Both candidate gene and neutral genetic diversity correlate with parasite resistance in female Mediterranean mouflon.
Coccidia
Gastro-intestinal nematodes
Heterozygosity-fitness correlations
Immunocompetence
MHC
Journal
BMC ecology
ISSN: 1472-6785
Titre abrégé: BMC Ecol
Pays: England
ID NLM: 101088674
Informations de publication
Date de publication:
05 03 2019
05 03 2019
Historique:
received:
03
09
2018
accepted:
23
02
2019
entrez:
7
3
2019
pubmed:
7
3
2019
medline:
15
6
2019
Statut:
epublish
Résumé
Parasite infections can have substantial impacts on population dynamics and are accordingly a key challenge for wild population management. Here we studied genetic mechanisms driving parasite resistance in a large herbivore through a comprehensive approach combining measurements of neutral (16 microsatellites) and adaptive (MHC DRB1 exon 2) genetic diversity and two types of gastrointestinal parasites (nematodes and coccidia). While accounting for other extrinsic and intrinsic predictors known to impact parasite load, we show that both neutral genetic diversity and DRB1 are associated with resistance to gastrointestinal nematodes. Intermediate levels of multi-locus heterozygosity maximized nematodes resistance, suggesting that both in- and outbreeding depression might occur in the population. DRB1 heterozygosity and specific alleles effects were detected, suggesting the occurrence of heterozygote advantage, rare-allele effects and/or fluctuating selection. On the contrary, no association was detected between genetic diversity and resistance to coccidia, indicating that different parasite classes are impacted by different genetic drivers. This study provides important insights for large herbivores and wild sheep pathogen management, and in particular suggests that factors likely to impact genetic diversity and allelic frequencies, including global changes, are also expected to impact parasite resistance.
Sections du résumé
BACKGROUND
Parasite infections can have substantial impacts on population dynamics and are accordingly a key challenge for wild population management. Here we studied genetic mechanisms driving parasite resistance in a large herbivore through a comprehensive approach combining measurements of neutral (16 microsatellites) and adaptive (MHC DRB1 exon 2) genetic diversity and two types of gastrointestinal parasites (nematodes and coccidia).
RESULTS
While accounting for other extrinsic and intrinsic predictors known to impact parasite load, we show that both neutral genetic diversity and DRB1 are associated with resistance to gastrointestinal nematodes. Intermediate levels of multi-locus heterozygosity maximized nematodes resistance, suggesting that both in- and outbreeding depression might occur in the population. DRB1 heterozygosity and specific alleles effects were detected, suggesting the occurrence of heterozygote advantage, rare-allele effects and/or fluctuating selection. On the contrary, no association was detected between genetic diversity and resistance to coccidia, indicating that different parasite classes are impacted by different genetic drivers.
CONCLUSIONS
This study provides important insights for large herbivores and wild sheep pathogen management, and in particular suggests that factors likely to impact genetic diversity and allelic frequencies, including global changes, are also expected to impact parasite resistance.
