Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila.


Journal

PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074

Informations de publication

Date de publication:
02 2019
Historique:
received: 02 08 2018
accepted: 16 12 2018
entrez: 13 2 2019
pubmed: 13 2 2019
medline: 12 3 2019
Statut: epublish

Résumé

Most of the current knowledge on the genetic basis of adaptive evolution is based on the analysis of single nucleotide polymorphisms (SNPs). Despite increasing evidence for their causal role, the contribution of structural variants to adaptive evolution remains largely unexplored. In this work, we analyzed the population frequencies of 1,615 Transposable Element (TE) insertions annotated in the reference genome of Drosophila melanogaster, in 91 samples from 60 worldwide natural populations. We identified a set of 300 polymorphic TEs that are present at high population frequencies, and located in genomic regions with high recombination rate, where the efficiency of natural selection is high. The age and the length of these 300 TEs are consistent with relatively young and long insertions reaching high frequencies due to the action of positive selection. Besides, we identified a set of 21 fixed TEs also likely to be adaptive. Indeed, we, and others, found evidence of selection for 84 of these reference TE insertions. The analysis of the genes located nearby these 84 candidate adaptive insertions suggested that the functional response to selection is related with the GO categories of response to stimulus, behavior, and development. We further showed that a subset of the candidate adaptive TEs affects expression of nearby genes, and five of them have already been linked to an ecologically relevant phenotypic effect. Our results provide a more complete understanding of the genetic variation and the fitness-related traits relevant for adaptive evolution. Similar studies should help uncover the importance of TE-induced adaptive mutations in other species as well.

Identifiants

pubmed: 30753202
doi: 10.1371/journal.pgen.1007900
pii: PGENETICS-D-18-01558
pmc: PMC6372155
doi:

Substances chimiques

DNA Transposable Elements 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1007900

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM089926
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM118165
Pays : United States

