Selective sorting of ancestral introgression in maize and teosinte along an elevational cline.
Journal
PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
received:
11
08
2021
accepted:
07
09
2021
revised:
21
10
2021
pubmed:
12
10
2021
medline:
1
12
2021
entrez:
11
10
2021
Statut:
epublish
Résumé
While often deleterious, hybridization can also be a key source of genetic variation and pre-adapted haplotypes, enabling rapid evolution and niche expansion. Here we evaluate these opposing selection forces on introgressed ancestry between maize (Zea mays ssp. mays) and its wild teosinte relative, mexicana (Zea mays ssp. mexicana). Introgression from ecologically diverse teosinte may have facilitated maize's global range expansion, in particular to challenging high elevation regions (> 1500 m). We generated low-coverage genome sequencing data for 348 maize and mexicana individuals to evaluate patterns of introgression in 14 sympatric population pairs, spanning the elevational range of mexicana, a teosinte endemic to the mountains of Mexico. While recent hybrids are commonly observed in sympatric populations and mexicana demonstrates fine-scale local adaptation, we find that the majority of mexicana ancestry tracts introgressed into maize over 1000 generations ago. This mexicana ancestry seems to have maintained much of its diversity and likely came from a common ancestral source, rather than contemporary sympatric populations, resulting in relatively low FST between mexicana ancestry tracts sampled from geographically distant maize populations. Introgressed mexicana ancestry in maize is reduced in lower-recombination rate quintiles of the genome and around domestication genes, consistent with pervasive selection against introgression. However, we also find mexicana ancestry increases across the sampled elevational gradient and that high introgression peaks are most commonly shared among high-elevation maize populations, consistent with introgression from mexicana facilitating adaptation to the highland environment. In the other direction, we find patterns consistent with adaptive and clinal introgression of maize ancestry into sympatric mexicana at many loci across the genome, suggesting that maize also contributes to adaptation in mexicana, especially at the lower end of its elevational range. In sympatric maize, in addition to high introgression regions we find many genomic regions where selection for local adaptation maintains steep gradients in introgressed mexicana ancestry across elevation, including at least two inversions: the well-characterized 14 Mb Inv4m on chromosome 4 and a novel 3 Mb inversion Inv9f surrounding the macrohairless1 locus on chromosome 9. Most outlier loci with high mexicana introgression show no signals of sweeps or local sourcing from sympatric populations and so likely represent ancestral introgression sorted by selection, resulting in correlated but distinct outcomes of introgression in different contemporary maize populations.
Identifiants
pubmed: 34634032
doi: 10.1371/journal.pgen.1009810
pii: PGENETICS-D-21-01078
pmc: PMC8530355
doi:
Banques de données
figshare
['10.6084/m9.figshare.16641799']
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1009810Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM108779
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM136290
Pays : United States
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Genetics. 2004 Aug;167(4):1949-59
pubmed: 15342532
G3 (Bethesda). 2018 Feb 2;8(2):551-566
pubmed: 29196497
Genetics. 1992 Oct;132(2):583-9
pubmed: 1427045
Nat Rev Genet. 2013 Dec;14(12):840-52
pubmed: 24240513
PLoS Genet. 2020 Dec 3;16(12):e1009213
pubmed: 33270639
Science. 2003 Aug 29;301(5637):1211-6
pubmed: 12907807
Nat Genet. 2012 May 13;44(6):720-4
pubmed: 22581231
Front Plant Sci. 2018 Jun 28;9:886
pubmed: 30002665
Genetics. 2006 Jan;172(1):519-31
pubmed: 16204211
Science. 2010 Jul 2;329(5987):75-8
pubmed: 20595611
PLoS Genet. 2014 Jun 26;10(6):e1004410
pubmed: 24967630
Heredity (Edinb). 2015 Jun;114(6):552-63
pubmed: 25585918
Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):2101-3
pubmed: 11172082
PLoS Genet. 2021 Feb 22;17(2):e1009095
pubmed: 33617525
PLoS Genet. 2019 Dec 20;15(12):e1008512
pubmed: 31860672
Genetics. 2016 Apr;202(4):1485-501
pubmed: 26857625
Proc Biol Sci. 2016 Sep 28;283(1839):
pubmed: 27683368
Genetics. 1991 Sep;129(1):285-95
pubmed: 1682215
Evolution. 2015 Jun;69(6):1406-1422
pubmed: 25929355
Science. 1993 Oct 8;262(5131):233-5
pubmed: 17841871
Science. 2009 Nov 20;326(5956):1112-5
pubmed: 19965430
Nature. 2017 Jun 22;546(7659):524-527
pubmed: 28605751
Nat Commun. 2019 Feb 25;10(1):923
pubmed: 30804385
Nature. 2014 Mar 20;507(7492):354-7
pubmed: 24476815
PLoS Genet. 2013 May;9(5):e1003477
pubmed: 23671421
Mol Ecol. 2010 Apr;19(7):1296-311
pubmed: 20196812
Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12959-62
pubmed: 12244216
Genetics. 2013 Apr;193(4):1233-54
pubmed: 23410830
PLoS Biol. 2016 Feb 12;14(2):e1002379
pubmed: 26871574
Nat Commun. 2019 Aug 23;10(1):3810
pubmed: 31444327
Mol Ecol. 2019 Jun;28(11):2814-2830
pubmed: 30980686
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Genome Biol. 2017 Nov 13;18(1):215
pubmed: 29132403
Mol Ecol. 2010 Mar;19(6):1162-73
pubmed: 20163543
Nat Rev Genet. 2010 Mar;11(3):175-80
pubmed: 20051985
Nature. 1997 Apr 3;386(6624):485-8
pubmed: 9087405
PLoS Genet. 2020 May 14;16(5):e1008791
pubmed: 32407310
Gene. 1998 Nov 26;223(1-2):321-32
pubmed: 9858759
Bioinformatics. 2012 Oct 1;28(19):2520-2
pubmed: 22908215
Nat Genet. 2015 Dec;47(12):1489-93
pubmed: 26523777
PLoS Biol. 2019 Feb 7;17(2):e2006288
pubmed: 30730876
Genome Biol Evol. 2013;5(9):1594-609
pubmed: 23902747
Trends Genet. 2012 Dec;28(12):606-15
pubmed: 23021022
Nature. 2004 Dec 2;432(7017):630-5
pubmed: 15577912
Evolution. 2019 Nov;73(11):2230-2246
pubmed: 31389004
Science. 2020 May 15;368(6492):731-736
pubmed: 32409469
Genome Res. 2013 Sep;23(9):1514-21
pubmed: 23861382
Nature. 2005 Aug 25;436(7054):1119-26
pubmed: 16041362
Genetics. 2004 Mar;166(3):1451-61
pubmed: 15082562
New Phytol. 2018 Oct;220(2):395-408
pubmed: 30035321
Mol Ecol. 2016 Jun;25(11):2499-517
pubmed: 27038381
J Hered. 2018 Mar 16;109(3):333-338
pubmed: 28992108
Plant Physiol. 1994 Jul;105(3):881-9
pubmed: 8058838
Science. 2018 May 11;360(6389):656-660
pubmed: 29674434
Genetics. 1993 Jun;134(2):559-70
pubmed: 8325489
PeerJ. 2019 May 3;7:e6815
pubmed: 31110920
PLoS Genet. 2013 Jun;9(6):e1003604
pubmed: 23825971
Genetics. 2018 Oct;210(2):719-731
pubmed: 30131346
Proc Natl Acad Sci U S A. 2009 Mar 31;106(13):5019-24
pubmed: 19307570
Mol Biol Evol. 2019 Sep 1;36(9):1975-1989
pubmed: 31225876
Nucleic Acids Res. 2019 Jan 8;47(D1):D1146-D1154
pubmed: 30407532
New Phytol. 2019 Feb;221(3):1279-1288
pubmed: 30368812
Science. 2009 Aug 7;325(5941):714-8
pubmed: 19661422
Genetics. 2009 Apr;181(4):1399-413
pubmed: 19153259
Genetics. 2016 Jun;203(2):881-91
pubmed: 27038113
Genetics. 2013 Nov;195(3):693-702
pubmed: 24026093
Plant J. 2016 Jun;86(5):391-402
pubmed: 27012534
PLoS Genet. 2016 Nov 8;12(11):e1006340
pubmed: 27824859
Annu Rev Genet. 2004;38:37-59
pubmed: 15568971
PLoS One. 2018 Feb 16;13(2):e0192676
pubmed: 29451888
Science. 2015 Jan 2;347(6217):1258524
pubmed: 25431491
Science. 2010 May 7;328(5979):710-722
pubmed: 20448178
Genetics. 2005 Apr;169(4):2241-54
pubmed: 15687282
Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9161-6
pubmed: 11470895
F1000Res. 2018 Aug 24;7:1338
pubmed: 30254741
BMC Bioinformatics. 2014 Nov 25;15:356
pubmed: 25420514
Mol Ecol. 2017 May;26(10):2738-2756
pubmed: 28256021
Nature. 2005 Aug 4;436(7051):714-9
pubmed: 16079849
Genetics. 2019 Nov;213(3):771-787
pubmed: 31527048
Proc Natl Acad Sci U S A. 2020 Oct 13;117(41):25618-25627
pubmed: 32989136
PLoS Genet. 2017 Jan 3;13(1):e1006529
pubmed: 28045893
Proc Natl Acad Sci U S A. 2017 Jul 3;114(27):7061-7066
pubmed: 28634295
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
PLoS Genet. 2018 Apr 12;14(4):e1007130
pubmed: 29649209
Curr Biol. 2019 Jul 22;29(14):R705-R714
pubmed: 31336092
Proc Natl Acad Sci U S A. 2019 Mar 19;116(12):5643-5652
pubmed: 30842282
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278
PLoS Genet. 2011 Apr;7(4):e1001373
pubmed: 21533020
Genetics. 1995 Sep;141(1):333-46
pubmed: 8536981
Evolution. 2013 Nov;67(11):3258-73
pubmed: 24102455
Elife. 2015 Mar 25;4:
pubmed: 25807085
Science. 2019 Nov 1;366(6465):594-599
pubmed: 31672890
PLoS One. 2012;7(8):e43450
pubmed: 22912876
Bioinformatics. 2011 Apr 15;27(8):1157-8
pubmed: 21320865