Identifiants
pubmed: 30836982
doi: 10.1186/s12898-019-0228-x
pii: 10.1186/s12898-019-0228-x
pmc: PMC6402107
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
12Références
Parasite Immunol. 2016 Sep;38(9):527-34
pubmed: 27426017
Mol Ecol. 2007 Jun;16(12):2474-87
pubmed: 17561907
Mol Ecol. 2014 Apr;23(8):1899-909
pubmed: 24581039
Vet Rec. 2014 Sep 13;175(10):250-5
pubmed: 25217603
Heredity (Edinb). 2014 Mar;112(3):240-7
pubmed: 24149650
PLoS One. 2018 Mar 14;13(3):e0192825
pubmed: 29538393
Front Genet. 2015 Mar 24;6:105
pubmed: 25852746
Res Vet Sci. 2005 Dec;79(3):191-6
pubmed: 16054889
Proc Biol Sci. 2009 Oct 7;276(1672):3477-85
pubmed: 19586947
PLoS One. 2017 May 2;12(5):e0176960
pubmed: 28464013
J Evol Biol. 2017 Nov;30(11):1953-1965
pubmed: 28787533
J Evol Biol. 2014 Dec;27(12):2807-19
pubmed: 25370831
Parasitol Res. 2011 Dec;109(6):1483-500
pubmed: 21842390
Biol Lett. 2008 Apr 23;4(2):228-31
pubmed: 18270161
Evolution. 1999 Aug;53(4):1259-1267
pubmed: 28565537
Rev Sci Tech. 2010 Aug;29(2):329-50
pubmed: 20919586
Mol Ecol. 2013 Feb;22(3):757-73
pubmed: 22998224
Science. 1998 Dec 18;282(5397):2256-8
pubmed: 9856948
Int J Parasitol. 2007 Jan;37(1):121-9
pubmed: 17067607
Evolution. 2001 Mar;55(3):616-25
pubmed: 11327168
Parasite Immunol. 2013 Nov;35(11):362-73
pubmed: 23855786
Mol Ecol Resour. 2014 May;14(3):519-30
pubmed: 24314098
Vet Parasitol. 2003 Jul 25;115(2):147-66
pubmed: 12878420
Vet Parasitol. 2012 Sep 30;189(1):8-14
pubmed: 22494941
Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10896-9
pubmed: 1438295
Oecologia. 2003 Oct;137(2):286-95
pubmed: 12898385
Front Zool. 2005 Oct 20;2:16
pubmed: 16242022
Genetics. 2007 Aug;176(4):2501-8
pubmed: 17603099
Parasitology. 2007 Jan;134(Pt 1):23-31
pubmed: 16948876
Proc Biol Sci. 2010 Apr 7;277(1684):979-88
pubmed: 20071384
Mol Ecol. 2014 Oct;23(20):5072-88
pubmed: 25211523
Animal. 2012 May;6(5):741-7
pubmed: 22558922
Ecol Evol. 2017 Nov 16;7(22):9580-9591
pubmed: 29187991
Parasite Immunol. 2016 Sep;38(9):569-86
pubmed: 27387842
Proc Natl Acad Sci U S A. 2004 Feb 24;101(8):2381-5
pubmed: 14983018
BMC Ecol. 2011 Feb 01;11:5
pubmed: 21284886
Vet Parasitol. 2011 May 11;177(3-4):339-44
pubmed: 21208746
J Evol Biol. 2007 Jan;20(1):79-86
pubmed: 17210002
Evolution. 2010 May;64(5):1202-17
pubmed: 20148954
Biol Lett. 2005 Mar 22;1(1):105-7
pubmed: 17148140
Mol Ecol. 2009 Mar;18(6):1112-23
pubmed: 19222748
Evolution. 2007 Jun;61(6):1339-52
pubmed: 17542844
Mol Ecol. 2010 Apr;19(7):1324-34
pubmed: 20298469
Proc Biol Sci. 2009 Mar 22;276(1659):1119-28
pubmed: 19129114
Trends Ecol Evol. 2010 Apr;25(4):207-14
pubmed: 19897275
Animal. 2010 Mar;4(3):377-92
pubmed: 22443942
Ann Parasitol Hum Comp. 1970 May-Jun;45(3):321-42
pubmed: 5531507
Nature. 1975 Jul 3;256(5512):50-2
pubmed: 1079575
Nat Rev Genet. 2014 Jan;15(1):56-62
pubmed: 24322726
Mol Ecol. 2011 Oct;20(19):3949-52
pubmed: 21951418
Heredity (Edinb). 2006 Jan;96(1):7-21
pubmed: 16094301
Mol Ecol. 2005 Nov;14(13):4159-68
pubmed: 16262866
Evolution. 2011 Nov;65(11):3175-94
pubmed: 22023584
Sci Rep. 2017 Oct 20;7(1):13700
pubmed: 29057949
Parasit Vectors. 2013 May 27;6:153
pubmed: 23711194
J Evol Biol. 2003 May;16(3):363-77
pubmed: 14635837
J Vet Med B Infect Dis Vet Public Health. 2001 Nov;48(9):665-73
pubmed: 11765802
Mol Ecol. 2008 Sep;17(17):3808-17
pubmed: 18647238
Parasitology. 1995;111 Suppl:S3-14
pubmed: 8632922
Heredity (Edinb). 2001 Apr;86(Pt 4):439-50
pubmed: 11520344
Science. 2000 Jan 21;287(5452):443-9
pubmed: 10642539
Int J Parasitol. 1995 Jul;25(7):815-22
pubmed: 7558567
Am Nat. 2010 Nov;176(5):613-24
pubmed: 20849271
Mol Ecol. 2009 Jul;18(13):2746-65
pubmed: 19500255
Parasitology. 2001;122 Suppl:S23-38
pubmed: 11442193
N Z Vet J. 2006 Aug;54(4):153-60
pubmed: 16915336
Immunol Rev. 1995 Feb;143:181-97
pubmed: 7558076
Mol Ecol. 2015 Apr;24(7):1419-32
pubmed: 25728376
Parasitology. 2016 Jul;143(8):983-97
pubmed: 27046508
Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3714-9
pubmed: 9520432
Proc Biol Sci. 2015 Jan 07;282(1798):20141873
pubmed: 25392468
Exp Appl Acarol. 2018 Feb;74(2):159-169
pubmed: 29460092
PLoS One. 2017 Apr 7;12(4):e0175385
pubmed: 28388681
Mol Ecol. 2016 Oct;25(19):4730-44
pubmed: 27485035
Parasitology. 1992 Dec;105 ( Pt 3):493-503
pubmed: 1461688
J Anim Ecol. 2017 Mar;86(2):371-383
pubmed: 27981576
Vet Parasitol. 2010 Jan 20;167(1):55-61
pubmed: 19850412
J Hered. 2005 Mar-Apr;96(2):85-8
pubmed: 15618305
Trends Parasitol. 2016 Jun;32(6):470-480
pubmed: 27183838
Mol Ecol. 2011 Oct;20(19):4028-41
pubmed: 21714823
J Evol Biol. 2016 Mar;29(3):617-32
pubmed: 26687843
Science. 1982 Oct 22;218(4570):384-7
pubmed: 7123238
Heredity (Edinb). 2007 Sep;99(3):265-77
pubmed: 17519969
Parasitology. 2001 May;122(Pt 5):571-82
pubmed: 11393831
Mol Ecol Resour. 2018 May;18(3):474-489
pubmed: 29288544
Mol Ecol. 2003 Mar;12(3):733-42
pubmed: 12675828
Mol Ecol. 2012 Mar;21(5):1271-82
pubmed: 22289112
Science. 2003 Sep 5;301(5638):1343
pubmed: 12958352
Mol Ecol. 2002 Dec;11(12):2467-74
pubmed: 12453232
PLoS One. 2012;7(9):e45404
pubmed: 23049796
Evol Appl. 2016 Dec 20;10(2):199-211
pubmed: 28127396
Sci Rep. 2017 Nov 15;7(1):15592
pubmed: 29142204
Mol Ecol. 2010 Mar;19 Suppl 1:255-65
pubmed: 20331784
Behav Processes. 1992;26(2-3):155-65
pubmed: 24924325
Vet Parasitol. 2016 Mar 15;218:5-9
pubmed: 26872921
Anim Genet. 1991;22(3):199-209
pubmed: 1928826
Evol Appl. 2016 Jun 03;9(6):805-17
pubmed: 27330556
BMC Ecol. 2014 Nov 12;14:27
pubmed: 25388877
Immunogenetics. 2008 Dec;60(12):749-58
pubmed: 18797863
Curr Biol. 2006 Sep 19;16(18):R790-1; author reply R791-2
pubmed: 16979542
Mol Ecol Resour. 2012 Nov;12(6):1151-7
pubmed: 22823139
Mol Ecol. 2007 Feb;16(3):463-75
pubmed: 17257106
Vet Parasitol. 2000 Jun 10;90(1-2):111-8
pubmed: 10828517
J Evol Biol. 2008 Sep;21(5):1307-20
pubmed: 18624885
Genet Mol Res. 2006 Oct 31;5(4):581-608
pubmed: 17183471
Mol Ecol. 2007 Sep;16(17):3712-20
pubmed: 17845443
Rev Sci Tech. 1993 Mar;12(1):115-35
pubmed: 8518439
Parasitology. 2009 Sep;136(11):1357-65
pubmed: 19660155
Mol Ecol. 2005 Sep;14(10):3209-17
pubmed: 16101786
Oecologia. 2011 Nov;167(3):635-46
pubmed: 21607671
Parasite Immunol. 2008 Feb;30(2):63-70
pubmed: 18186766
Mol Ecol. 2007 Nov;16(22):4858-66
pubmed: 17944853
Proc Biol Sci. 2004 Dec 7;271 Suppl 6:S471-3
pubmed: 15801607
Genetics. 2008 Nov;180(3):1593-608
pubmed: 18791233
J Evol Biol. 2014 Nov;27(11):2468-82
pubmed: 25264126
Ecol Lett. 2017 Oct;20(10):1325-1336
pubmed: 28871636