi.org/10.1126/science.1194694
  2. Bartel, R., Oberhauser, K., De Roode, J., & Altizer, S. (2011). Monarch butterfly migration and parasite transmission in eastern North America. Ecology, 92(2), 342-351. https://doi.org/10.1890/10-0489.1
  3. Best, A., White, A., & Boots, M. (2008). Maintenance of host variation in tolerance to pathogens and parasites. Proceedings of the National Academy of Sciences of the United States of America, 105(52), 20786-20791. https://doi.org/10.1073/pnas.0809558105
  4. Blanchet, S., Rey, O., & Loot, G. (2010). Evidence for host variation in parasite tolerance in a wild fish population. Evolutionary Ecology, 24(5), 1129-1139. https://doi.org/10.1007/s10682-010-9353-x
  5. Boots, M., Best, A., Miller, M., & White, A. (2009). The role of ecological feedbacks in the evolution of host defence: What does theory tell us? Philosophical Transactions of the Royal Society B: Biological Sciences, 364(1513), 27-36. https://doi.org/10.1098/rstb.2008.0160
  6. Boots, M., & Bowers, R. (1999). Three mechanisms of host resistance to microparasites - Avoidance, recovery and tolerance - Show different evolutionary dynamics. Journal of Theoretical Biology, 201(1), 13-23. https://doi.org/10.1006/jtbi.1999.1009
  7. Bradley, C., & Altizer, S. (2005). Parasites hinder monarch butterfly flight: Implications for disease spread in migratory hosts. Ecology Letters, 8(3), 290-300. https://doi.org/10.1111/j.1461-0248.2005.00722.x
  8. Budischak, S. A., & Cressler, C. E. (2018). Fueling defense: Effects of resources on the ecology and evolution of tolerance to parasite infection. Frontiers in Immunology, 9, 2453. https://doi.org/10.3389/fimmu.2018.02453
  9. Burgan, S. C., Gervasi, S. S., Johnson, L. R., & Martin, L. B. (2019). How individual variation in host tolerance affects competence to transmit parasites. Physiological and Biochemical Zoology, 92(1), 49-57. https://doi.org/10.1086/701169
  10. Casadevall, A., & Pirofski, L. A. (1999). Host-pathogen interactions: Redefining the basic concepts of virulence and pathogenicity. Infection and Immunity, 67(8), 3703-3713. https://doi.org/10.1128/IAI.67.8.3703-3713.1999
  11. Duffy, M. A., & Forde, S. E. (2009). Ecological feedbacks and the evolution of resistance. Journal of Animal Ecology, 78(6), 1106-1112. https://doi.org/10.1111/j.1365-2656.2009.01568.x
  12. Duffy, M. A., Ochs, J. H., Penczykowski, R. M., Civitello, D. J., Klausmeier, C. A., & Hall, S. R. (2012). Ecological context influences epidemic size and parasite-driven evolution. Science, 335(6076), 1636-1638. https://doi.org/10.1126/science.1215429
  13. Ferris, C., Wright, R., Brockhurst, M. A., & Best, A. (2020). The evolution of host resistance and parasite infectivity is highest in seasonal resource environments that oscillate at intermediate amplitudes. Proceedings of the Royal Society B: Biological Sciences, 287(1927), 20200787. https://doi.org/10.1098/rspb.2020.0787
  14. Frank, S. A. (1996). Models of parasite virulence. The Quarterly review of biology, 71(1), 37-78.
  15. Gandon, S., van Baalen, M., & Jansen, V. A. (2002). The evolution of parasite virulence, superinfection, and host resistance. The American Naturalist, 159(6), 658-669. https://doi.org/10.1086/339993
  16. Grab, K., Hiller, B., Hurlbert, J., Ingram, M., Parker, A., Pokutnaya, D., & Knutie, S. (2019). Host tolerance and resistance to parasitic nest flies differs between two wild bird species. Ecology and Evolution, 9(21), 12144-12155. https://doi.org/10.1002/ece3.5682
  17. Hall, R., Altizer, S., & Bartel, R. (2014). Greater migratory propensity in hosts lowers pathogen transmission and impacts. Journal of Animal Ecology, 83(5), 1068-1077. https://doi.org/10.1111/1365-2656.12204
  18. Halttunen, E., Gjelland, K.-Ø., Hamel, S., Serra-Llinares, R.-M., Nilsen, R., Arechavala-Lopez, P., Skarðhamar, J., Johnsen, I. A., Asplin, L., Karlsen, Ø., Bjørn, P.-A., & Finstad, B. (2018). Sea trout adapt their migratory behaviour in response to high salmon lice concentrations. Journal of Fish Diseases, 41(6), 953-967. https://doi.org/10.1111/jfd.12749
  19. Hegemann, A., Alcalde Abril, P., Sjöberg, S., Muheim, R., Alerstam, T., Nilsson, J.-Å., & Hasselquist, D. (2018). A mimicked bacterial infection prolongs stopover duration in songbirds-but more pronounced in short- than long-distance migrants. Journal of Animal Ecology, 87(6), 1698-1708. https://doi.org/10.1111/1365-2656.12895
  20. Iritani, R., & Iwasa, Y. (2014). Parasite infection drives the evolution of state-dependent dispersal of the host. Theoretical Population Biology, 92, 1-13. https://doi.org/10.1016/j.tpb.2013.10.005
  21. Karvonen, A., Kristjánsson, B. K., Skúlason, S., Lanki, M., Rellstab, C., & Jokela, J. (2013). Water temperature, not fish morph, determines parasite infections of sympatric Icelandic threespine sticklebacks (Gasterosteus aculeatus). Ecology and Evolution, 3(6), 1507-1517. https://doi.org/10.1002/ece3.568
  22. Kim, D., & Shaw, A. (2021). Data from: Migration and tolerance shape host behaviour and response to parasite infection. Dryad Digital Repository, https://doi.org/10.5061/dryad.nzs7h44rg
  23. Klemme, I., Hyvärinen, P., & Karvonen, A. (2020). Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations. Proceedings of the Royal Society B: Biological Sciences, 287(1925), 20200388. https://doi.org/10.1098/rspb.2020.0388
  24. Klemme, I., & Karvonen, A. (2017). Vertebrate defense against parasites: Interactions between avoidance, resistance, and tolerance. Ecology and Evolution, 7(2), 561-571. https://doi.org/10.1002/ece3.2645
  25. Knutie, S. (2018). Relationships among introduced parasites, host defenses, and gut microbiota of Galapagos birds. Ecosphere, 9(5), e02286. https://doi.org/10.1002/ecs2.2286
  26. Knutie, S. A., Wilkinson, C. L., Wu, Q. C., Ortega, C. N., & Rohr, J. R. (2017). Host resistance and tolerance of parasitic gut worms depend on resource availability. Oecologia, 183(4), 1031-1040. https://doi.org/10.1007/s00442-017-3822-7
  27. Kurze, C., Routtu, J., & Moritz, R. F. (2016). Parasite resistance and tolerance in honeybees at the individual and social level. Zoology, 119(4), 290-297. https://doi.org/10.1016/j.zool.2016.03.007
  28. Landsberg, J., Vermeer, G., Richards, S., & Perry, N. (1991). Control of the parasitic copepod Caligus elongatus on pond-reared red drum. Journal of Aquatic Animal Health, 3(3), 206-209. https://doi.org/10.1577/1548-8667(1991)003<0206:COTPCC>2.3.CO;2
  29. Li, W., Song, R., Wu, S., Zou, H., Nie, P., & Wang, G. (2011). Seasonal occurrence of helminths in the anadromous fish Coilia nasus (Engraulidae): Parasite indicators of fish migratory movements. Journal of Parasitology, 97(2), 192-196. https://doi.org/10.1645/GE-2621.1
  30. Lion, S., & Metz, J. A. (2018). Beyond R0 maximisation: On pathogen evolution and environmental dimensions. Trends in Ecology & Evolution, 33(6), 458-473. https://doi.org/10.1016/j.tree.2018.02.004
  31. Loehle, C. (1995). Social barriers to pathogen transmission in wild animal populations. Ecology, 76(2), 326-335. https://doi.org/10.2307/1941192
  32. Malenke, J. R., Newbold, N., & Clayton, D. H. (2011). Condition-specific competition governs the geographic distribution and diversity of ectoparasites. The American Naturalist, 177(4), 522-534. https://doi.org/10.1086/658176
  33. Miller, M., White, A., & Boots, M. (2006). The evolution of parasites in response to tolerance in their hosts: The good, the bad, and apparent commensalism. Evolution, 60(5), 945. https://doi.org/10.1111/j.0014-3820.2006.tb01173.x
  34. Moyer, B., Drown, D., & Clayton, D. (2002). Low humidity reduces ectoparasite pressure: Implications for host life-history evolution. Oikos, 97(2), 223-228. https://doi.org/10.1034/j.1600-0706.2002.970208.x
  35. Moyer, B. R., & Wagenbach, G. E. (1995). Sunning by Black Noddies (Anous minutus) may kill chewing lice (Quadraceps hopkinsi). The Auk, 112(4), 1073-1077. https://doi.org/10.2307/4089047
  36. Peacock, S., Bouhours, J., Lewis, M., & Molnár, P. (2018). Macroparasite dynamics of migratory host populations. Theoretical Population Biology, 120, 29-41. https://doi.org/10.1016/j.tpb.2017.12.005
  37. Penczykowski, R. M., Laine, A. L., & Koskella, B. (2016). Understanding the ecology and evolution of host-parasite interactions across scales. Evolutionary Applications, 9(1), 37-52. https://doi.org/10.1111/eva.12294
  38. Råberg, L. (2014). How to live with the enemy: Understanding tolerance to parasites. PLoS Biology, 12(11), e1001989. https://doi.org/10.1371/journal.pbio.1001989
  39. Råberg, L., Sim, D., & Read, A. (2007). Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science, 318(5851), 812-814. https://doi.org/10.1126/science.1148526
  40. Restif, O., & Koella, J. C. (2003). Shared control of epidemiological traits in a coevolutionary model of host-parasite interactions. The American Naturalist, 161(6), 827-836. https://doi.org/10.1086/375171
  41. Restif, O., & Koella, J. C. (2004). Concurrent evolution of resistance and tolerance to pathogens. The American Naturalist, 164(4), E90-E102. https://doi.org/10.1086/423713
  42. Ricker, W. E. (1975). Computation and interpretation of biological statistics of fish populations. Bulletin - Fisheries Research Board of Canada, 191, 1-382.
  43. Rohr, J., Raffel, T., & Hall, C. (2010). Developmental variation in resistance and tolerance in a multi-host-parasite system. Functional Ecology, 24(5), 1110-1121. https://doi.org/10.1111/j.1365-2435.2010.01709.x
  44. Sears, B. F., Snyder, P. W., & Rohr, J. R. (2015). Host life history and host-parasite syntopy predict behavioural resistance and tolerance of parasites. Journal of Animal Ecology, 84(3), 625-636. https://doi.org/10.1111/1365-2656.12333
  45. Shaw, A., & Binning, S. (2016). Migratory recovery from infection as a selective pressure for the evolution of migration. The American Naturalist, 187(4), 502-516. https://doi.org/10.1086/685386
  46. Shaw, A., Craft, M., Zuk, M., & Binning, S. (2019). Host migration strategy is shaped by forms of parasite transmission and infection cost. Journal of Animal Ecology, 88(10), 1601-1612. https://doi.org/10.1111/1365-2656.13050
  47. Stowe, K. A. (1998). Experimental evolution of resistance in Brassica rapa: Correlated response of tolerance in lines selected for glucosinolate content. Evolution, 52(3), 703-712. https://doi.org/10.1111/j.1558-5646.1998.tb03695.x
  48. Teitelbaum, C., Huang, S., Hall, R., & Altizer, S. (2018). Migratory behaviour predicts greater parasite diversity in ungulates. Proceedings of the Royal Society B: Biological Sciences, 285(1875), 20180089. https://doi.org/10.1098/rspb.2018.0089
  49. Thieltges, D. W., Dolch, T., Krakau, M., & Poulin, R. (2010). Salinity gradient shapes distance decay of similarity among parasite communities in three marine fishes. Journal of Fish Biology, 76(7), 1806-1814. https://doi.org/10.1111/j.1095-8649.2010.02618.x
  50. Vale, P. F., Wilson, A. J., Best, A., Boots, M., & Little, T. J. (2011). Epidemiological, evolutionary, and coevolutionary implications of context-dependent parasitism. The American Naturalist, 177(4), 510-521. https://doi.org/10.1086/659002
  51. van Baalen, M. (1998). Coevolution of recovery ability and virulence. Proceedings of the Royal Society of London. Series B: Biological Sciences, 265(1393), 317-325. https://doi.org/10.1098/rspb.1998.0298
  52. Zeller, M., & Koella, J. C. (2017). The role of the environment in the evolution of tolerance and resistance to a pathogen. The American Naturalist, 190(3), 389-397. https://doi.org/10.1086/692759
  53. Zuk, M., & Stoehr, A. (2002). Immune defense and host life history. The American Naturalist, 160(S4), S9-S22. https://doi.org/10.1086/342131

MeSH Term

Animal Migration
Animals
Host-Parasite Interactions
Models, Theoretical
Parasites
Parasitic Diseases

Word Cloud

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