Evolution of haploid and diploid populations reveals common, strong, and variable pleiotropic effects in non-home environments.

S. cerevisiae evolution evolutionary biology genetics genomics pleiotropy trade-offs yeast

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
20 10 2023
Historique:
received: 21 09 2023
accepted: 27 09 2023
medline: 8 11 2023
pubmed: 20 10 2023
entrez: 20 10 2023
Statut: epublish

Résumé

Adaptation is driven by the selection for beneficial mutations that provide a fitness advantage in the specific environment in which a population is evolving. However, environments are rarely constant or predictable. When an organism well adapted to one environment finds itself in another, pleiotropic effects of mutations that made it well adapted to its former environment will affect its success. To better understand such pleiotropic effects, we evolved both haploid and diploid barcoded budding yeast populations in multiple environments, isolated adaptive clones, and then determined the fitness effects of adaptive mutations in 'non-home' environments in which they were not selected. We find that pleiotropy is common, with most adaptive evolved lineages showing fitness effects in non-home environments. Consistent with other studies, we find that these pleiotropic effects are unpredictable: they are beneficial in some environments and deleterious in others. However, we do find that lineages with adaptive mutations in the same genes tend to show similar pleiotropic effects. We also find that ploidy influences the observed adaptive mutational spectra in a condition-specific fashion. In some conditions, haploids and diploids are selected with adaptive mutations in identical genes, while in others they accumulate mutations in almost completely disjoint sets of genes.

Identifiants

pubmed: 37861305
doi: 10.7554/eLife.92899
pii: 92899
pmc: PMC10629826
doi:
pii:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIGMS NIH HHS
ID : T32GM007276
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM110275
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM141828
Pays : United States
Organisme : NIGMS NIH HHS
ID : F32 GM122360-02
Pays : United States
Organisme : NIGMS NIH HHS
ID : F32 GM122360
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007276
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM118165
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM131824
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM104239
Pays : United States

Informations de copyright

© 2023, Chen, Johnson, Hérissant et al.

Déclaration de conflit d'intérêts

VC, MJ, LH, PH, DY, YL, AA, SH, DP, MD, GS No competing interests declared

Références

Science. 2008 Apr 18;320(5874):362-5
pubmed: 18420932
Curr Opin Genet Dev. 2015 Dec;35:33-9
pubmed: 26370471
PLoS Biol. 2022 May 27;20(5):e3001633
pubmed: 35622868
Genetics. 2014 Jun;197(2):451-65
pubmed: 24939991
Nature. 2000 Oct 12;407(6805):736-9
pubmed: 11048718
Science. 2011 Jun 3;332(6034):1190-2
pubmed: 21636771
Nat Rev Genet. 2015 Oct;16(10):567-82
pubmed: 26347030
Curr Opin Genet Dev. 2022 Aug;75:101943
pubmed: 35752001
Genomics. 2014 Dec;104(6 Pt A):399-405
pubmed: 25281774
Nature. 1983 Apr 7;302(5908):495-500
pubmed: 6339947
PLoS Genet. 2013 Nov;9(11):e1003972
pubmed: 24278038
EMBO Rep. 2019 Aug;20(8):e46992
pubmed: 31338963
Proc Natl Acad Sci U S A. 2007 May 15;104 Suppl 1:8649-54
pubmed: 17494741
Proc Natl Acad Sci U S A. 2012 Jan 31;109(5):1595-600
pubmed: 22307617
Nature. 2013 Aug 29;500(7464):571-4
pubmed: 23873039
mSphere. 2018 May 9;3(3):
pubmed: 29743200
Yeast. 1995 Jan;11(1):53-5
pubmed: 7762301
Nat Ecol Evol. 2020 Apr;4(4):601-611
pubmed: 32152531
Sci Rep. 2019 Feb 20;9(1):2328
pubmed: 30787483
Elife. 2015 Mar 25;4:
pubmed: 25806684
Cell. 2016 Sep 8;166(6):1585-1596.e22
pubmed: 27594428
Ecol Lett. 2019 Jun;22(6):1009-1018
pubmed: 30924583
PLoS Genet. 2019 Feb 15;15(2):e1007958
pubmed: 30768593
Science. 2016 Sep 9;353(6304):1147-51
pubmed: 27609891
PLoS Genet. 2011 Apr;7(4):e1002056
pubmed: 21552329
Elife. 2021 Oct 01;10:
pubmed: 34596043
Nat Genet. 2011 Dec 18;44(1):101-5
pubmed: 22179135
Curr Opin Genet Dev. 2022 Aug;75:101951
pubmed: 35797741
Nat Commun. 2015 Jan 20;6:6102
pubmed: 25600558
Genomics. 2014 Dec;104(6 Pt A):447-52
pubmed: 25263109
Nature. 2015 Mar 12;519(7542):181-6
pubmed: 25731169
Evolution. 2013 Jun;67(6):1573-81
pubmed: 23730752
PLoS Genet. 2021 Jan 25;17(1):e1009314
pubmed: 33493203
PLoS Genet. 2008 Dec;4(12):e1000303
pubmed: 19079573
Mol Biol Evol. 2021 Sep 27;38(10):4362-4375
pubmed: 34132791
Elife. 2020 Dec 02;9:
pubmed: 33263280
Genetics. 2022 May 31;221(2):
pubmed: 35435209
Genetics. 2005 Apr;169(4):1915-25
pubmed: 15716499
Science. 2004 Feb 6;303(5659):808-13
pubmed: 14764870
Science. 2011 Jun 3;332(6034):1193-6
pubmed: 21636772
Nat Commun. 2021 Aug 31;12(1):5193
pubmed: 34465770
Science. 2014 Jun 27;344(6191):1519-1522
pubmed: 24970088
Proc Natl Acad Sci U S A. 2011 Dec 20;108(51):20666-71
pubmed: 22143780
G3 (Bethesda). 2014 Mar 20;4(3):399-409
pubmed: 24368781
Curr Biol. 2021 Dec 6;31(23):5314-5326.e10
pubmed: 34699784
G3 (Bethesda). 2017 Jan 5;7(1):143-153
pubmed: 27821633
Science. 2012 Jan 27;335(6067):457-61
pubmed: 22282810
Nat Genet. 2002 Aug;31(4):400-4
pubmed: 12134146
Nat Genet. 2008 Dec;40(12):1499-504
pubmed: 19029899
Genetics. 2016 Jul;203(3):1401-13
pubmed: 27194750
Microb Genom. 2021 May;7(5):
pubmed: 33945454
Elife. 2021 Jan 27;10:
pubmed: 33501915
Elife. 2023 Oct 20;12:
pubmed: 37861305
PLoS Genet. 2022 Jun 15;18(6):e1009840
pubmed: 35704655
PLoS Genet. 2014 Jan;10(1):e1004041
pubmed: 24415948
Nature. 2017 Nov 2;551(7678):45-50
pubmed: 29045390
Science. 2019 Oct 25;366(6464):490-493
pubmed: 31649199
PLoS Biol. 2015 Nov 18;13(11):e1002299
pubmed: 26581035
Elife. 2021 Jan 19;10:
pubmed: 33464204
Curr Biol. 2018 Feb 19;28(4):515-525.e6
pubmed: 29429618
Nat Ecol Evol. 2019 Feb;3(2):293-301
pubmed: 30598529
Genome Res. 2014 Dec;24(12):2033-40
pubmed: 25079858
Evol Lett. 2022 May 26;6(3):266-279
pubmed: 35784450
Mol Biol Evol. 2017 Oct 1;34(10):2613-2626
pubmed: 28957501
Nat Ecol Evol. 2019 Nov;3(11):1539-1551
pubmed: 31611676

Auteurs

Vivian Chen (V)

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

Milo S Johnson (MS)

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States.
Quantitative Biology Initiative, Harvard University, Cambridge, United States.
NSF-Simons Center for Mathematical and Statistical Analysis of Biology, Harvard University, Boston, United States.

Lucas Hérissant (L)

Department of Genetics, Stanford University, Stanford, United States.

Parris T Humphrey (PT)

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States.

David C Yuan (DC)

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

Yuping Li (Y)

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

Atish Agarwala (A)

Department of Physics, Stanford University, Stanford, United States.

Samuel B Hoelscher (SB)

Department of Genetics, Stanford University, Stanford, United States.

Dmitri A Petrov (DA)

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

Michael M Desai (MM)

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States.
Quantitative Biology Initiative, Harvard University, Cambridge, United States.
NSF-Simons Center for Mathematical and Statistical Analysis of Biology, Harvard University, Boston, United States.
Department of Physics, Harvard University, Cambridge, United States.

Gavin Sherlock (G)

Department of Genetics, Stanford University, Stanford, United States.

Articles similaires

T-Lymphocytes, Regulatory Lung Neoplasms Proto-Oncogene Proteins p21(ras) Animals Humans

Pathogenic mitochondrial DNA mutations inhibit melanoma metastasis.

Spencer D Shelton, Sara House, Luiza Martins Nascentes Melo et al.
1.00
DNA, Mitochondrial Humans Melanoma Mutation Neoplasm Metastasis

Prevalence and implications of fragile X premutation screening in Thailand.

Areerat Hnoonual, Sunita Kaewfai, Chanin Limwongse et al.
1.00
Humans Fragile X Mental Retardation Protein Thailand Male Female
Humans Receptors, Antigen, T-Cell Proto-Oncogene Proteins p21(ras) Pancreatic Neoplasms T-Lymphocytes

Classifications MeSH