Genetic variation at innate and adaptive immune genes - contrasting patterns of differentiation and local adaptation in a wild gull.
Journal
Heredity
ISSN: 1365-2540
Titre abrégé: Heredity (Edinb)
Pays: England
ID NLM: 0373007
Informations de publication
Date de publication:
Oct 2023
Oct 2023
Historique:
received:
04
05
2023
accepted:
30
07
2023
revised:
15
07
2023
pmc-release:
01
10
2024
pubmed:
9
8
2023
medline:
9
8
2023
entrez:
8
8
2023
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 37553491
doi: 10.1038/s41437-023-00645-2
pii: 10.1038/s41437-023-00645-2
pmc: PMC10539538
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
282-291Informations de copyright
© 2023. The Author(s), under exclusive licence to The Genetics Society.
Références
Sci Rep. 2014 Nov 05;4:6920
pubmed: 25370306
Mol Biol Evol. 2009 Dec;26(12):2755-64
pubmed: 19713326
Mol Ecol. 2013 Sep;22(17):4470-82
pubmed: 23901904
Mol Ecol. 2008 Sep;17(18):4015-26
pubmed: 19238703
Mol Ecol Resour. 2011 May;11(3):562-6
pubmed: 21481215
Heredity (Edinb). 2021 Mar;126(3):548-560
pubmed: 32985616
Mol Ecol Resour. 2010 May;10(3):564-7
pubmed: 21565059
Mol Ecol. 2015 Dec;24(23):5852-63
pubmed: 26509790
Mol Biol Evol. 2017 Dec 1;34(12):3299-3302
pubmed: 29029172
Evolution. 2018 Jun;72(6):1278-1293
pubmed: 29665025
Mol Biol Evol. 2018 Sep 1;35(9):2170-2184
pubmed: 29893911
Mol Biol Evol. 2011 May;28(5):1703-15
pubmed: 21239391
PLoS One. 2013 Jul 23;8(7):e69135
pubmed: 23935938
Infect Genet Evol. 2021 Nov;95:105069
pubmed: 34487864
Parasitology. 2004 Jul;129(Pt 1):101-13
pubmed: 15267117
BMC Evol Biol. 2017 Feb 20;17(1):56
pubmed: 28219340
Elife. 2019 Jan 08;8:
pubmed: 30620335
Nat Rev Immunol. 2012 Jul 13;12(8):557-69
pubmed: 22790179
Trends Genet. 2020 Apr;36(4):298-311
pubmed: 32044115
Mol Ecol. 2007 Apr;16(7):1439-51
pubmed: 17391268
Nature. 1993 Jul 1;364(6432):33-9
pubmed: 8316295
Parasitology. 2022 Sep;149(11):1479-1486
pubmed: 35768413
Annu Rev Genet. 2010;44:445-77
pubmed: 20809801
Science. 2007 Jun 22;316(5832):1738-43
pubmed: 17588928
Sci Rep. 2019 Apr 2;9(1):5523
pubmed: 30940855
Genetics. 2003 Jul;164(3):1229-36
pubmed: 12871927
Proc Biol Sci. 2011 Apr 22;278(1709):1264-72
pubmed: 20943698
J Anim Ecol. 2010 Mar;79(2):317-26
pubmed: 19891713
Front Immunol. 2020 Dec 14;11:601089
pubmed: 33381122
J Evol Biol. 2014 Nov;27(11):2347-59
pubmed: 25244157
Mol Ecol Resour. 2016 Mar;16(2):498-510
pubmed: 26257385
Proc Biol Sci. 2010 Apr 7;277(1684):979-88
pubmed: 20071384
Mol Ecol. 2011 Dec;20(24):5213-25
pubmed: 22106868
Mol Ecol Resour. 2017 Jan;17(1):5-11
pubmed: 27327208
Mol Biol Evol. 2020 Jun 1;37(6):1708-1726
pubmed: 32096861
Virus Evol. 2015 May 26;1(1):vev003
pubmed: 27774277
Ecol Evol. 2014 Mar;4(6):688-98
pubmed: 24683452
Mol Genet Genomics. 2022 Sep;297(5):1329-1342
pubmed: 35786764
J Hered. 2018 Jun 27;109(5):501-509
pubmed: 29893971
BMC Genomics. 2008 Feb 01;9:62
pubmed: 18241342
Ecol Evol. 2016 Sep 28;6(20):7498-7510
pubmed: 28725416
PLoS One. 2020 May 29;15(5):e0233714
pubmed: 32469968
Mol Biol Evol. 2013 May;30(5):1196-205
pubmed: 23420840
Evolution. 2006 Feb;60(2):383-9
pubmed: 16610328
Microbes Infect. 2004 Aug;6(10):946-59
pubmed: 15310472
Nat Commun. 2017 Nov 3;8(1):1294
pubmed: 29101318
PLoS Biol. 2004 Jun;2(6):e141
pubmed: 15208708
Evolution. 2021 Nov;75(11):2736-2746
pubmed: 34596241
Mol Biol Evol. 2018 Mar 1;35(3):773-777
pubmed: 29301006
Zoological Lett. 2015 Mar 25;1:13
pubmed: 26605058
Mol Biol Evol. 2022 May 3;39(5):
pubmed: 35574644
Biometrics. 2008 Dec;64(4):1178-86
pubmed: 18355386
Mol Ecol. 2021 Jun;30(11):2528-2542
pubmed: 33949028
Mol Ecol. 2022 Dec;31(24):6390-6406
pubmed: 36208104
Mol Ecol. 2010 Sep;19(18):3894-908
pubmed: 20723045
PLoS Genet. 2012;8(7):e1002764
pubmed: 22807683
Science. 2013 Mar 1;339(6123):1063-7
pubmed: 23371554
Mol Ecol Resour. 2010 Mar;10(2):237-51
pubmed: 21565019
Bioinformatics. 2008 Jun 1;24(11):1403-5
pubmed: 18397895
J Hered. 2017 Mar 1;108(2):127-134
pubmed: 27940472
Evol Appl. 2018 Jul 28;11(10):1763-1778
pubmed: 30459828
Mol Ecol. 2014 Mar;23(5):1028-39
pubmed: 24447303
Parasitol Res. 2014 Mar;113(3):837-50
pubmed: 24297694
Ecol Evol. 2020 Jun 01;10(12):5489-5505
pubmed: 32607169
Inflamm Res. 2010 Oct;59(10):791-808
pubmed: 20593217
J Anim Ecol. 2019 Aug;88(8):1226-1239
pubmed: 31002193
PLoS Genet. 2008 Dec;4(12):e1000304
pubmed: 19081788
Nat Rev Immunol. 2006 Dec;6(12):895-906
pubmed: 17110955
Mol Ecol. 2015 Aug;24(15):3873-87
pubmed: 26120040
PLoS Comput Biol. 2019 May 16;15(5):e1007015
pubmed: 31095555
Mol Ecol. 2015 Dec;24(24):6095-106
pubmed: 26547898
J Mol Biol. 1991 May 20;219(2):277-319
pubmed: 2038058
Dev Comp Immunol. 2021 Jun;119:103990
pubmed: 33422554
J Hered. 2021 Jul 15;112(4):335-345
pubmed: 33942876
Nucleic Acids Res. 2023 Jan 6;51(D1):D1053-D1060
pubmed: 36350643
R Soc Open Sci. 2016 Aug 10;3(8):160216
pubmed: 27853596
Mol Ecol Resour. 2017 Jul;17(4):642-655
pubmed: 27762049
Bioinformatics. 2011 Aug 15;27(16):2194-200
pubmed: 21700674
Am J Hum Genet. 2003 Nov;73(5):1162-9
pubmed: 14574645