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:

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.

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

Similar content being viewed by others

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).

References

  • Alcaide M, Edwards SV (2011) Molecular evolution of the toll-like receptor multigene family in birds. Mol Biol Evol 28:1703–1715

    Article  CAS  PubMed  Google Scholar 

  • Alcaide M, Muñoz J, Martínez‐de la Puente J, Soriguer R, Figuerola J (2014) Extraordinary MHC class II B diversity in a non‐passerine, wild bird: the Eurasian Coot Fulica atra (Aves: Rallidae). Ecol Evol 4:688–698

    Article  PubMed  PubMed Central  Google Scholar 

  • Amundson CL, Arnold TW (2010) Anthelmintics increase survival of American Coot (Fulica americana) chicks. Auk 127:653–659

    Article  Google Scholar 

  • Andrés AM, Hubisz MJ, Indap A, Torgerson DG, Degenhardt JD, Boyko AR et al. (2009) Targets of balancing selection in the human genome. Mol Biol Evol 26:2755–2764

    Article  PubMed  PubMed Central  Google Scholar 

  • Anisimova M, Nielsen R, Yang Z (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229–1236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Archer FI, Adams PE, Schneiders BB (2017) stratag: an r package for manipulating, summarizing and analysing population genetic data. Mol Ecol Res 17:5–11

    Article  CAS  Google Scholar 

  • Babik W (2010) Methods for MHC genotyping in non‐model vertebrates. Mol Ecol Res 10:237–251

    Article  CAS  Google Scholar 

  • Barker DJ, Maccari G, Georgiou X, Cooper MA, Flicek P, Robinson J, Marsh SG (2022) The IPD-IMGT/HLA Database. Nucleic Acids Res 2022:gkac1011

    Google Scholar 

  • Bateson ZW, Whittingham LA, Johnson JA, Dunn PO (2015) Contrasting patterns of selection and drift between two categories of immune genes in prairie‐chickens. Mol Ecol 24:6095–6106

    Article  CAS  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Bentkowski P, Radwan J (2019) Evolution of major histocompatibility complex gene copy number. PLoS Comput Biol 15:e1007015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biedrzycka A, Sebastian A, Migalska M, Westerdahl H, Radwan J (2017) Testing genotyping strategies for ultra‐deep sequencing of a co‐amplifying gene family: MHC class I in a passerine bird. Mol Ecol Res 17:642–655

    Article  CAS  Google Scholar 

  • Bonneaud C, Pérez‐Tris J, Federici P, Chastel O, Sorci G (2006) Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution 60:383–389

    CAS  PubMed  Google Scholar 

  • Bosch M, Torres J, Figuerola J (2000) A helminth community in breeding Yellow-legged Gulls (Larus cachinnans): pattern of association and its effect on host fitness. Can J Zool 78:777–786

    Article  Google Scholar 

  • Boyd RJ, Denommé MR, Grieves LA, MacDougall‐Shackleton EA (2021) Stronger population differentiation at infection‐sensing than infection‐clearing innate immune loci in songbirds: different selective regimes for different defenses. Evolution 75:2736–2746

    Article  CAS  PubMed  Google Scholar 

  • Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33–39

    Article  CAS  PubMed  Google Scholar 

  • Calvete C, Blanco-Aguiar JA, Virgós E, Cabezas-Díaz S, Villafuerte R (2004) Spatial variation in helminth community structure in the red-legged partridge (Alectoris rufa L.): effects of definitive host density. Parasitology 129:101–113

    Article  CAS  PubMed  Google Scholar 

  • Chang ZL (2010) Important aspects of Toll-like receptors, ligands and their signaling pathways. Inflamm Res 59:791–808

    Article  CAS  PubMed  Google Scholar 

  • Chao A, Jost L, Chiang SC, Jiang YH, Chazdon RL (2008) A two‐stage probabilistic approach to multiple‐community similarity indices. Biometrics 64:1178–1186

    Article  PubMed  Google Scholar 

  • Clark LV, Jasieniuk M (2011) Polysat: an R package for polyploid microsatellite analysis. Mol Ecol Res 11:562–566

    Article  Google Scholar 

  • Davies CS, Taylor MI, Hammers M, Burke T, Komdeur J, Dugdale HL, Richardson DS (2021) Contemporary evolution of the innate immune receptor gene TLR3 in an isolated vertebrate population. Mol Ecol 30:2528–2542

    Article  PubMed  Google Scholar 

  • Dearborn DC, Warren S, Hailer F (2022) Meta‐analysis of major histocompatibility complex (MHC) class IIA reveals polymorphism and positive selection in many vertebrate species. Mol Ecol 31:6390–6406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Article  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ekblom R, Saether SA, Jacobsson P, Fiske P, Sahlman T, Grahn M et al. (2007) Spatial pattern of MHC class II variation in the great snipe (Gallinago media). Mol Ecol 16:1439–1451

    Article  PubMed  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Gazzinelli RT, Denkers EY (2006) Protozoan encounters with Toll-like receptor signalling pathways: implications for host parasitism. Nat Rev Immunol 6:895–906

    Article  CAS  PubMed  Google Scholar 

  • Gerdol M, Lucente D, Buonocore F, Poerio E, Scapigliati G, Mattiucci S et al. (2019) Molecular and structural characterization of MHC class II β genes reveals high diversity in the cold-adapted icefish Chionodraco hamatus. Sci Rep. 9:5523

    Article  PubMed  PubMed Central  Google Scholar 

  • Gemayel R, Vinces MD, Legendre M, Verstrepen KJ (2010) Variable tandem repeats accelerate evolution of coding and regulatory sequences. Ann Rev Genet 44:445–477

    Article  CAS  PubMed  Google Scholar 

  • Gibson D, Bray R, Harris E (2005) Host–parasite database of the Natural History Museum, London. https://www.nhm.ac.uk/research-curation/scientific-resources/taxonomy-systematics/host-parasites/database/index.jsp

  • Gillingham MA, Béchet A, Courtiol A, Rendón-Martos M, Amat JA, Samraoui B et al. (2017) Very high MHC Class IIB diversity without spatial differentiation in the mediterranean population of greater Flamingos. BMC Evol Biol 17:56

    Article  PubMed  PubMed Central  Google Scholar 

  • Given AD, Mills JA, Baker AJ (2002) Isolation of polymorphic microsatellite loci from the red‐billed gull (Larus novaehollandiae scopulinus) and amplification in related species. Mol Ecol Notes 2:416–418

    Article  CAS  Google Scholar 

  • Gonzalez‐Quevedo C, Spurgin LG, Illera JC, Richardson DS (2015) Drift, not selection, shapes toll‐like receptor variation among oceanic island populations. Mol Ecol 24:5852–5863

    Article  PubMed  PubMed Central  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Article  Google Scholar 

  • Grueber CE, Wallis GP, Jamieson IG (2013) Genetic drift outweighs natural selection at toll‐like receptor (TLR) immunity loci in a re‐introduced population of a threatened species. Mol Ecol 22:4470–4482

    Article  CAS  PubMed  Google Scholar 

  • Guernier V, Hochberg ME, Guégan JF (2004) Ecology drives the worldwide distribution of human diseases. PLoS Biol 2:e141

    Article  PubMed  PubMed Central  Google Scholar 

  • Gutiérrez JS, Piersma T, Thieltges DW (2019) Micro‐and macroparasite species richness in birds: the role of host life history and ecology. J Anim Ecol 88:1226–1239

    Article  PubMed  Google Scholar 

  • Herdegen M, Babik W, Radwan J (2014) Selective pressures on MHC class II genes in the guppy (Poecilia reticulata) as inferred by hierarchical analysis of population structure. J Evol Biol 27:2347–2359

    Article  CAS  PubMed  Google Scholar 

  • Herdegen-Radwan M, Phillips KP, Babik W, Mohammed RS, Radwan J (2021) Balancing selection versus allele and supertype turnover in MHC class II genes in guppies. Heredity 126:548–560

    Article  CAS  PubMed  Google Scholar 

  • Indykiewicz P, Podlaszczuk P, Janiszewska A, Minias P (2018) Extensive gene flow along the urban–rural gradient in a migratory colonial bird. J Avian Biol 49:e01723

    Article  Google Scholar 

  • Jakubas D, Indykiewicz P, Kowalski J, Iciek T, Minias P (2020) Intercolony variation in foraging flight characteristics of black‐headed gulls Chroicocephalus ridibundus during the incubation period. Ecol Evol 10:5489–5505

    Article  PubMed  PubMed Central  Google Scholar 

  • Janeway JCA, Travers P, Walport M, Shlomchik MJ (2001) Immunobiology: the immune system in health and disease. Garland Science, New York

  • Joffre OP, Segura E, Savina A, Amigorena S (2012) Cross-presentation by dendritic cells. Nat Rev Immunol 12:557–569

  • Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Kanarek G, Zaleśny G (2014) Extrinsic-and intrinsic-dependent variation in component communities and patterns of aggregations in helminth parasites of great cormorant (Phalacrocorax carbo) from NE Poland. Parasitol Res 113:837–850

    Article  PubMed  Google Scholar 

  • Kaufman J (2020) From chickens to humans: the importance of peptide repertoires for MHC class I alleles. Front Immunol 11:601089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Kohyama TI, Omote K, Nishida C, Takenaka T, Saito K, Fujimoto S, Masuda R (2015) Spatial and temporal variation at major histocompatibility complex class IIB genes in the endangered Blakiston’s fish owl. Zoological Lett 1:13

  • Kozakiewicz CP, Burridge CP, Funk WC, VandeWoude S, Craft ME, Crooks KR et al. (2018) Pathogens in space: advancing understanding of pathogen dynamics and disease ecology through landscape genetics. Evol Appl 11:1763–1778

    Article  PubMed  PubMed Central  Google Scholar 

  • Kryazhimskiy S, Plotkin JB (2008) The population genetics of dN/dS. PLoS Genet 4:e1000304

    Article  PubMed  PubMed Central  Google Scholar 

  • Leclaire S, van Dongen WF, Voccia S, Merkling T, Ducamp C, Hatch SA et al. (2014) Preen secretions encode information on MHC similarity in certain sex-dyads in a monogamous seabird. Sci Rep 4:6920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levy H, Fiddaman SR, Vianna JA, Noll D, Clucas GV, Sidhu JK et al. (2020) Evidence of pathogen-induced immunogenetic selection across the large geographic range of a wild seabird. Mol Biol Evol 37:1708–1726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lighten J, Papadopulos AS, Mohammed RS, Ward BJ, Paterson IG, Baillie L (2017) Evolutionary genetics of immunological supertypes reveals two faces of the Red Queen. Nat Comm 8:1294

    Article  Google Scholar 

  • Loiseau C, Zoorob R, Robert A, Chastel O, Julliard R, Sorci G (2011) Plasmodium relictum infection and MHC diversity in the house sparrow (Passer domesticus). Proc R Soc B 278:1264–1272

    Article  PubMed  Google Scholar 

  • Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1:vev003

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller HC, Allendorf F, Daugherty CH (2010) Genetic diversity and differentiation at MHC genes in island populations of tuatara (Sphenodon spp.). Mol Ecol 19:3894–3908

    Article  PubMed  Google Scholar 

  • Minias P, Drzewińska-Chańko J, Włodarczyk R (2021a) Evolution of innate and adaptive immune genes in a non-model waterbird, the common tern. Infect Genet Evol 95:105069

    Article  CAS  PubMed  Google Scholar 

  • Minias P, Janiszewska A, Pikus E, Zadworny T, Anderwald D (2021b) MHC reflects fine-scale habitat structure in white-tailed eagles, Haliaeetus albicilla. J Hered 112:335–345

    Article  CAS  PubMed  Google Scholar 

  • Minias P, Pikus E, Whittingham LA, Dunn PO (2018) A global analysis of selection at the avian MHC. Evolution 72:1278–1293

    Article  PubMed  Google Scholar 

  • Minias P, Vinkler M (2022) Selection balancing at innate immune genes: adaptive polymorphism maintenance in Toll-like receptors. Mol Biol Evol 39:msac102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K (2013) FUBAR: a fast, unconstrained Bayesian approximation for inferring selection. Mol Biol Evol 30:1196–1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson-Flower MJ, Germain RR, MacDougall-Shackleton EA, Taylor SS, Arcese P (2018) Purifying selection in the toll-like receptors of song sparrows Melospiza melodia. J Hered 109:501–509

    Article  CAS  PubMed  Google Scholar 

  • Péron G, Lebreton JD, Crochet PA (2010) Breeding dispersal in black‐headed gull: the value of familiarity in a contrasted environment. J Anim Ecol 79:317–326

    Article  PubMed  Google Scholar 

  • Promerová M, Králová T, Bryjová A, Albrecht T, Bryja J (2013) MHC class IIB exon 2 polymorphism in the Grey partridge (Perdix perdix) is shaped by selection, recombination and gene conversion. PLoS ONE 8:e69135

    Article  PubMed  PubMed Central  Google Scholar 

  • Quéméré E, Galan M, Cosson JF, Klein F, Aulagnier S, Gilot‐Fromont E et al. (2015) Immunogenetic heterogeneity in a widespread ungulate: the European roe deer (Capreolus capreolus). Mol Ecol 24:3873–3887

    Article  PubMed  Google Scholar 

  • Quesniaux V, Fremond C, Jacobs M, Parida S, Nicolle D, Yeremeev V et al. (2004) Toll-like receptor pathways in the immune responses to mycobacteria. Microbes Infect 6:946–959

    Article  CAS  PubMed  Google Scholar 

  • Radwan J, Babik W, Kaufman J, Lenz TL, Winternitz J (2020) Advances in the evolutionary understanding of MHC polymorphism. Trends Genet 36:298–311

    Article  CAS  PubMed  Google Scholar 

  • Ranathunge C, Chimahusky ME, Welch ME (2022) A comparative study of population genetic structure reveals patterns consistent with selection at functional microsatellites in common sunflower. Mol Genet Genom 297:1329–1342

    Article  CAS  Google Scholar 

  • Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302

    Article  CAS  PubMed  Google Scholar 

  • Sallaberry‐Pincheira N, González‐Acuña D, Padilla P, Dantas GP, Luna‐Jorquera G, Frere E et al. (2016) Contrasting patterns of selection between MHC I and II across populations of Humboldt and Magellanic penguins. Ecol Evol 6:7498–7510

    Article  PubMed  PubMed Central  Google Scholar 

  • Saper MA, Bjorkman P, Wiley DC (1991) Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 Å resolution. J Mol Biol 219:277–319

    Article  CAS  PubMed  Google Scholar 

  • Sarquis-Adamson Y, MacDougall-Shackleton EA (2016) Song sparrows Melospiza melodia have a home-field advantage in defending against sympatric malarial parasites. R Soc Open Sci 3:160216

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Shapiro MD, Kronenberg Z, Li C, Domyan ET, Pan H, Campbell M et al. (2013) Genomic diversity and evolution of the head crest in the rock pigeon. Science 339:1063–1067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shultz AJ, Sackton TB (2019) Immune genes are hotspots of shared positive selection across birds and mammals. eLife 8:e41815

    Article  PubMed  PubMed Central  Google Scholar 

  • Slade JW, Sarquis-Adamson Y, Gloor GB, Lachance MA, MacDougall-Shackleton EA (2017) Population differences at MHC do not explain enhanced resistance of song sparrows to local parasites. J Hered 108:127–134

    CAS  PubMed  Google Scholar 

  • Spurgin LG, Illera JC, Jorgensen TH, Dawson DA, Richardson DS (2014) Genetic and phenotypic divergence in an island bird: isolation by distance, by colonization or by adaptation? Mol Ecol 23:1028–1039

    Article  PubMed  Google Scholar 

  • Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B 277:979–988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spurgin LG, Van Oosterhout C, Illera JC, Bridgett S, Gharbi K, Emerson BC, Richardson DS (2011) Gene conversion rapidly generates major histocompatibility complex diversity in recently founded bird populations. Mol Ecol 20:5213–5225

    Article  CAS  PubMed  Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Temperley ND, Berlin S, Paton IR, Griffin DK, Burt DW (2008) Evolution of the chicken Toll-like receptor gene family: a story of gene gain and gene loss. BMC Genomics 9:62

    Article  PubMed  PubMed Central  Google Scholar 

  • Tirard C, Helfenstein F, Danchin E (2002) Polymorphic microsatellites in the black‐legged kittiwake Rissa tridactyla. Mol Ecol Notes 2:431–433

    Article  CAS  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO‐CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Velová H, Gutowska-Ding MW, Burt DW, Vinkler M (2018) Toll-like receptor evolution in birds: gene duplication, pseudogenization, and diversifying selection. Mol Biol Evol 35:2170–2184

    Article  PubMed  PubMed Central  Google Scholar 

  • Waterhouse RM, Kriventseva EV, Meister S, Xi Z, Alvarez KS, Bartholomay LC et al. (2007) Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316:1738–1743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weaver S, Shank SD, Spielman SJ, Li M, Muse SV, Kosakovsky Pond SL (2018) Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol Biol Evol 35:773–777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Włodarczyk R, Bouwhuis S, Bichet C, Podlaszczuk P, Chyb A, Indykiewicz P et al. (2022) Contrasting haemoparasite prevalence in larid species with divergent ecological niches and migration patterns. Parasitology 149:1479–1486

    Article  PubMed  Google Scholar 

  • Xu W, Zhou X, Fang W, Chen X (2020) Genetic diversity of toll-like receptor genes in the vulnerable Chinese egret (Egretta eulophotes). PLoS ONE 15:e0233714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Zhou M, Zhong Y, Xu L, Zeng C, Zhao X, Zhang M (2021) Gene duplication and adaptive evolution of Toll-like receptor genes in birds. Dev Comp Immunol 119:103990

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

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

Authors
  1. Piotr Minias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patrycja Podlaszczuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Piotr Indykiewicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mateusz Ledwoń
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jacek Nowakowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Amelia Chyb
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tomasz Janiszewski
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Corresponding author

Correspondence to Piotr Minias.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval

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.

Additional information

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

Associate editor: Gerald Heckel.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41437-023-00645-2

Search

Advanced search

Quick links