The evolution of immunity in relation to colonization and migration

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.

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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.

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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.

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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.

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Correspondence to Emily A. O’Connor.

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Supplementary methods, supplementary figures 1 to 7

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Code for the R scripts for all analyses run

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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

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