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Proc Natl Acad Sci U S A. 2015 Nov 3;112(44):E6010-9
pubmed: 26483487
Mol Ecol. 2019 Mar;28(6):1506-1522
pubmed: 30506554
Mol Biol Evol. 1998 Nov;15(11):1562-7
pubmed: 12572619
Science. 2016 Feb 12;351(6274):aac7247
pubmed: 26912865
PLoS One. 2011 Jan 31;6(1):e16526
pubmed: 21304975
Curr Opin Plant Biol. 2017 Apr;36:88-94
pubmed: 28242535
Mol Biol Evol. 2020 Sep 1;37(9):2661-2678
pubmed: 32413142
Annu Rev Genet. 2014;48:561-81
pubmed: 25292358
PLoS Genet. 2016 Aug 12;12(8):e1006249
pubmed: 27517860
Genetics. 2014 Feb;196(2):523-38
pubmed: 24336751
PLoS Biol. 2008 Oct 21;6(10):e251
pubmed: 18942889
Mol Biol Evol. 2017 Feb 1;34(2):349-360
pubmed: 27777283
Genome Biol. 2008;9(2):R39
pubmed: 18291035
Bioinformatics. 2017 Sep 01;33(17):2779-2780
pubmed: 28472360
J Insect Physiol. 2017 Apr;98:267-274
pubmed: 28161445
Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
pubmed: 12136088
PLoS Genet. 2015 Feb 23;11(2):e1005004
pubmed: 25706129
Proc Natl Acad Sci U S A. 2007 Jul 3;104(27):11340-5
pubmed: 17592135
Nat Protoc. 2009;4(1):44-57
pubmed: 19131956
PLoS One. 2014 May 02;9(5):e91929
pubmed: 24786468
PLoS Genet. 2010 Jun 24;6(6):e1000998
pubmed: 20585622
Curr Opin Genet Dev. 2014 Dec;29:1-8
pubmed: 25129844
Elife. 2016 Jun 03;5:
pubmed: 27258693
Nucleic Acids Res. 2017 Jan 4;45(D1):D663-D671
pubmed: 27799470
Science. 2002 Sep 27;297(5590):2253-6
pubmed: 12351787
Mol Ecol. 2013 Oct;22(20):5084-97
pubmed: 24102956
Mol Biol Evol. 2014 May;31(5):1275-91
pubmed: 24554778
Mol Biol Evol. 2011 May;28(5):1633-44
pubmed: 21172826
Bioinformatics. 2012 May 15;28(10):1353-8
pubmed: 22492648
Gene. 2010 Sep 1;463(1-2):18-20
pubmed: 20452408
Nat Rev Genet. 2010 Oct;11(10):665-7
pubmed: 20838407
PLoS Genet. 2014 Nov 06;10(11):e1004775
pubmed: 25375361
Curr Opin Insect Sci. 2019 Feb;31:70-76
pubmed: 31109676
Proc Natl Acad Sci U S A. 2003 May 27;100(11):6569-74
pubmed: 12743378
PLoS Genet. 2014 Aug 14;10(8):e1004560
pubmed: 25122208
Mol Biol Evol. 2010 Jun;27(6):1226-34
pubmed: 20150340
Science. 2016 Mar 4;351(6277):1083-7
pubmed: 26941318
Genetics. 2007 Mar;175(3):1071-7
pubmed: 17179088
Mol Biol Evol. 2014 Oct;31(10):2824-7
pubmed: 25015648
Mol Biol Evol. 2004 Apr;21(4):670-80
pubmed: 14739245
Mol Ecol. 2013 Mar;22(6):1503-17
pubmed: 23293987
Nature. 2012 Feb 08;482(7384):173-8
pubmed: 22318601
PLoS Biol. 2006 Mar;4(3):e72
pubmed: 16494531
Nucleic Acids Res. 2016 Jan 4;44(D1):D786-92
pubmed: 26467478
Genetics. 2015 Jan;199(1):85-93
pubmed: 25335504
PLoS Comput Biol. 2005 Jul;1(2):166-75
pubmed: 16110336
Science. 2016 Oct 7;354(6308):54-59
pubmed: 27846491
PLoS Genet. 2013 Jun;9(6):e1003534
pubmed: 23754958
Genetics. 2010 Aug;185(4):1411-23
pubmed: 20516501
PLoS Genet. 2012;8(12):e1003080
pubmed: 23284287
Mol Biol Evol. 2015 Jul;32(7):1800-14
pubmed: 25862139
PLoS Genet. 2012;8(10):e1002905
pubmed: 23071443
Nucleic Acids Res. 2015 Feb 27;43(4):e22
pubmed: 25510498
Philos Trans R Soc Lond B Biol Sci. 2010 Apr 27;365(1544):1229-39
pubmed: 20308098
Mol Biol Evol. 2016 May;33(5):1317-36
pubmed: 26796550
Genome Res. 2014 Jul;24(7):1193-208
pubmed: 24714809
Biol Direct. 2011 Mar 17;6:19
pubmed: 21414203
Sci Rep. 2017 Feb 20;7:42663
pubmed: 28218276
Elife. 2016 Dec 02;5:
pubmed: 27911260
Am Nat. 2016 Oct;188(4):379-97
pubmed: 27622873
Genome Biol. 2002;3(12):RESEARCH0084
pubmed: 12537573
Bioinformatics. 2011 Aug 1;27(15):2156-8
pubmed: 21653522
Syst Biol. 2003 Oct;52(5):696-704
pubmed: 14530136
Nat Rev Genet. 2017 Feb;18(2):71-86
pubmed: 27867194
Mol Ecol. 2012 Oct;21(19):4748-69
pubmed: 22913798
Sci Rep. 2018 Nov 1;8(1):16143
pubmed: 30385770
Genetics. 2014 May;197(1):1-18
pubmed: 24653003
Genetics. 2014 May;197(1):361-73
pubmed: 24610860
BMC Genomics. 2014 Jun 26;15:526
pubmed: 24964727
Genet Res. 1966 Dec;8(3):269-94
pubmed: 5980116
Nat Genet. 2018 Jan;50(1):20-25
pubmed: 29255259
Mol Biol Evol. 2009 Sep;26(9):1949-61
pubmed: 19458110
PLoS Genet. 2006 Oct 13;2(10):e166
pubmed: 17040129
Proc Natl Acad Sci U S A. 2011 Dec 20;108(51):20666-71
pubmed: 22143780
Nucleic Acids Res. 2009 Jan;37(1):1-13
pubmed: 19033363
Genome Res. 2015 Mar;25(3):445-58
pubmed: 25589440
Bioinformatics. 2010 Jul 1;26(13):1669-70
pubmed: 20472542
G3 (Bethesda). 2015 Feb 11;5(4):593-603
pubmed: 25673134
Mol Biol Evol. 2016 Dec;33(12):3308-3313
pubmed: 27687565
Mol Ecol. 2014 Apr;23(8):2020-30
pubmed: 24629106
Genetics. 2015 Apr;199(4):1229-41
pubmed: 25631317
PLoS Genet. 2012 Jan;8(1):e1002487
pubmed: 22291611
Mob Genet Elements. 2017 Jan 11;7(1):1-20
pubmed: 28228978
Genetics. 2011 Jan;187(1):245-60
pubmed: 21059887
Methods Mol Biol. 2012;855:361-83
pubmed: 22407716
Genetics. 1995 Dec;141(4):1605-17
pubmed: 8601498
Mol Ecol. 2016 Jan;25(2):454-69
pubmed: 26671840
Nucleic Acids Res. 2015 Dec 15;43(22):10655-72
pubmed: 26578579
Genetics. 1993 Aug;134(4):1289-303
pubmed: 8375663
Evolution. 1984 Nov;38(6):1358-1370
pubmed: 28563791
Mol Biol Evol. 2016 Feb;33(2):442-55
pubmed: 26494843
Methods Ecol Evol. 2015 Apr;6(4):445-464
pubmed: 25937885
Science. 2005 Jul 29;309(5735):764-7
pubmed: 16051794
Mol Ecol. 2016 Mar;25(5):1157-74
pubmed: 26547394
Trends Genet. 1988 Apr;4(4):106-11
pubmed: 3149056
Mol Biol Evol. 2003 Jun;20(6):880-92
pubmed: 12716993
Curr Opin Genet Dev. 2016 Dec;41:44-52
pubmed: 27584858
Genetics. 2015 Dec;201(4):1555-79
pubmed: 26482796
G3 (Bethesda). 2017 Aug 7;7(8):2763-2778
pubmed: 28637810
PLoS Genet. 2010 Apr 08;6(4):e1000905
pubmed: 20386746
Genet Res. 1974 Feb;23(1):23-35
pubmed: 4407212
Genetics. 1989 Nov;123(3):585-95
pubmed: 2513255
Nat Methods. 2011 Dec 04;9(2):179-81
pubmed: 22138821
Nucleic Acids Res. 1997 Dec 15;25(24):4876-82
pubmed: 9396791
Aging (Albany NY). 2014 Jan;6(1):58-69
pubmed: 24519859
Mol Ecol. 2018 Mar;27(6):1342-1356
pubmed: 29524276
Genet Res. 1987 Feb;49(1):31-41
pubmed: 3032743
Proc Natl Acad Sci U S A. 2014 Jun 3;111(22):8131-6
pubmed: 24847061

Auteurs

Gabriel E Rech (GE)

Institute of Evolutionary Biology (IBE), CSIC-Universitat Pompeu Fabra, Barcelona, Spain.

María Bogaerts-Márquez (M)

Institute of Evolutionary Biology (IBE), CSIC-Universitat Pompeu Fabra, Barcelona, Spain.

Maite G Barrón (MG)

Institute of Evolutionary Biology (IBE), CSIC-Universitat Pompeu Fabra, Barcelona, Spain.

Miriam Merenciano (M)

Institute of Evolutionary Biology (IBE), CSIC-Universitat Pompeu Fabra, Barcelona, Spain.

José Luis Villanueva-Cañas (JL)

Institute of Evolutionary Biology (IBE), CSIC-Universitat Pompeu Fabra, Barcelona, Spain.

Vivien Horváth (V)

Institute of Evolutionary Biology (IBE), CSIC-Universitat Pompeu Fabra, Barcelona, Spain.

Anna-Sophie Fiston-Lavier (AS)

Institut des Sciences de l'Evolution de Montpellier (UMR 5554, CNRS-UM-IRD-EPHE), Université de Montpellier, Place Eugène Bataillon, Montpellier, France.

Isabelle Luyten (I)

URGI, INRA, Université Paris-Saclay, Versailles, France.

Sandeep Venkataram (S)

Department of Biology, Stanford University, Stanford, CA, United States of America.

Hadi Quesneville (H)

URGI, INRA, Université Paris-Saclay, Versailles, France.

Dmitri A Petrov (DA)

Department of Biology, Stanford University, Stanford, CA, United States of America.

Josefa González (J)

Institute of Evolutionary Biology (IBE), CSIC-Universitat Pompeu Fabra, Barcelona, Spain.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH