Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

The evolution of immunity in relation to colonization and migration

Nature Ecology & Evolution volume 2, pages 841–849 (2018)Cite this article

Subjects

Abstract

Colonization and migration have a crucial effect on patterns of biodiversity, with disease predicted to play an important role in these processes. However, evidence of the effect of pathogens on broad patterns of colonization and migration is limited. Here, using phylogenetic analyses of 1,311 species of Afro-Palaearctic songbirds, we show that colonization events from regions of high (sub-Saharan Africa) to low (the Palaearctic) pathogen diversity were up to 20 times more frequent than the reverse, and that migration has evolved 3 times more frequently from African- as opposed to Palaearctic-resident species. We also found that resident species that colonized the Palaearctic from Africa, as well as African species that evolved long-distance migration to breed in the Palaearctic, have reduced diversity of key immune genes associated with pathogen recognition (major histocompatibility complex class I). These results suggest that changes in the pathogen community that occur during colonization and migration shape the evolution of the immune system, potentially by adjusting the trade-off between the benefits of extensive pathogen recognition and the costs of immunopathology that result from high major histocompatibility complex class I diversity.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Colonization and migration change the pathogens that species face.
Fig. 2: Evolutionary history of colonization events.
Fig. 3: Changes in MHC-I diversity during the colonization process.
Fig. 4: Changes in MHC diversity during the evolution of migration.

Similar content being viewed by others

References

  1. Bauer, S. & Hoye, B. J. Migratory animals couple biodiversity and ecosystem functioning worldwide. Science 344, 1242552 (2014).

    Article  CAS  PubMed  Google Scholar 

  2. Pecl, G. T. et al. Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355, eaai9214 (2017).

    Article  PubMed  Google Scholar 

  3. Helmus, M. R., Mahler, D. L. & Losos, J. B. Island biogeography of the Anthropocene. Nature 513, 543–546 (2014).

    Article  CAS  PubMed  Google Scholar 

  4. Sax, D. F. et al. Ecological and evolutionary insights from species invasions. Trends Ecol. Evol. 22, 465–471 (2007).

    Article  PubMed  Google Scholar 

  5. Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J. & Kuris, A. M. Introduced species and their missing parasites. Nature 421, 628–630 (2003).

    Article  CAS  PubMed  Google Scholar 

  6. Altizer, S., Bartel, R. & Han, B. A. Animal migration and infectious disease risk. Science 331, 296–302 (2011).

    Article  CAS  PubMed  Google Scholar 

  7. Mitchell, C. E. & Power, A. G. Release of invasive plants from fungal and viral pathogens. Nature 421, 625–627 (2003).

    Article  CAS  PubMed  Google Scholar 

  8. Westerdahl, H. et al. in Animal Movement Across Scales (eds Hansson, L. A. & Åkesson, S.) Ch. 8 (Oxford Univ. Press, Oxford, 2014).

  9. Keane, R. M. & Crawley, M. J. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17, 164–170 (2002).

    Article  Google Scholar 

  10. Almberg, E. S., Cross, P. C., Dobson, A. P., Smith, D. W. & Hudson, P. J. Parasite invasion following host reintroduction: a case study of Yellowstone’s wolves. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 2840–2851 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Guégan, J.-F., Prugnolle, F. & Thomas, F. in Evolution in Health and Disease (eds Stearns, S. C. & Koella, J. C.) Ch. 2 (Oxford Univ. Press, Oxford, 2008).

  12. Guernier, V., Hochberg, M. E. & Guégan, J.-F. Ecology drives the worldwide distribution of human diseases. PLoS Biol. 2, e141 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Bordes, B., Guégan, J. F. & Morand, S. Microparasite species richness in rodents is higher at lower latitudes and is associated with reduced litter size. Oikos 120, 1889–1896 (2011).

    Article  Google Scholar 

  14. Nunn, C. L., Altizer, S. M., Sechrest, W. & Cunningham, A. A. Latitudinal gradients of parasite species richness in primates. Divers. Distrib. 11, 249–256 (2005).

    Article  Google Scholar 

  15. Yang, X. B. & Feng, F. Ranges and diversity of soybean fungal diseases in North America. Phytopathology 91, 769–775 (2001).

    Article  CAS  PubMed  Google Scholar 

  16. Rohde, K. Ecology and biogeography of marine parasites. Adv. Mar. Biol. 43, 1–83 (2002).

    Article  PubMed  Google Scholar 

  17. Wellman, F. L. More diseases on crops in the tropics than in the temperate zone. Ceíba 14, 17–28 (1968).

    Google Scholar 

  18. Clark, N. J., Clegg, S. M. & Klaassen, M. Migration strategy and pathogen risk: non‐breeding distribution drives malaria prevalence in migratory waders. Oikos 125, 1358–1368 (2016).

    Article  Google Scholar 

  19. Mendes, L., Piersma, T., Lecoq, M., Spaans, B. & Ricklefs, R. E. Disease‐limited distributions? Contrasts in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109, 396–404 (2005).

    Article  Google Scholar 

  20. Merino, S. et al. Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Austral Ecol. 33, 329–340 (2008).

    Article  Google Scholar 

  21. Lenz, T. L. Computational prediction of MHC II–antigen binding supports divergent allele advantage and explains trans-species polymorphism. Evolution 65, 2380–2390 (2011).

    Article  PubMed  Google Scholar 

  22. Murphy, K., Janeway C. A. Jr., Travers, P., Walport, M. & Ehrenstein, M. Janeway’s Immunobiology 7th edn (Garland Science, New York, 2008).

  23. Hughes, A. L. & Hughes, M. A. K. Coding sequence polymorphism in avian mitochondrial genomes reflects population histories. Mol. Ecol. 16, 1369–1376 (2007).

    Article  CAS  PubMed  Google Scholar 

  24. Aguilar, A. et al. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc. Natl Acad. Sci. USA 101, 3490–3494 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Schierup, M. H., Vekemans, X. & Charlesworth, D. The effect of subdivision on variation at multi-allelic loci under balancing selection. Genet. Res. 76, 51–62 (2000).

    Article  CAS  PubMed  Google Scholar 

  26. Van Oosterhout, C. et al. Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 60, 2562–2574 (2006).

    Article  CAS  PubMed  Google Scholar 

  27. Sorci, G. Immunity, resistance and tolerance in bird–parasite interactions. Parasite Immunol. 35, 350–361 (2013).

    CAS  PubMed  Google Scholar 

  28. Eizaguirre, C., Lenz, T. L., Kalbe, M. & Milinski, M. Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat. Comm. 3, 621 (2012).

    Article  Google Scholar 

  29. Piertney, S. B. & Oliver, M. K. The evolutionary ecology of the major histocompatibility complex. Heredity 96, 7–21 (2006).

    Article  CAS  PubMed  Google Scholar 

  30. Edwards, S. V. & Hedrick, P. W. Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol. Evol. 13, 305–311 (1998).

    Article  CAS  PubMed  Google Scholar 

  31. Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

    Article  CAS  PubMed  Google Scholar 

  32. Kiepiela, P. et al. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432, 769–775 (2004).

    Article  CAS  PubMed  Google Scholar 

  33. McKiernan, S. M. et al. Distinct MHC class I and II alleles are associated with hepatitis C viral clearance, originating from a single source. Hepatology 40, 108–114 (2004).

    Article  CAS  PubMed  Google Scholar 

  34. Wallny, H. J. et al. Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC-determined response to Rous sarcoma virus in chickens. Proc. Natl Acad. Sci. USA 103, 1434–1439 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hellgren, O. et al. Detecting shifts of transmission areas in avian blood parasites—a phylogenetic approach. Mol. Ecol. 16, 1281–1290 (2007).

    Article  PubMed  Google Scholar 

  36. Piersma, T. Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80, 623–631 (1997).

    Article  Google Scholar 

  37. Westerdahl, H., Wittzell, H. & von Schantz, T. Mhc diversity in two passerine birds: no evidence for a minimal essential Mhc. Immunogenetics 52, 92–100 (2000).

    Article  CAS  PubMed  Google Scholar 

  38. Abbas, A. K., Lichtman, A. H. & Pillai, S. Basic Immunology: Functions and Disorders of the Immune System 4th edn (Elsevier Saunders, Philadelphia, 2014).

  39. Wegner, K. M., Kalbe, M., Kurtz, J., Reusch, T. B. H. & Milinski, M. Parasite selection for immunogenetic optimality. Science 301, 1343 (2003).

    Article  CAS  PubMed  Google Scholar 

  40. Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).

    Article  CAS  PubMed  Google Scholar 

  41. Buehler, D. & Piersma, T. Travelling on a budget: predictions and ecological evidence for bottlenecks in the annual cycle of long-distance migrants. Philos. Trans. R. Soc. B 363, 247–266 (2008).

    Article  Google Scholar 

  42. Hasselquist, D. Comparative immunoecology in birds: hypotheses and tests. J. Ornithol. 148, 571–582 (2007).

    Article  Google Scholar 

  43. Yohannes, E. et al. Isotope signatures in winter moulted feathers predict malaria prevalence in a breeding avian host. Oecologia 158, 299–306 (2008).

    Article  PubMed  Google Scholar 

  44. Winger, B. M., Barker, F. K. & Ree, R. H. Temperate origins of long-distance seasonal migration in New World songbirds. Proc. Natl Acad. Sci. USA 111, 12115–12120 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Harvell, C. D. et al. Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162 (2002).

    Article  CAS  PubMed  Google Scholar 

  46. Altizer, S., Ostfeld, R. S., Johnson, P. T., Kutz, S. & Harvell, C. D. Climate change and infectious diseases: from evidence to a predictive framework. Science 341, 514–519 (2013).

    Article  CAS  PubMed  Google Scholar 

  47. Gill, F. & Donsker, D. IOC World Bird List Version 6.2 (International Ornithological Congress, 2016); https://doi.org/10.14344/IOC.ML.6.2

  48. Del Hoyo, J., Elliott, A., Sargatal, J., Christie, D. A. & de Juana E. Handbook of the Birds of the World Alive (Lynx Edicions, Barcelona, 2016).

  49. Hackett, S. J. et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008).

    Article  CAS  PubMed  Google Scholar 

  50. Pagel, M. A. & Meade, A. Bayesian analysis of correlated evolution of discrete characters by reversible‐jump Markov chain Monte Carlo. Am. Nat. 167, 808–825 (2006).

    PubMed  Google Scholar 

  51. Bollback, J. P. SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC Bioinforma. 7, 88 (2006).

    Article  Google Scholar 

  52. Revell, L. J. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Article  Google Scholar 

  53. Plummer, M., Best, N., Cowles, K. & Vines, K. CODA: convergence diagnosis and output analysis for MCMC. R. News 6, 7–11 (2006).

    Google Scholar 

  54. Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–511 (1992).

    Article  Google Scholar 

  55. Hadfield, J. MCMC methods for multi-response generalised linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

    Article  Google Scholar 

  56. de Villemereuil, V., Gimenez, O. & Doligez, B. Comparing parent–offspring regression with frequentist and Bayesian animal models to estimate heritability in wild populations: a simulation study for Gaussian and binary traits. Methods Ecol. Evol. 4, 260–275 (2013).

    Article  Google Scholar 

  57. Minias, P., Whittingham, L. A. & Dunn, P. O. Coloniality and migration are related to selection on MHC genes in birds. Evolution 71, 432–441 (2017).

    Article  CAS  PubMed  Google Scholar 

  58. Bird Species Distribution Maps of the World Version 5.0. (BirdLife International & NatureServe, 2015).

  59. Barker, F. K., Cibois, A., Schikler, P., Feinstein, J. & Cracraft, J. Phylogeny and diversification of the largest avian radiation. Proc. Natl Acad. Sci. USA 101, 11040–11045 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. O’Connor, E. A., Strandh, M., Hasselquist, D., Nilsson, J. Å. & Westerdahl, H. The evolution of highly variable immunity genes across a passerine bird radiation. Mol. Ecol. 25, 977–989 (2016).

    Article  PubMed  Google Scholar 

  61. Sebastian, A., Herdegen, M., Migalska, M. & Radwan, J. AmpliSAS: a web server for multilocus genotyping using next-generation amplicon sequencing data. Mol. Ecol. Res. 16, 498–510 (2016).

    Article  CAS  Google Scholar 

  62. Peaper, D. R. & Cresswell, P. Regulation of MHC class I assembly and peptide binding. Annu. Rev. Cell Dev. Biol. 24, 343–368 (2008).

    Article  CAS  PubMed  Google Scholar 

  63. Bjorkman, P. et al. The foreign antigen binding site and T cell recognition regions. Nature 329, 512–518 (1987).

    Article  CAS  PubMed  Google Scholar 

  64. Tamura, T., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Gil, M., Zanetti, M. S., Zoller, S. & Anisimova, M. CodonPhyML: fast maximum likelihood phylogeny estimation under codon substitution models. Mol. Biol. Evol. 30, 1270–1280 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Yang, Z., Wong, W. S. & Nielsen, R. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22, 1107–1118 (2005).

    Article  CAS  PubMed  Google Scholar 

  67. Wilson, D. J. & McVean, G. Estimating diversifying selection and functional constraint in the presence of recombination. Genetics 172, 1411–1425 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Hartl, D. L. & Clark, A. G. Principles of Population Genetics (Sinauer Associates, Sunderland, 1998).

  69. Carnaval, A. C., Hickerson, M. J., Haddad, C. F., Rodrigues, M. T. & Moritz, C. Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 323, 785–789 (2009).

    Article  CAS  PubMed  Google Scholar 

  70. Lanfear, R., Ho, S. Y., Love, D. & Bromham, L. Mutation rate is linked to diversification in birds. Proc. Natl Acad. Sci. USA 107, 20423–20428 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Garamszegi, L. Z. Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology (Springer, Berlin, 2014).

  72. Brown, J. H. in Macroecology Ch. 5 (Univ. Chicago Press, Chicago, 1995).

  73. Blueweiss, L., Fox, H., Kudzma, V., Nakashima, D., Peters, R. & Sams, S. Relationships between body size and some life history parameters. Oecologia 37, 257–272 (1978).

    Article  CAS  PubMed  Google Scholar 

  74. Nunn, C. L., Altizer, S., Jones, K. E. & Sechrest, W. Comparative tests of parasite species richness in primates. Am. Nat. 162, 597–614 (2003).

    Article  PubMed  Google Scholar 

  75. Dunning, J. B. Jr. CRC Handbook of Avian Body Masses (CRC Press, Boca Raton, 2013).

Download references

Acknowledgements

This report received support from the Centre for Animal Movement Research, financed by a Linnaeus grant (349–2007–8690) from the Swedish Research Council and Lund University, the Swedish Research Council (621–2011–3674 and 2015–05149 to H.W., 621–2013–4386 to J.-Å.N., 621–2013–4357 and 2016–04391 to D.H., and 2010–5641 to C.K.C.), the Crafoord Foundation (20110600 to H.W.), the Royal Physiographic Society (Schyberg Foundation; 2011-04-13 to H.W.) and a Wallenberg Academy Fellowship to C.K.C. We are grateful to O. Hellgren, L. Råberg, B. Hansson, S. Bensch, J. Neto, M. Melo, U. Ottosson and A. Marzal for assistance with sampling. We thank M. Anisimova and A. Busin (Institute of Applied Simulation, Zurich University of Applied Science) who designed and implemented the pipeline for the positive selection and recombination analysis. We also thank I. Ekström for help with the graphics.

Author information

Authors and Affiliations

  1. Molecular Ecology and Evolution Laboratory, Lund University, Lund, Sweden

    Emily A. O’Connor, Charlie K. Cornwallis, Dennis Hasselquist, Jan-Åke Nilsson & Helena Westerdahl

Authors
  1. Emily A. O’Connor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Charlie K. Cornwallis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dennis Hasselquist
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jan-Åke Nilsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Helena Westerdahl
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study design. All data collection and laboratory work was performed by E.A.O. Data analyses were conducted by E.A.O. and C.K.C. All authors contributed to interpreting the data and writing the manuscript.

Corresponding author

Correspondence to Emily A. O’Connor.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary methods, supplementary figures 1 to 7

Life Sciences Reporting Summary

Supplementary Tables

Supplementary Tables 1 to 18

Supplementary Code

Code for the R scripts for all analyses run

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

O’Connor, E.A., Cornwallis, C.K., Hasselquist, D. et al. The evolution of immunity in relation to colonization and migration. Nat Ecol Evol 2, 841–849 (2018). https://doi.org/10.1038/s41559-018-0509-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-018-0509-3

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing