title: Starvation-associated genome restructuring can lead to reproductive isolation in yeast.
abstract: Knowledge of the mechanisms that lead to reproductive isolation is essential for understanding population structure and speciation. While several models have been advanced to explain post-mating reproductive isolation, experimental data supporting most are indirect. Laboratory investigations of this phenomenon are typically carried out under benign conditions, which result in low rates of genetic change unlikely to initiate reproductive isolation. Previously, we described an experimental system using the yeast Saccharomyces cerevisiae where starvation served as a proxy to any stress that decreases reproduction and/or survivorship. We showed that novel lineages with restructured genomes quickly emerged in starved populations, and that these survivors were more fit than their ancestors when re-starved. Here we show that certain yeast lineages that survive starvation have become reproductively isolated from their ancestor. We further demonstrate that reproductive isolation arises from genomic rearrangements, whose frequency in starving yeast is several orders of magnitude greater than an unstarved control. By contrast, the frequency of point mutations is less than 2-fold greater. In a particular case, we observe that a starved lineage becomes reproductively isolated as a direct result of the stress-related accumulation of a single chromosome. We recapitulate this result by demonstrating that introducing an extra copy of one or several chromosomes into naïve, i.e. unstarved, yeast significantly diminishes their fertility. This type of reproductive barrier, whether arising spontaneously or via genetic manipulation, can be removed by making a lineage euploid for the altered chromosomes. Our model provides direct genetic evidence that reproductive isolation can arise frequently in stressed populations via genome restructuring without the precondition of geographic isolation.
authors.affiliation: Division of Biological Sciences, University of Montana, Missoula, Montana, United States of America. evgueny.kroll@mso.umt.edu
authors.forename: Evgueny
authors.initials: E
authors.lastname: Kroll
authors.forename: Scott
authors.initials: S
authors.lastname: Coyle
authors.forename: Barbara
authors.initials: B
authors.lastname: Dunn
authors.forename: Gregory
authors.initials: G
authors.lastname: Koniges
authors.forename: Anthony
authors.initials: A
authors.lastname: Aragon
authors.forename: Jeremy
authors.initials: J
authors.lastname: Edwards
authors.forename: Frank
authors.initials: F
authors.lastname: Rosenzweig
mesh_terms: D016681:Genome, Fungal / Q000235:genetics*; D060047:Reproductive Isolation; D012441:Saccharomyces cerevisiae / Q000235:genetics / Q000502:physiology; D015003:Yeasts / Q000235:genetics* / Q000502:physiology
references.citation: Genetics. 1964 Sep;50:435-58
references.pmid: 14207709
references.citation: Proc Natl Acad Sci U S A. 1933 Apr;19(4):397-403
references.pmid: 16577530
references.citation: Int J Syst Evol Microbiol. 2000 Sep;50 Pt 5:1931-1942
references.pmid: 11034507
references.citation: Res Microbiol. 2000 Sep;151(7):583-90
references.pmid: 11037136
references.citation: Heredity (Edinb). 2009 Jan;102(1):39-44
references.pmid: 18648383
references.citation: J Bacteriol. 1994 Aug;176(16):5101-7
references.pmid: 8051023
references.citation: Crit Rev Biochem Mol Biol. 2007 Jul-Aug;42(4):247-58
references.pmid: 17687667
references.citation: Nat Genet. 2007 Oct;39(10):1273-7
references.pmid: 17828265
references.citation: Science. 1984 Nov 16;226(4676):792-801
references.pmid: 15739260
references.citation: J Bacteriol. 1999 Sep;181(18):5800-7
references.pmid: 10482523
references.citation: Cell. 2008 Dec 12;135(6):1065-73
references.pmid: 19070577
references.citation: Cell. 2000 Nov 22;103(5):723-31
references.pmid: 11114329
references.citation: Mol Biol Evol. 2008 Feb;25(2):310-8
references.pmid: 18032404
references.citation: Bioessays. 2000 Dec;22(12):1085-94
references.pmid: 11084624
references.citation: Curr Protoc Mol Biol. 2008 Apr;Chapter 13:Unit 13.2
references.pmid: 18425759
references.citation: Heredity (Edinb). 2012 Feb;108(2):87-95
references.pmid: 21829224
references.citation: J Mol Biol. 2006 Oct 27;363(3):660-72
references.pmid: 16997324
references.citation: Genome Biol. 2009;10(3):R25
references.pmid: 19261174
references.citation: J Evol Biol. 2003 May;16(3):429-37
references.pmid: 14635842
references.citation: Semin Cell Dev Biol. 2011 Oct;22(8):875-85
references.pmid: 21802523
references.citation: Nature. 1989 Nov 23;342(6248):396-401
references.pmid: 2555716
references.citation: BMC Genet. 2009 Jul 13;10:36
references.pmid: 19594932
references.citation: Trends Genet. 2000 Sep;16(9):395-403
references.pmid: 10973068
references.citation: Genetics. 2003 Dec;165(4):1745-59
references.pmid: 14704163
references.citation: FEMS Microbiol Lett. 2009 Apr;293(1):1-10
references.pmid: 19175410
references.citation: Genetics. 2003 Dec;165(4):2167-79
references.pmid: 14704195
references.citation: Heredity (Edinb). 2009 Jan;102(1):24-30
references.pmid: 18766201
references.citation: Genetics. 2006 Nov;174(3):1455-68
references.pmid: 16980391
references.citation: Genes Dev. 1998 Aug 15;12(16):2574-86
references.pmid: 9716409
references.citation: Genetics. 1999 Apr;151(4):1299-313
references.pmid: 10101158
references.citation: Science. 2003 Sep 26;301(5641):1908-11
references.pmid: 14512629
references.citation: Genetics. 1985 Jun;110(2):173-85
references.pmid: 3891508
references.citation: BMC Evol Biol. 2012 Apr 02;12:46
references.pmid: 22471618
references.citation: BMC Genomics. 2005 Apr 16;6:53
references.pmid: 15833139
references.citation: Nat Genet. 2000 Jul;25(3):333-7
references.pmid: 10888885
references.citation: Evolution. 1993 Dec;47(6):1637-1653
references.pmid: 28568007
references.citation: Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16144-9
references.pmid: 12446845
references.citation: PLoS Genet. 2011 Aug;7(8):e1002223
references.pmid: 21901104
references.citation: J Cell Biol. 1996 Apr;133(1):75-84
references.pmid: 8601615
references.citation: EXS. 1997;83:241-54
references.pmid: 9342852
references.citation: Genome Res. 2008 May;18(5):821-9
references.pmid: 18349386
references.citation: Proc Natl Acad Sci U S A. 2012 Dec 18;109(51):21010-5
references.pmid: 23197825
references.citation: Science. 2002 Nov 29;298(5599):1773-5
references.pmid: 12459586
references.citation: PLoS Genet. 2009 Aug;5(8):e1000625
references.pmid: 19714216
references.citation: Nature. 1990 Jul 5;346(6279):79-81
references.pmid: 2195353
references.citation: PLoS Genet. 2010 Jul 29;6(7):e1001038
references.pmid: 20686707
references.citation: Trends Genet. 1989 Feb;5(2):46-50
references.pmid: 2646795
references.citation: Genome Res. 2000 Apr;10(4):403-9
references.pmid: 10779481
references.citation: Genetics. 1991 Aug;128(4):695-701
references.pmid: 1916241
references.citation: PLoS Genet. 2008 Dec;4(12):e1000303
references.pmid: 19079573
references.citation: mBio. 2011 Jul 26;2(4):
references.pmid: 21791579
references.citation: Trends Genet. 2005 Dec;21(12):673-82
references.pmid: 16242204
references.citation: Cytogenet Genome Res. 2002;96(1-4):45-51
references.pmid: 12438779
references.citation: Methods Enzymol. 1991;194:1-863
references.pmid: 2005781
references.citation: Cell. 2011 Sep 16;146(6):889-903
references.pmid: 21925314
references.citation: Science. 1985 May 17;228(4701):823-4
references.pmid: 4001923
references.citation: Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8420-7
references.pmid: 9671692
references.citation: Curr Genet. 1992 Jul;22(1):13-9
references.pmid: 1611666
references.citation: Genetics. 1997 Oct;147(2):371-82
references.pmid: 9335579
references.citation: Genetics. 1998 Apr;148(4):1667-86
references.pmid: 9560386
references.citation: Mol Cell Biol. 1996 Nov;16(11):6110-20
references.pmid: 8887641
references.citation: Yeast. 1998 Jan 30;14(2):115-32
references.pmid: 9483801
references.citation: Genetics. 2008 Jun;179(2):737-46
references.pmid: 18558649
references.citation: Genetics. 1989 Oct;123(2):255-60
references.pmid: 2684744
references.citation: PLoS Genet. 2008 Oct 03;4(10):e1000208
references.pmid: 18833303
references.citation: Heredity (Edinb). 2011 Feb;106(2):348-56
references.pmid: 20531448
references.citation: Heredity (Edinb). 1999 Nov;83 ( Pt 5):503-8
references.pmid: 10620021
references.citation: Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):13875-9
references.pmid: 19667210
references.citation: Science. 2003 May 30;300(5624):1404-9
references.pmid: 12775833
references.citation: Mol Cell. 1998 Jul;2(1):9-22
references.pmid: 9702187
references.citation: Nature. 2007 May 31;447(7144):585-8
references.pmid: 17538619
references.citation: Nature. 2003 Mar 6;422(6927):68-72
references.pmid: 12621434
references.citation: Nature. 2011 Jul 20;475(7356):348-52
references.pmid: 21776081