Neutral Forces and Balancing Selection Interplay to Shape the Major Histocompatibility Complex Spatial Patterns in the Striped Hamster in Inner Mongolia: Suggestive of Broad-Scale Local Adaptation.
balancing selection
local adaptation
major histocompatibility complex
parasite
population differentiation
striped hamster
Journal
Genes
ISSN: 2073-4425
Titre abrégé: Genes (Basel)
Pays: Switzerland
ID NLM: 101551097
Informations de publication
Date de publication:
22 07 2023
22 07 2023
Historique:
received:
26
06
2023
revised:
20
07
2023
accepted:
21
07
2023
medline:
31
7
2023
pubmed:
29
7
2023
entrez:
29
7
2023
Statut:
epublish
Résumé
The major histocompatibility complex (MHC) plays a key role in the adaptive immune response to pathogens due to its extraordinary polymorphism. However, the spatial patterns of MHC variation in the striped hamster remain unclear, particularly regarding the relative contribution of the balancing selection in shaping MHC spatial variation and diversity compared to neutral forces. In this study, we investigated the immunogenic variation of the striped hamster in four wild populations in Inner Mongolia which experience a heterogeneous parasitic burden. Our goal was to identify local adaptation by comparing the genetic structure at the MHC with that at seven microsatellite loci, taking into account neutral processes. We observed significant variation in parasite pressure among sites, with parasite burden showing a correlation with temperature and precipitation. Molecular analysis revealed a similar co-structure between MHC and microsatellite loci. We observed lower genetic differentiation at MHC loci compared to microsatellite loci, and no correlation was found between the two. Overall, these results suggest a complex interplay between neutral evolutionary forces and balancing selection in shaping the spatial patterns of MHC variation. Local adaptation was not detected on a small scale but may be applicable on a larger scale.
Sections du résumé
BACKGROUND
The major histocompatibility complex (MHC) plays a key role in the adaptive immune response to pathogens due to its extraordinary polymorphism. However, the spatial patterns of MHC variation in the striped hamster remain unclear, particularly regarding the relative contribution of the balancing selection in shaping MHC spatial variation and diversity compared to neutral forces.
METHODS
In this study, we investigated the immunogenic variation of the striped hamster in four wild populations in Inner Mongolia which experience a heterogeneous parasitic burden. Our goal was to identify local adaptation by comparing the genetic structure at the MHC with that at seven microsatellite loci, taking into account neutral processes.
RESULTS
We observed significant variation in parasite pressure among sites, with parasite burden showing a correlation with temperature and precipitation. Molecular analysis revealed a similar co-structure between MHC and microsatellite loci. We observed lower genetic differentiation at MHC loci compared to microsatellite loci, and no correlation was found between the two.
CONCLUSIONS
Overall, these results suggest a complex interplay between neutral evolutionary forces and balancing selection in shaping the spatial patterns of MHC variation. Local adaptation was not detected on a small scale but may be applicable on a larger scale.
Identifiants
pubmed: 37510404
pii: genes14071500
doi: 10.3390/genes14071500
pmc: PMC10379431
pii:
doi:
Substances chimiques
Histocompatibility Antigens Class II
0
Histocompatibility Antigens
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Références
Bioinformatics. 2012 Oct 1;28(19):2537-9
pubmed: 22820204
Immunogenetics. 2014 Jun;66(6):393-402
pubmed: 24752816
J Hered. 2017 Sep 1;108(6):628-639
pubmed: 28605534
Trends Genet. 2012 Oct;28(10):480-6
pubmed: 22867968
J Vector Ecol. 2002 Jun;27(1):70-81
pubmed: 12125875
Evolution. 2014 Jan;68(1):176-89
pubmed: 24372603
Mol Ecol. 2021 Apr;30(7):1659-1671
pubmed: 33576071
Immunobiology. 2010 Sep-Oct;215(9-10):673
pubmed: 20692532
Annu Rev Genet. 1998;32:415-35
pubmed: 9928486
Evol Appl. 2016 Aug 21;9(10):1271-1284
pubmed: 27877205
Mol Ecol. 2012 Jan;21(2):431-41
pubmed: 22142265
Bioinformatics. 2009 Jun 1;25(11):1451-2
pubmed: 19346325
Nat Methods. 2012 Jul 30;9(8):772
pubmed: 22847109
Trends Genet. 2020 Apr;36(4):298-311
pubmed: 32044115
Glob Ecol Biogeogr. 2021 Sep;30(9):1810-1821
pubmed: 34539245
Immunogenetics. 2013 Nov;65(11):795-809
pubmed: 23989891
J Forensic Sci. 2011 Jan;56(1):29-35
pubmed: 20887353
Nat Rev Immunol. 2011 Nov 11;11(12):823-36
pubmed: 22076556
Evolution. 2003 Aug;57(8):1707-22
pubmed: 14503614
Philos Trans R Soc Lond B Biol Sci. 2019 Apr 1;374(1769):20180202
pubmed: 30967080
Ecohealth. 2022 Sep;19(3):365-377
pubmed: 36125583
J Mol Evol. 2014 May;78(5):293-305
pubmed: 24748547
Mol Ecol. 2009 Jan;18(1):80-92
pubmed: 19140966
Proc Biol Sci. 2010 Apr 7;277(1684):979-88
pubmed: 20071384
Mol Ecol. 2012 Feb;21(3):541-53
pubmed: 21883591
Mol Ecol Resour. 2016 Mar;16(2):498-510
pubmed: 26257385
Evolution. 2023 Jan 23;77(1):221-238
pubmed: 36626810
PLoS One. 2012;7(2):e31820
pubmed: 22389675
PLoS One. 2010 Jun 16;5(6):e10948
pubmed: 20585386
Int J Epidemiol. 2009 Dec;38(6):1634-41
pubmed: 19584125
Bioinformatics. 2001 Aug;17(8):754-5
pubmed: 11524383
Ecol Evol. 2018 Mar 26;8(8):4162-4172
pubmed: 29721288
Proc Biol Sci. 2009 Mar 22;276(1659):1119-28
pubmed: 19129114
PLoS Negl Trop Dis. 2021 Aug 3;15(8):e0009558
pubmed: 34343197
Philos Trans R Soc Lond B Biol Sci. 2009 Jan 12;364(1513):15-26
pubmed: 18926975
Ecol Lett. 2006 Apr;9(4):467-84
pubmed: 16623732
Ecol Evol. 2019 Mar 01;9(7):3891-3898
pubmed: 31015974
Ecol Lett. 2009 Jan;12(1):5-12
pubmed: 19087108
Nat Commun. 2012 Jan 10;3:621
pubmed: 22233631
Mol Ecol Resour. 2010 May;10(3):564-7
pubmed: 21565059
Mol Biol Evol. 1986 Sep;3(5):418-26
pubmed: 3444411
Sci Total Environ. 2020 Sep 1;733:137782
pubmed: 32209235
PLoS One. 2015 Oct 08;10(10):e0140170
pubmed: 26448462
Biology (Basel). 2021 Dec 08;10(12):
pubmed: 34943211
PLoS Biol. 2004 Jun;2(6):e141
pubmed: 15208708
Mol Biol Evol. 2018 Mar 1;35(3):773-777
pubmed: 29301006
Mol Ecol. 2012 Feb;21(4):887-906
pubmed: 22066802
Heredity (Edinb). 2011 Mar;106(3):404-20
pubmed: 21224881
Front Immunol. 2021 Jul 26;12:703025
pubmed: 34381454
Mol Biol Evol. 2012 Jul;29(7):1713-20
pubmed: 22323362
Ecol Evol. 2013 Jun;3(6):1552-68
pubmed: 23789067
Mol Ecol. 2008 Sep;17(18):4053-67
pubmed: 19238706
Hydrobiologia. 2019;832(1):215-233
pubmed: 30880832
Bioinformatics. 1998;14(1):68-73
pubmed: 9520503
Animals (Basel). 2022 Mar 13;12(6):
pubmed: 35327121
Proc Biol Sci. 2008 Dec 22;275(1653):2813-21
pubmed: 18713722
Mol Ecol. 2016 Nov;25(21):5451-5466
pubmed: 27596520
PLoS One. 2012;7(12):e50971
pubmed: 23251409
BMC Ecol Evol. 2022 Apr 1;22(1):41
pubmed: 35365100
Mol Ecol. 2007 Apr;16(7):1413-25
pubmed: 17391266
Trends Parasitol. 2003 Jul;19(7):293-9
pubmed: 12855379
Int J Parasitol Parasites Wildl. 2019 Apr 29;9:174-183
pubmed: 31193431
Evolution. 2002 Oct;56(10):1902-8
pubmed: 12449477
Bioinformatics. 2007 Jul 15;23(14):1801-6
pubmed: 17485429
Genetics. 2003 Aug;164(4):1567-87
pubmed: 12930761