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Genetic variation at innate and adaptive immune genes – contrasting patterns of differentiation and local adaptation in a wild gull

Heredity volume 131, pages 282–291 (2023)Cite this article

Subjects

Abstract

Immunogenetic variation in natural vertebrate populations is expected to respond to spatial and temporal fluctuations in pathogen assemblages. While spatial heterogeneity in pathogen-driven selection enhances local immunogenetic adaptations and population divergence, different immune genes may yield contrasting responses to the environment. Here, we investigated population differentiation at the key pathogen recognition genes of the innate and adaptive immune system in a colonial bird species, the black-headed gull Chroicocephalus ridibundus. We assessed genetic variation at three toll-like receptor (TLR) genes (innate immunity) and the major histocompatibility complex (MHC) class I and II genes (adaptive immunity) in gulls from seven colonies scattered across Poland. As expected, we found much greater polymorphism at the MHC than TLRs. Population differentiation at the MHC class II, but not MHC-I, was significantly stronger than at neutral microsatellite loci, suggesting local adaptation. This could reflect spatial variation in the composition of extracellular parasite communities (e.g., helminths), possibly driven by sharp differences in habitat structure between colonies. Despite contrasting patterns of population differentiation, both MHC classes showed similar regimes of diversifying selection. Some significant population differentiation was also observed at TLRs, suggesting that innate immune receptors may respond to fine-scale spatial variation in pathogen pressure, although this pattern could have been enhanced by drift. Our results suggested that local adaptation at the pathogen recognition immune genes can be maintained at relatively small or moderate spatial scales in species with high dispersal potential and they highlighted the complexity of immunogenetic responses of animals to heterogeneous environments.

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Fig. 1: Study area.
Fig. 2: Genetic population differentiation.
Fig. 3: Population differentiation at the MHC-II.
Fig. 4: Selection on MHC genes.

Data availability

All data used in this study are available in Dryad (https://doi.org/10.5061/dryad.15dv41p32). All novel sequences generated in this study have been deposited in GenBank (OR333996-OR334322).

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Acknowledgements

We thank all participants in fieldwork, especially Jacek Betleja, Beata Dulisz, and Jarosław Kowalski. We thank three anonymous reviewers for constructive comments on the earlier drafts of the manuscript.

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Authors and Affiliations

  1. Department of Biodiversity Studies and Bioeducation, Faculty of Biology and Environmental Protection, University of Łódź, Banacha 1/3, 90-237, Łódź, Poland

    Piotr Minias, Patrycja Podlaszczuk, Amelia Chyb & Tomasz Janiszewski

  2. Department of Biology and Animal Environment, Faculty of Animal Breeding and Biology, Bydgoszcz University of Science and Technology, Mazowiecka 28, 85-084, Bydgoszcz, Poland

    Piotr Indykiewicz

  3. Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Sławkowska 17, 31-016, Kraków, Poland

    Mateusz Ledwoń

  4. Department of Ecology and Environmental Protection, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Plac Łódzki 3, 10-727, Olsztyn, Poland

    Jacek Nowakowski

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  1. Piotr Minias
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Contributions

PM designed the study. PI, ML, JN, and TJ performed fieldwork and collected samples. PP and ACh performed laboratory analyses. PM and PP performed statistical and bioinformatic analyses. PM wrote the first draft of the manuscript, all authors revised the manuscript for intellectual content and approved the final draft.

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Correspondence to Piotr Minias.

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Catching of birds was authorised by the Polish Academy of Sciences, with the approval of the General Directorate for Environmental Protection, Poland. The study was performed under the permit from the Local Bioethical Committee for Experiments on Animals in Łódź and appropriate Regional Environmental Protection Directorates in Poland.

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Minias, P., Podlaszczuk, P., Indykiewicz, P. et al. Genetic variation at innate and adaptive immune genes – contrasting patterns of differentiation and local adaptation in a wild gull. Heredity 131, 282–291 (2023). https://doi.org/10.1038/s41437-023-00645-2

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